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==Chapter Seven - Determinate and Plastic Principles in Neuropsychological Development==
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{{DickersonMcGurk1982 header}}
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=Chapter Seven - Determinate and Plastic Principles in Neuropsychological Development=
  
 
Denis M. Parker  
 
Denis M. Parker  
  
  
Introduction  
+
==Introduction==
  
To those interested in the relationship between brain mechanisms and  
+
To those interested in the relationship between brain mechanisms and behaviour, study of the outcome of damage to the central nervous system currently provides the most useful information concerning the structural basis of cognition and action. Observation of the pattern of behavioural loss and the extent to which recovery is possible following specific brain injury enables differing models of brain organization to be specifically tested. In fact, this question of the pattern of loss and the extent of recovery lies at the heart of a controversy, between the advocates of functional localization and those who proposed a diffuse physical basis for cognitive functions, which began during the nineteenth century. Some investigators stressed the return of almost complete function following a transient period of loss (Flourens, 1824), or stressed the re- emergence of functions at a reduced level while denying that behavioural effects contingent on the damage were specifically related to the region destroyed (Goltz, 1892). These views were amplified during the present century by the experimental work of Lashley (1929) who argued that, excluding the primary sensory and motor areas of the cortex, the association areas contributed in a unified way to the performance of any complex skill—the well-known principle of Mass Action. The degree of functional loss that could be detected following brain damage was assumed to be determined by the extent, rather than the location, of damaged tissue. The results of Lashley’s experiments, together with his theoretical exposition of them, supported the views of Goldstein (1939) who regarded cognitive skills as a function of the entire organism. He saw the symptoms following brain damage as manifestations of a complex adaptive syndrome in which higher intellectual abilities, in particular the ability to abstract, were likely to be depressed. This general intellectual loss was likely to be seen in the patients’ failure on a variety of cognitive tasks, but particularly in linguistic skills since these demanded, more than other capabilities, the integrity of the entire brain. Holding views such as these, there was no problem in accounting for the return of functions after cerebral injury since the intact areas of the brain would continue to function in their usual way following an initial period of shock, although there would of course be a loss of efficiency. Factors such as the age of the subject at the time of injury were seen to play a part, and indeed one of Lashley’s students (Tsang, 1937) had provided evidence that proportionately equivalent lesions in adult and juvenile rats produced less impairment in the younger animals.
behaviour, study of the outcome of damage to the central nervous system  
 
currently provides the most useful information concerning the structural basis of  
 
cognition and action. Observation of the pattern of behavioural loss and the  
 
extent to which recovery is possible following specific brain injury enables  
 
differing models of brain organization to be specifically tested. In fact, this  
 
question of the pattern of loss and the extent of recovery lies at the heart of a  
 
controversy, between the advocates of functional localization and those who  
 
proposed a diffuse physical basis for cognitive functions, which began during the  
 
nineteenth century. Some investigators stressed the return of almost complete  
 
function following a transient period of loss (Flourens, 1824), or stressed the re-  
 
emergence of functions at a reduced level while denying that behavioural effects  
 
contingent on the damage were specifically related to the region destroyed  
 
(Goltz, 1892). These views were amplified during the present century by the  
 
experimental work of Lashley (1929) who argued that, excluding the primary  
 
sensory and motor areas of the cortex, the association areas contributed in a  
 
unified way to the performance of any complex skill—the well-known principle  
 
of Mass Action. The degree of functional loss that could be detected following  
 
brain damage was assumed to be determined by the extent, rather than the  
 
location, of damaged tissue. The results of Lashley’s experiments, together with  
 
his theoretical exposition of them, supported the views of Goldstein (1939) who  
 
  
 +
In contrast to models of the brain based on assumptions of global processing and diffuse representation, from the middle nineteenth century onwards evidence began to accumulate rapidly that restricted brain lesions often produced highly specific disorders in which the patients’ remaining spectrum of skills were relatively unaffected. Broca (1861) produced two cases in which the patients’ verbal expression was drastically impaired but whose comprehension of language appeared to be relatively good. Wernicke (1874) produced evidence that patients’ ability to comprehend and utter meaningful linguistic statements could be grossly impaired yet their pronunciation and rate of verbal output could remain unimpaired. Other descriptions followed of patients with restricted and often bizarre symptom complexes. Dejerine’s description (1892) of Mr. C is perhaps one of the classic cases. This patient, who had right visual field blindness, could nevertheless recognize objects and continue his everyday life. Despite apparently normal vision in his left visual field and the ability to speak and write normally, he was unable to read by sight even the sentences he had written himself a short while before. He was however able to ‘read’ by feeling the shapes of cut out letters. Other syndromes described included those of disordered motor planning (Leipmann, 1908), the inability to recognize objects (Lissauer, 1890), and the inability to recognize melody (Henschen, 1926). The list could be continued, but the importance of these cases was that they convinced a substantial number of investigators that the brain could not be organized in a diffuse equipotential manner but, on the contrary, must contain relatively specialized processors even for such uniquely human processes as the comprehension and generation of language.
  
203
+
Modern neuropsychology has moved away from the exclusive study of such rare and extraordinary cases to the systematic examination of groups of patients in which the behavioural effects of differences in known cerebral pathology can be investigated. The more extreme forms of cerebral localization have been rejected, but the acceptance of specialized processing within and between the two hemispheres of the brain has gained wide acceptance (see Walsh, 1978, and Hecaen and Albert, 1978). This current position regarding the distribution of functional systems within and between the cerebral hemispheres in the adult’s central nervous system is of considerable importance to those interested in neuropsychological development. The relative paucity of information concerning the specific effects of brain damage during development necessitates the use of the effects of adult brain damage as a yardstick against which the outcome of early brain damage may be set. By contrasting the effects of early brain injury with those which occur following damage to the mature brain, it may be possible to ascertain whether the organizational pattern typical of the adult brain is present also in early development or whether it emerges gradually.
  
 +
It may seem odd that this question should be asked at all, given the fact that, superficially at least, the anatomical structure of the brain is broadly similar in the neonate and the adult, even to the extent of the presence of the adult pattern of anatomical asymmetry (Wada et al, 1975). However, evidence has been presented from time to time which argues that certain crucial functional differences are present. Animal studies have indicated that effects of motor cortex damage in infancy are less deleterious than equivalent damage at maturity since the younger animals escape the flaccid paralysis and spasticity of their elders and retain their postural and locomotor capabilities (Kennard, 1940). Even in humans the claim has been made that children may escape some of the effects of cerebellar injury suffered by adults (Geschwind, 1972). In the area of language it has been known for some time that children who become aphasic following massive left hemisphere injury usually recover speech rapidly (Guttman, 1942), a phenomenon which is not unknown but is certainly rare in the adult (Dejerine and Andre-Thomas, 1912). In such cases it is possible to resort to concepts like plasticity in order to explain the greater resilience of the immature brain, but in some cases the reorganization following injury appears to be so expeditious that it is difficult to believe that other areas of the brain not previously involved have acquired behavioural functions so rapidly (Kennard, 1940; Geschwind, 1972). Even if the idea of greater neural plasticity is accepted, the question may still be asked as to how great this capacity for compensation is? When children become aphasic following unilateral brain damage and language eventually resides in the contralateral hemisphere, does it cope as adequately as the damaged hemisphere would have done? The existence of greater plasticity in the developing brain does not necessarily mean that disparate structures are functionally equivalent. This inference would be valid only if different structures were shown to attain the same degree of functional sophistication.
  
 +
These two issues concerning the establishment of the adult pattern of neural organization and the extent to which it can be modified following early brain damage will be explored in the following pages.
  
204
 
  
 +
==The context within which damage occurs during development==
  
 +
It is clear, that, as a child grows from birth, the various indices of maturation (behavioural, neurophysiological and morphological) tend to move together towards levels accepted as indicating greater maturity. The range and complexity of spatial, linguistic and social skills increases. In association with them electrophysiological measures of brain activity move from showing a slow and irregular pattern at birth to faster rhythms and widening of the bandwidth characteristics with increasing age. Neuroanatomical changes are also evident both at a gross level, where changes in surface area and the fissural pattern of the brain are seen (Turner, 1948, 1950), and at the microscopic level, where the size of neurones and the complexity of the dendritic pattern increases (Marshall, 1968). When investigators are concerned exclusively with behavioural development, electrophysiological and anatomical factors may provide an interesting but non-essential background. However, where one is concerned with the outcome of brain injury, which occurs early rather than late in the developmental sequence, then the broad neurobiological context in which the injury occurs assumes increasing prominence. A child who suffers brain injury has not just lived for a shorter time, and consequently experienced less, than an adult. The injury has occurred within a system which has a complex and uncompleted developmental plan which is rapidly unfolding, rather than as in the adult where injury occurs within a system where the developmental sequence may have reached a plateau of several decades’ duration. With this in mind some relevant data which outline the changing status of cerebral structures during development will be examined.
  
  
 +
==Electrophysiological and neuroanatomical maturation==
  
regarded cognitive skills as a function of the entire organism. He saw the  
+
Electrophysiological measures of cerebral development in man indicate a progressive increase in mean frequency content of the EEG from birth to maturity. Whilst in the neonate this is characterized by a labile pattern with periods of almost total electrical silence and an unclearly differentiated sleep pattern, the adult shows a pattern of continuous activity with a frequency spectrum that is at least superficially related to the subject’s state of alertness and with a well-differentiated pattern during the various stages of sleep (see Marshall, 1968, and Milner, 1976, for reviews, and Thompson, this volume). The adult pattern, with the occipital alpha frequency centred in the region of 10 Hz, and the presence of clear beta activity (14-30 Hz) during arousal, is attained only gradually (Henry, 1944). The most typical frequency band shifts from the delta region (1-3 Hz) at age 1 year and below, through the theta band (4-7 Hz) between 2 and 5 years, to the alpha band (8-13 Hz) between 6 years and adulthood. Beta frequencies become increasingly common in late childhood, and are an increasingly common feature of the adult EEG. Measurement of evoked potentials reveals that peak latencies are long in infancy and decrease as maturation proceeds, whilst in general, amplitude tends to decline after an initial rise. This amplitude trend is also characteristic of the development of the gross EEG (Shagass, 1972). Whilst the behavioural significance of the EEG in man is currently an extremely active research area, the status of the research findings is not always unequivocal. The existence during infancy and childhood of a differential density of waveforms in the left and right hemispheres (Walter, 1950) and the presence of lateral differences in auditory evoked potentials (Molfese, 1977) cannot be taken as evidence of functional asymmetry within the cortex at these ages, since they may indicate changes in the thalamus and corpus striatum, which are simply mirrored in an as yet incompletely differentiated and immature cerebral mantle. The EEG data do, however, allow us to see the gradual emergence of intracerebral rhythms whose mean cycle time becomes shorter with age, and whose responsiveness to external stimulation becomes crisper. Furthermore, this developmental trend continues throughout the period from birth to sexual maturity and may actually show reversal in old age (Shagass, 1972).
symptoms following brain damage as manifestations of a complex adaptive
 
syndrome in which higher intellectual abilities, in particular the ability to  
 
abstract, were likely to be depressed. This general intellectual loss was likely to
 
be seen in the patients’ failure on a variety of cognitive tasks, but particularly in
 
linguistic skills since these demanded, more than other capabilities, the integrity
 
of the entire brain. Holding views such as these, there was no problem in  
 
accounting for the return of functions after cerebral injury since the intact areas
 
of the brain would continue to function in their usual way following an initial
 
period of shock, although there would of course be a loss of efficiency. Factors
 
such as the age of the subject at the time of injury were seen to play a part, and  
 
indeed one of Lashley’s students (Tsang, 1937) had provided evidence that
 
proportionately equivalent lesions in adult and juvenile rats produced less
 
impairment in the younger animals.  
 
  
In contrast to models of the brain based on assumptions of global processing
+
The impression of a long-term developmental cycle which emerges from examination of human electrophysiological development perhaps finds even stronger support when neuroanatomical development is examined. It is apparent that although the full complement of neurones is probably present in the central nervous system at birth, the brain continues to grow in overall size and the characteristic sulcal and gyral pattern of the adult emerges gradually over the first 6 years, and perhaps even later in the case of the frontal lobe (Turner, 1948, 1950). When the internal differentiation of the brain is considered a complex and protracted pattern of development unfolds (Yakovlev and Lecours, 1967; Lecours, 1975). Using the density of myelin, the lipid sheath surrounding the axons of neurones, as a criterion of maturation these workers have mapped the development of CNS pathways and structures and used the termination of the myelogenetic cycle as an index of when the system reaches final functional maturity.
and diffuse representation, from the middle nineteenth century onwards
 
evidence began to accumulate rapidly that restricted brain lesions often
 
produced highly specific disorders in which the patients’ remaining spectrum of  
 
skills were relatively unaffected. Broca (1861) produced two cases in which the  
 
patients’ verbal expression was drastically impaired but whose comprehension
 
of language appeared to be relatively good. Wernicke (1874) produced evidence
 
that patients’ ability to comprehend and utter meaningful linguistic statements
 
could be grossly impaired yet their pronunciation and rate of verbal output
 
could remain unimpaired. Other descriptions followed of patients with restricted
 
and often bizarre symptom complexes. Dejerine’s description (1892) of Mr. C is
 
perhaps one of the classic cases. This patient, who had right visual field
 
blindness, could nevertheless recognize objects and continue his everyday life.  
 
Despite apparently normal vision in his left visual field and the ability to speak
 
and write normally, he was unable to read by sight even the sentences he had
 
written himself a short while before. He was however able to ‘read’ by feeling the
 
shapes of cut out letters. Other syndromes described included those of
 
disordered motor planning (Leipmann, 1908), the inability to recognize objects
 
(Lissauer, 1890), and the inability to recognize melody (Henschen, 1926). The list
 
could be continued, but the importance of these cases was that they convinced a
 
substantial number of investigators that the brain could not be organized in a
 
diffuse equipotential manner but, on the contrary, must contain relatively
 
specialized processors even for such uniquely human processes as the comprehension and generation of language.  
 
  
Modern neuropsychology has moved away from the exclusive study of such
+
It is apparent from this research that brain development does not proceed uniformly in all central nervous subsystems. Sensory fibre tracts and associated nuclei myelinate before the cortical intra- and interhemispheric communication systems. Different sensory systems however may show a diversity of time courses. The optic radiations subserving the visual cortex show a short cycle of myelination closely following the myelination of the optic tract, and is virtually complete by 4 months of age. The acoustic radiation subserving the auditory cortex does not show complete development until the 4th year, in marked contrast to the prethalamic auditory system, which is mature by the 4th postnatal month. The intracortical and interhemispheric association fibres, which allow communication between different regions and whose disruption leads to many of the bizarre neuropsychological disconnection syndromes (Geschwind, 1965), have prolonged maturational cycles extending into the second decade of life. Examination of the cortex itself indicates that some regions implicated in linguistic competence (inferior parietal lobule) show a slow onset of myelination and that this process may also continue beyond the second decade of life. It should be emphasized that although the study of the myelogenetic cycles of maturation shows a complex extended pattern of development from birth to maturity, a caveat is necessary. Neural conduction can occur in fibres before they become myelinated (Ulett et al , 1944) and indeed myelination may be aided by neural activity (Langworthy, 1933). However, myelin contributes greatly to the efficiency and speed of neural conduction, which underlies the complex analysis and planning characteristics of human cognition and action. The importance of myelin may be appreciated by considering the devastating behavioural effects of demyelination disease in man such as occurs in multiple sclerosis. The myelogenetic analysis emphasizes the manner in which the brain becomes structurally mature. Phylogenetically older structures, in general, mature earlier than those of recent phyletic origin. There are exceptions to this, for example the reticular formation, whose developmental cycle again extends into the second decade of life, partly no doubt because its final operational capability is not required until cortical systems are completely mature.
rare and extraordinary cases to the systematic examination of groups of patients
 
in which the behavioural effects of differences in known cerebral pathology can
 
be investigated. The more extreme forms of cerebral localization have been
 
  
 +
Both the electrophysiological and neuroanatomical data indicate that the human central nervous system develops over an extended period. Particularly fascinating are the observations that the higher auditory systems (geniculo- temporal pathways) exhibit a developmental cycle that is more than ten times longer than visual structures at the same level of the CNS. It is probable that this reflects the necessity of incorporating into the growing brain the species specific demand of learning the complexities of language via the acoustic mode and allows for the building of the culture-specific phoneme system which is eventually used. However, it is apparent that a considerable part of the developing child’s life is characterized by the presence of cortical structures which are functionally (by electrophysiological and anatomical criteria) immature. The status that these immature structures have in subserving the growing child’s cognitive repertoire is not straightforward. It is possible to envisage the mapping of cognitive growth within the cerebral structures which subserve cognition in the adult in at least two ways. The first view would regard all those structures which are involved in a given functional system in the adult as also being involved in infancy, although the immaturity of the system considered as a whole would limit its capabilities. The limitations seen for instance in perceptual and motor systems in the neonate would be ascribed to the immaturity of the cortical system, which was nevertheless functional, rather than to the fact that lower but morphologically more mature structures are controlling the behaviour. The alternative view would regard neurobehavioural development as a process beginning with relatively primitive analysis and response control systems residing in phylogenetically older structures which mature earlier in the developmental sequence. As development proceeds, phylogenetically newer structures, which attain maturity later in the developmental sequence, will capture and modulate the activity of the older systems as well as adding more complex control processes. This process will not have a uniform time course across all systems. In the case of the visual system this transition may occur relatively early in development at two to three months of age since the cortical network in this case has a short developmental cycle. In the case of audition the whole process may be more protracted with cortical control becoming ascendant in the period of 2-4 years, whilst in the complex action systems controlled by the frontal lobe, the processes may take even longer, given the differential growth of the region beyond 6 years of age (Turner, 1948, 1950). Evidence that it is this latter view which is the more reasonable description of neurobehavioural development comes from a number of observations that will be subsequently outlined, but it must be said in advance that the case is by no means proven.
  
  
DETERMINATE AND PLASTIC PRINCIPLES
+
==Neuropsychological evidence concerning functional maturation==
  
 +
When damage occurs in the mature brain the effects are usually immediate; the degree of functional loss, whether it be sensory, motor or cognitive, is greatest immediately after the lesion and usually shows some remission over time. In the immature brain in a number of instances the pattern is almost the reverse of this. In the case of hemiplegia, sustained as a consequence of prenatal or perinatal injury, the symptoms of the disorder frequently emerge gradually over a prolonged period. Abnormalities in the use of the hand and arm may emerge at between 4 and 6 months, whilst differences in the behaviour of the legs may not become apparent until 10 months of age or more. Deficits in the use of the lower limbs may only become apparent when the child begins to walk, a milestone that is frequently attained in the normal age range (Lyon, 1961). Finally, athetoid movements do not make their appearance until much later, typically between three and four years of age (Lenneberg, 1968). Thus the developmental pattern is seen to move through a series of stages: for example, the grasp reflex is present initially in both the affected and the normal hand, but it persists on the affected side and usually the hand becomes clenched into a tight fist. Individual finger movements do not appear on the hemiplegic side, although movement of the thumbs may be possible. As the child grows, then, the deficit becomes more severe. However, it is noticeable that these children escape some of the more drastic consequences of hemiplegia resulting from cerebral injury at maturity.
  
205
+
The severity of paralysis in the upper limb is less and the lower limb is capable of greater use than after comparable damage in adults. That the residual function on the affected side is not attributable to surviving undamaged tissue in the diseased hemisphere is shown by the fact that removing the diseased hemisphere later in development does not cause further impairment and may frequently result in improvement (Cairns and Davidson, 1951).
  
 +
Two features then are apparent in these cases. The first is the greater capacity of the young brain to compensate and escape some of the consequences of equivalent injury in adulthood—its plastic propensity. The second feature is cogently described by Lenneberg (1968): ‘one may say that the child with a perinatal cerebral injury only gradually grows into his symptoms’. This emergence of deficit with age is compatible with the view that certain systems are pre-programmed to appear at certain stages in development and injury to them will only become apparent when they fail to appear. Similar affects in the motor sphere were observed by Kennard (1940) in macaque monkeys where ablation of the motor cortex in infancy resulted in surprisingly little immediate effect, but precluded the development of fine manipulatory skills, and this, together with signs of dyskenesia, became more apparent as the animals grew older. It appears that the motor cortex only begins to exert its influence gradually and its loss or malfunction may not become apparent until a later stage of development.
  
rejected, but the acceptance of specialized processing within and between the
+
Further support for the notion that behaviour early in development may be mediated exclusively by subcortical structures, with cortical processors becoming involved later, has been provided by Goldman (1976). It has been apparent for some time that tasks which require a monkey to remember the location of a stimulus over a brief interval of time are drastically affected by damage to the dorsolateral prefrontal cortex (Chow and Hutt, 1953). These are known as the delayed-response and delayed-alternation tasks. When the dorsolateral frontal cortex is removed within the first 2 months of life however, the operated animals perform as well on this task as unoperated controls as long as testing is carried out within the first year of life (Harlow et al , 1970). If these monkeys are followed into the second year of life they show evidence of increasing impairment of delayed response tasks. Lesions in subcortical structures which are functionally connected with the dorsolateral prefrontal cortex (dorsomedial nucleus of the thalamus and the head of the caudate nucleus), indicate that the monkeys operated on as juveniles show the same pattern of deficit as adults, i.e. failure on delayed alternation tasks (Goldman, 1974). These results emphasize that not only may the effects of brain damage fail to appear early in development and only reveal themselves as the animal grows, they also show that structures which are required for the adequate performance of a task in adulthood (the dorsolateral prefrontal cortex), are not necessary for the performance of the same task when the animal is an infant or a juvenile.
two hemispheres of the brain has gained wide acceptance (see Walsh, 1978, and  
 
Hecaen and Albert, 1978). This current position regarding the distribution of
 
functional systems within and between the cerebral hemispheres in the adult’s
 
central nervous system is of considerable importance to those interested in
 
neuropsychological development. The relative paucity of information concerning the specific effects of brain damage during development necessitates the use
 
of the effects of adult brain damage as a yardstick against which the outcome
 
of early brain damage may be set. By contrasting the effects of early brain  
 
injury with those which occur following damage to the mature brain, it may
 
be possible to ascertain whether the organizational pattern typical of the  
 
adult brain is present also in early development or whether it emerges gradually.  
 
  
It may seem odd that this question should be asked at all, given the fact that,
+
These experiments contribute a salutary warning to those who would assume that, because a cortical structure is implicated in a functional system in adulthood it must of necessity be involved in performance of those same functions at an earlier developmental stage. In infant and juvenile macaques subcortical systems are capable of mediating responses which in adults require the participation of the cortex. Furthermore, evidence is available which indicates that the time course over which the effects of cortical lesions become apparent during development differs for different regions. While monkeys aged 2\ months with orbital frontal cortex lesions are equivalent to unoperated controls in the performance of object reversal learning, deficits in performance became apparent by the time the animals are one year old (Goldman, 1974). Thus, while the effects of dorsolateral frontal cortex damage sustained in infancy on delayed alternation tasks do not become apparent until after one year of age, the effects of orbitofrontal damage in infancy on object reversal learning become apparent before one year of age. In the case of both delayed alternation and object reversal learning early in development subcortical structures are capable of mediating the behaviour successfully. With respect to these studies it should be pointed out that macaque monkeys attain sexual maturity between 24 and 30 months of age, so the effects of early brain damage may take a considerable proportion of the developmental cycle before they become apparent.
superficially at least, the anatomical structure of the brain is broadly similar in  
 
the neonate and the adult, even to the extent of the presence of the adult pattern
 
of anatomical asymmetry (Wada et al, 1975). However, evidence has been
 
presented from time to time which argues that certain crucial functional
 
differences are present. Animal studies have indicated that effects of motor cortex  
 
damage in infancy are less deleterious than equivalent damage at maturity since
 
the younger animals escape the flaccid paralysis and spasticity of their elders and
 
retain their postural and locomotor capabilities (Kennard, 1940). Even in  
 
humans the claim has been made that children may escape some of the effects of
 
cerebellar injury suffered by adults (Geschwind, 1972). In the area of language it
 
has been known for some time that children who become aphasic following
 
massive left hemisphere injury usually recover speech rapidly (Guttman, 1942), a
 
phenomenon which is not unknown but is certainly rare in the adult (Dejerine
 
and Andre-Thomas, 1912). In such cases it is possible to resort to concepts like
 
plasticity in order to explain the greater resilience of the immature brain, but in  
 
some cases the reorganization following injury appears to be so expeditious that  
 
it is difficult to believe that other areas of the brain not previously involved have
 
acquired behavioural functions so rapidly (Kennard, 1940; Geschwind, 1972).
 
Even if the idea of greater neural plasticity is accepted, the question may still be
 
asked as to how great this capacity for compensation is? When children become
 
aphasic following unilateral brain damage and language eventually resides in the
 
contralateral hemisphere, does it cope as adequately as the damaged hemisphere
 
would have done? The existence of greater plasticity in the developing brain
 
does not necessarily mean that disparate structures are functionally equivalent.
 
This inference would be valid only if different structures were shown to attain the
 
same degree of functional sophistication.  
 
  
These two issues concerning the establishment of the adult pattern of neural
+
The evidence cited so far has argued for a model of development in which the complete maturational cycle is prolonged, but within which different systems may attain functional maturity at widely divergent times. Initially, behaviour may be controlled by subcortical systems, and depending on the time-course of the maturational cycle in the higher reaches (cortical) of each system so control will pass to the phylogenetically newer and more adaptive system. Bronson (1974) has argued, on the basis of changes in the pattern of visual behaviour in infants, that in the case of the visual system a transfer of control passes from the superior colliculus to the striate cortex, from the ‘ambient’ to the ‘focal’ system (Trevarthen, 1968), during the 2nd and 3rd postnatal month. Such a view is certainly compatible with the rapid postnatal development of the geniculo- striate system (Yakovlev and Lecours, 1967). In the case of motor function the longer maturational cycle of the medullary pyramids (up to 12 months), which carry the axons of the Betz cells of the motor cortex to the spinal cord and are required for control of individual fingers and skilled sequences (Lawrence and Hopkins, 1972), leads one to expect that transition of control in this case may take place over a more protracted period. The emergence of comparative motor deficit between affected and normal side, in cases in infantile hemiplegia, between 4 and 12 months of age (Lyon, 1961) appears to reflect this longer cycle of development. In man, however, the long-term emergence of a deficit in previously established skills after early brain injury akin to that reported by Goldman (1974, 1976) for the macaque monkey, has not as yet been reported.
organization and the extent to which it can be modified following early brain  
 
damage will be explored in the following pages.  
 
  
 +
Nevertheless, evidence is available which indicates that, on some perceptual tasks, brain-damaged children may show either a consistent difference from controls over a wide age range (Cobrinik, 1959), or a progressive change, which either diverges from or converges to control values between the ages of 5 and 15 years depending on the particular measure being considered (Teuber and Rudel, 1962). Thus, slowly emerging effects of early brain damage in man are not unknown, but long-term effects, with an intervening ‘silent’ interval, have not, to the present author’s knowledge, been described.
  
  
206
+
==Interactive effects and their interpretation==
  
 +
Generalized effects on intelligence that result from presumed structural incapacity (Hebb, 1942) or following localized injury (Thompson, 1978) have indicated that while early injury may produce generalized depression of full- scale IQ, late injury produces a more specific pattern of deficit, with less depression of full-scale IQ. Research findings of this nature can be seen as support either for a model of brain development in which neural structures only gradually attain their mature state, or alternatively, as support for the view that reorganizational capacities are at work during development which allow savings on specific skills but at the cost of overall depression in intellectual attainment. However, there is no doubt that both views are valid and have independent evidence to support them. The developing brain is more vulnerable than the mature brain and this can be seen in the long term generalized deleterious consequences of nutritional deprivation during the brain-growth spurt, as measured by both neurochemical and anatomical criteria (Dobbing, 1968), and by behavioural criteria (Chase, 1973). However, it is also clear that substantial left hemisphere damage, which usually leads to long-term severe dysphasia in adulthood, results in only transitory dysphasic symptoms when the damage occurs early in childhood (Hecaen, 1976), and there is evidence of savings in visuo-spatial skills following early right hemisphere dysfunction, which is not apparent with equivalent damage at maturity (Kohn and Dennis, 1974).
  
 +
These findings provide unequivocal evidence of the reorganizational and plastic capacities of the developing brain. However, it is also evident that the usual predetermined pattern of left hemisphere specialization for language and right hemisphere specialization for visuo-spatial skills set limits to this plastic capacity. Where one hemisphere has sustained early injury, the language skills exhibited by a remaining and intact right hemisphere are less proficient than those exhibited by a remaining intact left hemisphere (Dennis and Kohn, 1975). It also appears that visuospatial abilities are better developed in an intact right hemisphere than when the left hemisphere alone remains fully functional (Kohn and Dennis, 1974). Thus, while reorganization is possible following early brain injury, this may be more limited than has been previously thought. Indeed, given the anatomical asymmetry present in the neonatal brain (Wada et al, 1975) it would be surprising if this structural specialization were not detectable at some stage in the behavioural effects of unilateral brain injury. The results of unilateral brain injury in early development nicely juxtapose two major tendencies which emerge from neurobehavioural research: on the one hand, the trend towards carrying through the construction of a preprogrammed system over a protracted time period and, on the other, an adaptive plastic capacity which allows the partial redirection of functional systems should damage occur.
  
 +
The complexity of the processes involved in the analysis of sensory information (Hubei and Wiesel, 1963; Werner and Whitsell, 1973) that has emerged from single neurone recording makes it clear why a great deal of preprogramming must be involved in the construction of complex adaptive neural systems. It is less easy to describe the mechanisms which allow complex brain systems to exhibit the degree of plasticity that they evidently do in early development. The explanation may reside in the fact that younger individuals are less susceptible to transneural degeneration effects and also show higher levels of biosynthetic activity in brain tissue, which may allow damaged networks greater restitutional capacity (see Goldman and Lewis, 1978, for review). It is also evident that behavioural recovery, seen after early injury in some cases, depends on the ability of young animals to profit from experience in a way not available to the adult. Monkeys sustaining brain injury in infancy show greater recovery the earlier training experience is given in development, although the ability to profit from this experience depends on the nature of the task and the site of the lesion in the brain (Goldman and Lewis, 1978). The results of this study gave some indication that it was the nonspecific stimulation effects of the training which were important in recovery, rather than specific carry-over from common features of the task.
  
 +
The fact that experience per se may be an important factor in promoting recovery is of considerable importance, since there has been suspicion about the value of training programmes in the recovery from brain damage (Byers and McLean, 1962). Given the intricacy of the neurobiological factors involved in early brain injury it may be too easy to forget about the cognitive dimension. During development a child moves from a relatively primitive analysis and interaction with the external world to a stage where his conceptual structures are complex and enable sophisticated analysis and prediction of the environment. The cognitive capacities evident at maturity have been built on simpler ones gathered progressively during childhood. Thus, impairment of systems which gather and utilize information as a consequence of cerebral damage could result in diminished intellectual achievement, not through injury to critical higher-level systems, but because essential ‘feeder’ mechanisms have malfunctioned. An adult with a subcortical lesion which destroys the left auditory radiation and the callosal input from the contralateral hemisphere may show a normal audiogram but be incapable of interpreting spoken language (Gloning et al ., 1963). Nevertheless, speech, reading and writing may be normal since their associated cortical circuitry is undamaged and language has been previously established. In a child, bilateral disruption of the auditory radiations by a lesion damaging the lips of the sylvian fissures and the insulae can preclude the normal development of language, despite evidence of hearing in the normal range (Landau et al , 1960). Even children who become peripherally deaf after acquiring speech may not only show arrested language development but lose previously acquired linguistic skills (Bay, 1975). This ‘cognitive starvation’ effect, which is easy to comprehend in the instances cited, may also operate within association areas of the cortex and may underlie the tendency of early brain pathology to produce more global intellectual depression effects than are seen with lesions in adolescence and adulthood.
  
The context within which damage occurs during development
+
The data briefly reviewed in this section emphasize that the effects of brain injury in the developing nervous system are particularly complex. When injury occurs, it is within a system whose functional capacities are still unfolding, and the effects of injury are sometimes not immediately apparent. The plastic capacity of the system may also mask the extent of any physical injury and lead to a false assumption that effects have been transitory. There is also the added complication that, whilst injury may not have damaged structures critical for the attainment of certain cognitive skills, because critical ‘feeder’ systems have been impaired, these cognitive mechanisms may not have the experiental basis upon which to build.
  
It is clear, that, as a child grows from birth, the various indices of maturation
+
==The consequences of early brain damage==
(behavioural, neurophysiological and morphological) tend to move together
 
towards levels accepted as indicating greater maturity. The range and complexity of spatial, linguistic and social skills increases. In association with them
 
electrophysiological measures of brain activity move from showing a slow and
 
irregular pattern at birth to faster rhythms and widening of the bandwidth
 
characteristics with increasing age. Neuroanatomical changes are also evident
 
both at a gross level, where changes in surface area and the fissural pattern of the
 
brain are seen (Turner, 1948, 1950), and at the microscopic level, where the size
 
of neurones and the complexity of the dendritic pattern increases (Marshall,
 
1968). When investigators are concerned exclusively with behavioural development, electrophysiological and anatomical factors may provide an interesting
 
but non-essential background. However, where one is concerned with the
 
outcome of brain injury, which occurs early rather than late in the developmental sequence, then the broad neurobiological context in which the injury
 
occurs assumes increasing prominence. A child who suffers brain injury has not
 
just lived for a shorter time, and consequently experienced less, than an adult.
 
The injury has occurred within a system which has a complex and uncompleted
 
developmental plan which is rapidly unfolding, rather than as in the adult where
 
injury occurs within a system where the developmental sequence may have
 
reached a plateau of several decades’ duration. With this in mind some relevant
 
data which outline the changing status of cerebral structures during development will be examined.
 
  
 +
Global and specific processing
  
Electrophysiological and neuroanatomical maturation
+
In 1942 Hebb drew attention to the different patterns seen following brain damage in both mature and immature nervous systems. Adults, he found, could be considered to be either aphasic or non-aphasic types (Hebb, 1942). The aphasic type showed obvious evidence of deterioration on verbal tasks and some also showed evidence of impairment on such non-verbal tasks as detecting absurd errors in pictures and block manipulation performance. However, some of the aphasic patients showed evidence of almost normal performance on nonverbal tasks, and Hebb remarked on the wide disparity of abilities seen on particular tests in individual aphasic patients. This conclusion of Hebb’s (that non-verbal skills may be retained to a remarkable extent in some cases of aphasia) is reinforced by more recent research on this topic (Zangwill, 1964; Kertesz and McCabe, 1975). In the non-aphasic type of brain injury on the other hand many verbal tasks could be adequately completed, but there was usually severe impairment on maze learning, block manipulation and picture absurdity tasks, as well as impairment on some verbal tasks, e.g. the defining of abstract words, or naming opposites. The two types were, however, sufficiently different for Hebb to state that following adult brain injury a reasonably specific pattern of deficit often emerges—some skills showing deterioration and others being relatively intact. In contrast, a group of children with what he termed ‘exogenous’ brain injury showed no evidence of a dual pattern, that is the ‘aphasic’ and ‘non-aphasic’ types did not occur as a consequence of early brain injury. The group as a whole showed depression of verbal IQ, but since he thought it unlikely that every case of brain injury in infancy involved damage to the language areas it must be that ‘low verbal test scores are produced by early lesions outside the speech areas’ (Hebb, 1942, p. 286). He went on to argue that the more global pattern of intellectual depression seen after early brain injury occurs as a result of the differing demands being made on the adult and the child after cerebral damage. The adult has merely to make use of skills which have already been acquired, whereas the child has still to assimilate a range of skills. Since a greater cognitive demand is made during the acquisition of a skill than by the performance of one already acquired, the growing child is at a greater loss than the adult when an equivalent amount of brain tissue has been lost in both. Hebb went further and argued—following Lashley (1929)—that some degree of equipotentiality must exist in the cortex and that areas outside the classical language areas must be involved in the development, but not the maintenance, of linguistic skills once they have been mastered.
  
Electrophysiological measures of cerebral development in man indicate a
+
Two major hypotheses then emerge from Hebb’s work (1942). The first is that early, rather than late, brain damage has a more global depressive effect upon intellectual development. The second hypothesis is that the developing nervous system is characterized by a greater degree of equipotentiality than that of the adult, since the attainment of normal adult performance on a range of specific skills seems to depend on the integrity of whole cerebrum. The first hypothesis has, in general, received support from subsequent research. Bryan and Brown (1957) found that there is a strong relation between the age of injury and mean IQ, so that those with an injury present at birth averaged a score of 62, those injured in infancy averaged 66 while those with injuries occurring between 3 and 10 years and between 10 and 20 years averaged 71 and 85 respectively. Thompson (1978) reported that in 282 subjects who sustained localized cerebral injury in childhood, there was a linear relationship between age of injury and full-scale IQ with those injured before 5 scoring 97 and those injured above 15 years scoring 106.5. It should be noted, however, that whilst McFie (1961a) found a rise in mean IQ between those injured in the age bands 1-4 and 5-9 years from 88.8 to 106.0, he found a fall in IQ with those sustaining injury between 10 and 15 years (82.7). However, on balance the findings would seem to support Hebb’s initial contention.
progressive increase in mean frequency content of the EEG from birth to
 
maturity. Whilst in the neonate this is characterized by a labile pattern with
 
periods of almost total electrical silence and an unclearly differentiated sleep
 
pattern, the adult shows a pattern of continuous activity with a frequency
 
spectrum that is at least superficially related to the subject’s state of alertness and  
 
with a well-differentiated pattern during the various stages of sleep (see
 
Marshall, 1968, and Milner, 1976, for reviews, and Thompson, this volume). The
 
adult pattern, with the occipital alpha frequency centred in the region of 10 Hz,
 
and the presence of clear beta activity (14-30 Hz) during arousal, is attained
 
only gradually (Henry, 1944). The most typical frequency band shifts from the  
 
delta region (1-3 Hz) at age 1 year and below, through the theta band (4-7 Hz)
 
between 2 and 5 years, to the alpha band (8-13 Hz) between 6 years and
 
adulthood. Beta frequencies become increasingly common in late childhood, and
 
  
 +
The second hypothesis emerging from Hebb’s (1942) study, that the developing nervous system is characterized by a greater degree of equipotentiality than that of the adult, is rather more contentious since it is more difficult to test than it might appear at first sight. It has already been pointed out that general depression of IQ cannot be used as evidence for a type of mass action operating during development, since it may also argue for an interdependence of separate capabilities being required for the construction of more complex schemata. It is also apparent that brain-damaged children show widely differing patterns of impairment, which would be difficult to comprehend if there were a tendency for the brain to act uniformly in the acquisition of cognitive skills (Strauss and Lehtinen, 1968). There is also the added difficulty that IQ tests may be rather insensitive to specific patterns of disability produced by brain injury, both in children (Boll and Reitan, 1972) and adults (Walsh, 1978), a factor which has resulted in the construction of specialized test batteries.
  
 +
However, instead of asking whether the general depressive effect of early brain damage on IQ is due to a greater degree of global processing in the immature CNS, it might be more fruitful to consider whether a similar pattern of impairment emerges on specific skills after similar damage in the child and the adult. McFie (1961a), in an investigation of the effects of localized post-infantile cerebral lesions in children, found that there was a tendency for Wechsler verbal scores to be lower following left hemisphere injury and performance scores to be lower following damage to the right hemisphere. He also noted a similarity in the pattern of impairment shown on the Memory for Designs component of the Terman-Merrill scale (1937) between children and adults when comparing the effects of frontal, temporal and parietal injury. He reported that the greatest deficit is to be found in both groups following right parietal damage. Fedio and Mirsky (1969) examined the pattern of impairment exhibited by children with either unilateral temporal lobe or with centrencephalic epilepsy on a test battery designed to measure performance on both verbal and non-verbal tasks, and a task of sustained attention. The children, who had a history of illness dating from early school years, showed similar impairment profiles to those of adults with similar pathology. Those with left temporal epileptiform foci required a greater number of trials to learn lists of ten words and showed greater loss after a 5- minute interval than those with right temporal or centrencephalic pathology. Those with right temporal pathology showed greatest impairment on the recall of the order of random shapes and on production of the Rey-Osterrieth figure. The centrencephalic group showed the greatest deficit on a task requiring sustained attention. Annet et al (1961) also found a similar pattern of verbal and spatial difficulties in children classified on the basis of lateralized EEG abnormalities. These results would suggest that children show impairments of the same type as those found in adults with similar pathology. It may be objected however, that in these cases the damage is characteristic of juvenile rather than infant brain damage, and, if adult cortical specialization appears gradually, then patterns of specific loss will also begin to appear, producing the observed similarity to the adult type by middle childhood. However, evidence does exist which would suggest that there is hemisphere specialization, even when damage occurs perinatally or in infancy.
  
DETERMINATE AND PLASTIC PRINCIPLES
+
Damage to the left, but not the right, hemisphere before the end of the first year of life results in impairment in the rate at which combinations of words (elementary syntax), but not single words, are learned (Bishop, 1967). Furthermore, children who have had either a left or right hemisphere removed as a consequence of damage sustained during the first year of life show differential effects depending on which hemisphere is involved. Those with left hemisphere removal show greater difficulty in the comprehension of syntax than right hemi- decorticates (Dennis and Kohn, 1975). In particular, difficulties as shown by a greater number of errors are apparent in comprehension of the passive negative, e.g. ‘the girl is not pushed by the boy’, as opposed to the active affirmative, ‘the boy pushes the girl’. In these experiments comprehension was assessed by having the child choose a picture which depicted the sentence. The greater difficulty in the comprehension of passive sentences was also apparent in longer response latencies. Children with early right hemisphere damage followed by hemi- spherectomy show difficulties on spatial tasks (Kohn and Dennis, 1974). The types of spatial task on which they show relative deficit are those which continue to show improvements in normal subjects through the teens, e.g. the WISC and Porteus mazes, and map reading tasks, which require a subject either to state the direction to be taken or to follow a route through markers placed on the floor. Early maturing skills, such as tactile form matching and visual closure, were unaffected in contrast to right hemisphere injury at maturity which severely depresses these abilities. Further analyses of three cases where hemispherectomy antedated the beginnings of speech were presented by Dennis and Whitaker (1976) and two cases where hemispherectomy for unilateral pathology was carried out at ages 3 and 4 years respectively were reported by Day and Ulatowska (1979). In these cases the pattern of deficit is similar to those previously reported and supports the view that the hemispheres are differentially involved in different aspects of cognition. Specialization would appear to be an early-established characteristic of the child’s brain although its potential for reorganization complicates the issue (see p. 225).
  
 +
Given that differences in the patterning of intelligence subtest scores only really become obvious during adolescence and beyond (Thompson, 1978), whereas specific deficits are detectable by specially devised tests in younger children, IQ tests appear to be insensitive instruments on which to base theories concerning brain development. One obvious factor which will lessen the sensitivity of IQ tests to brain damage early in development is the capacity to transfer the development of linguistic and spatial skills to the contralateral hemisphere should damage occur. This plastic capacity should not however be confused with ideas about mass action or equipotentiality. These latter ideas imply the existence of a type of diffuse processing network to which the association cortex within each hemisphere contributes uniformly (Lashley, 1929). The transfer of functional capability from one hemisphere to the other, however, is to be understood in a rather different context. Each cerebral hemisphere contains anatomical structures which are essentially duplicates of those found in the other, with the difference that certain cytoarchitectonic areas may be relatively larger or smaller. In some instances, particularly in the language area, these cytoarchitectonic differences in size may be as great as 700% in favour of the left hemisphere (Galaburda et al ., 1978). However, each specialized cortical area has a pattern of connections to the rest of the brain which, in essence, is a lateral reversal of those found in the other hemisphere. The ability of these ‘duplicates’ to assume some of the functional capacities previously assumed by their cytoarchitectonic counterparts is perhaps not too surprising. Indeed, the puzzling feature is that in a substantial majority of the adult population this ability is lost. The assumption that somehow the areas within each hemisphere act as a kind of equipotential unit, is not supported by the available evidence. If such a diffusely organized system were operative in the left hemisphere during development, then it would be reasonable to assume that unilateral damage, resulting in suboptimal processing capacity, would be sufficient reason to transfer linguistic processing to the remaining intact hemisphere. Milner (1973) has provided evidence, based on language lateralization, tested by the Wada (intracarotid injection of sodium amytal) technique, that only when early injury invades those areas shown to be important for linguistic processing in the adult, will language transfer to the right hemisphere. These results suggest that certain key regions, not the global processing capacity or total operational mode of one hemisphere, promote the establishment of language within that hemisphere.
  
207
+
In considering the question of global or specific processing in development, the evidence on balance suggests a specific processing configuration not dissimilar to that found in the adult brain. It has also been argued that one of the reasons why early brain damage often has a markedly depressive effect on intellectual growth may be that the substrate of complex cognitive processes may require the integrity of fundamental systems in order to attain their full potential. One line of evidence which supports this is the finding that right hemisphere damage, which occurs before one year of age, may have more depressive effects on cognitive growth than damage to the left hemisphere at an equivalent age, or damage to either hemisphere after one year of age (McFie, 1961 b; Woods, 1980). This greater deleterious effect of early right hemisphere pathology on both verbal and performance IQ scores argues for the participation of the right hemisphere in certain fundamental processes that may underlie both linguistic and spatial competence. Given the specialization of the right hemisphere for the acquisition of spatial skills it appears possible that a certain elementary sensori-motor coordinate system may normally be established by the right hemisphere, and in some way aid the differentiation of more complex skills which do not, at first sight, appear directly connected to it. The importance of elementary sensori-motor expedience in evolving more complex cognitive operations has been stressed by many theorists, and by Piaget (1979) in particular. However, regardless of whether or not the presence of this correspondence between theories of cognitive development and neuropsychological research finding is accepted, the results obtained by McFie (1971a, b) and Woods (1980) emphasize the importance of the presence of a particular structure at a particular stage during development rather than supporting the view that different structures are functionally equivalent.
  
  
are an increasingly common feature of the adult EEG. Measurement of evoked
+
==Aphasia in children==
potentials reveals that peak latencies are long in infancy and decrease as
 
maturation proceeds, whilst in general, amplitude tends to decline after an initial
 
rise. This amplitude trend is also characteristic of the development of the gross
 
EEG (Shagass, 1972). Whilst the behavioural significance of the EEG in man is
 
currently an extremely active research area, the status of the research findings is
 
not always unequivocal. The existence during infancy and childhood of a
 
differential density of waveforms in the left and right hemispheres (Walter, 1950)
 
and the presence of lateral differences in auditory evoked potentials (Molfese,
 
1977) cannot be taken as evidence of functional asymmetry within the cortex at
 
these ages, since they may indicate changes in the thalamus and corpus striatum,
 
which are simply mirrored in an as yet incompletely differentiated and immature
 
cerebral mantle. The EEG data do, however, allow us to see the gradual
 
emergence of intracerebral rhythms whose mean cycle time becomes shorter
 
with age, and whose responsiveness to external stimulation becomes crisper.
 
Furthermore, this developmental trend continues throughout the period from
 
birth to sexual maturity and may actually show reversal in old age (Shagass,
 
1972).
 
  
The impression of a long-term developmental cycle which emerges from
+
The study of language disorders in children is important to a number of problems in developmental neuropsychology. It has provided evidence concerning the extent of functional specialization in the cerebral hemispheres during maturation; data concerning the reorganizational or plastic capacity of the developing brain; and a third, equally important, question, evidence as to the manner in which language becomes established in cortical structures. This question is, in fact, separate from those of hemispheric specialization and plasticity. Here we are concerned with the similarity between the aphasic symptoms of the child and the adult. The greater the similarity of the syndromes the more likely it is that the adult structural pattern has become established, even if subsequently the recovery of the child is more complete because duplication of function in the contralateral hemisphere is still possible. In the present section each of these three topics will be examined, but the characteristics of childhood aphasia will be examined first.
examination of human electrophysiological development perhaps finds even
 
stronger support when neuroanatomical development is examined. It is
 
apparent that although the full complement of neurones is probably present in  
 
the central nervous system at birth, the brain continues to grow in overall size
 
and the characteristic sulcal and gyral pattern of the adult emerges gradually
 
over the first 6 years, and perhaps even later in the case of the frontal lobe
 
(Turner, 1948, 1950). When the internal differentiation of the brain is considered
 
a complex and protracted pattern of development unfolds (Yakovlev and
 
Lecours, 1967; Lecours, 1975). Using the density of myelin, the lipid sheath
 
surrounding the axons of neurones, as a criterion of maturation these workers
 
have mapped the development of CNS pathways and structures and used the  
 
termination of the myelogenetic cycle as an index of when the system reaches
 
final functional maturity.  
 
  
It is apparent from this research that brain development does not proceed
+
The clinical picture found in childhood aphasia was described by Guttman (1942), who noted that despite claims that the syndrome was rare, he had found it not an unusual accompaniment of head injury or intracranial pathology. In contrast to the adult, where complaints with speech difficulties, failures to name objects and paraphrasia are common, the aphasic child is usually apathetic and morose with such extreme poverty of speech that it approaches mutism. Absence of spontaneous speech, lack of willingness to speak, and a hesitant dysarthric telegrammatic-style speech are frequently noted, these symptoms being more common in the younger child. In contrast to the extreme poverty of speech production, comprehension of simple instructions is evident so that parts of the body or objects can be appropriately indicated when a request is made. When prompted to speak difficulties in the manipulation of lips and tongue may be apparent together with failure to produce sound. As recovery progresses, initially the child will speak single words when prompted. It will then move to sparse spontaneous utterances before speech moves into a stage when impoverished but spontaneous conversation occurs with persistent dysarthria. This pattern, which bears the imprint of an almost exclusively motor disorder, occurred in all cases below 10 years of age and occurred regardless of the location of the lesion within a hemisphere. Where damage occurred after the tenth year in some cases speech showed a lack of spontaneity but symptoms more characteristic of the adult pattern with impaired auditory comprehension, syntactical and paraphrasic errors, together with difficulties of naming were found. Dysarthria may or may not accompany these symptoms.
uniformly in all central nervous subsystems. Sensory fibre tracts and associated
 
nuclei myelinate before the cortical intra- and interhemispheric communication
 
systems. Different sensory systems however may show a diversity of time
 
courses. The optic radiations subserving the visual cortex show a short cycle of
 
myelination closely following the myelination of the optic tract, and is virtually
 
complete by 4 months of age. The acoustic radiation subserving the auditory
 
cortex does not show complete development until the 4th year, in marked
 
contrast to the prethalamic auditory system, which is mature by the 4th
 
postnatal month. The intracortical and interhemispheric association fibres,  
 
  
 +
This picture of aphasia in childhood has been supported by subsequent research in which the onset of the language loss is sudden following external injury or internal pathology. In Guttman’s cases the five instances of injury which produced aphasia in which the symptom was exclusively one of speech production difficulty were aged 8 years or below, and the two instances in which speech output was not affected but other aphasic symptoms were present were over 10 years of age. The series of cases reported by Hecaen (1976) show that in two instances where the disorder was exclusively one of speech production the children were aged 6, and in the remaining case 3j years. In children aged 7 years and more, comprehension, naming and paraphrasic disorders were more likely to occur. Both Guttman (1942) and Hecaen (1976) stress the fact that recovery may be extremely rapid, marked improvement sometimes being noted in as little as 6 weeks. In children aged over 10 years however, the time course of the disability may sometimes be prolonged. In middle to late childhood the aphasic symptoms begin to mimic the adult pattern, whereas in early childhood the disorder appears to be purely expressive. In adults expressive aphasia is often produced by lesions located in the anterior region of the hemisphere and difficulties in comprehension occur more frequently with temporal and inferior parietal damage (Geschwind, 1970). However, in children below 10 years, disorders of expression appear to occur regardless of the location of the lesion (Guttman, 1942). A second distinctive feature of the aphasic syndrome in young children is the absence of cases of jargon aphasia, where the speech output is rapid with relatively normal articulation but contains many circumlocutions and paraphrasias (Geschwind, 1972). Woods and Teuber (1978) claim to have one documented case of jargon aphasia in a 5-year-old child, but the clinical description is unlike the adult form. The child produced a stream of meaningless sounds, but when recognizable words were uttered they were most often the names of objects. The child also showed evidence of a purely apraxic disturbance, e.g. sticking out his tongue when asked to blow out a light. To the present author, the picture is too dissimilar to the adult form to be classed as an instance of jargon aphasia, the only feature in common being the high rate of vocal, as opposed to verbal, output.
  
 +
The cases of language loss in childhood so far described were instances where loss was abrupt, following external or internal injury, and where injury was usually confined to one cerebral hemisphere. A rather different type of childhood aphasia occurs when the language loss is associated with either the onset or development of bilateral epileptiform abnormalities (Landau and Kleffner, 1957; Worster-Drought, 1971; Gascon et al , 1973). In these cases, the loss of language is associated with difficulties in understanding speech, which, in some cases, may evolve over a matter of days or weeks. The child shows lack of response to speech, which may be mistaken for peripheral deafness. Audiometric testing reveals either mild or moderate hearing loss, but this loss is insufficient to account for the comprehension disorder and, in any case, hearing usually shows progressive improvement after an initial depression. In some cases auditory evoked potentials to pure tones may be normal, but evoked potentials to speech show abnormalities (Gascon et al ., 1973). Loss of language is gradual and persistent, and while in some cases recovery may occur over a period of years (Landau and Kleffner, 1957), in other cases it appears to be permanent (Worster- Drought, 1971). In some cases loss of speech may be almost total and auditory comprehension limited to less than a dozen words. Despite gross impairment in the development of language, frequently these children do not show impairment on non-verbal tasks in intelligence tests. Of the 14 cases described by Worster- Drought (1971), performance IQ ranged from 96 to 140, with only one case falling below 100. This remains true despite the fact that, in many cases, the onset of pathology is at less than 5 years of age. These cases of bilateral abnormality are in contrast to cases where a unilateral lesion produces aphasia, from which the child subsequently recovers yet shows a low overall IQ (Hecaen, 1976).
  
208
+
When damage to a single hemisphere produces aphasia the child usually recovers language, and in the young child this recovery is usually better than when damage occurs above 10 years (Lenneberg, 1967). This has often been seen as evidence that the two cerebral hemispheres are initially equipotential as far as the development of language is concerned. Further, it has sometimes been claimed that both cerebral hemispheres are involved initially in language development with lateralization increasing with age (see Dennis and Whitaker, 1977 for a review). It has already been noted that as far as attainment on certain language tests is concerned the two hemispheres are not equivalent. The view that the right hemisphere is involved in language acquisition in the infant and young child comes from reports of the high incidence of speech disturbances following right hemisphere damage. The incidence of language disorders with lesions of the left and right hemispheres described by different researchers varies widely. In the case of the left hemisphere, damage has been estimated to produce language disorder with an incidence varying from 25% (Ingram, 1964) to over 90% (Dunsdon, 1952). In the case of the right hemisphere the estimated incidence has varied from less than 1 % (Ingram, 1964) to nearly 38 % (Dunsdon, 1952). Only one investigator has claimed an equal frequency of language disorder following either left or right cerebral damage (Basser, 1962). The discrepancies seem too large to attribute to statistical sampling fluctuations. One of the problems encountered in this area is the definition of what constitutes an aphasic language disturbance. Language difficulties are associated with depressed general intelligence (Mein, 1960) so that severe brain damage which produces severe retardation may produce language disturbance indirectly. There is also the problem of whether speech disturbance should be considered an aphasic disturbance (Ingram, 1965). It is already apparent that the syndrome of aphasia • in children may vary from almost total mutism to a clinical picture similar to that of the adult with comprehension disturbance and naming impairment. That the type of impairment can vary not just with age of the child but also be related to the damaged hemisphere can be seen by examining the series of Hecaen (1976). Of 6 cases of right hemisphere damage, only the two youngest (6 and 3^ years) showed any disturbance and this was articulatory. Bishop (1967) has reported that in cases of infantile hemiplegia, articulatory disturbances are equally likely following damage to either hemisphere, but that left hemisphere damage additionally delays the acquisition of word combinations rather than single words.
  
 +
The possibility of a different pattern of impairment following left and right hemisphere injury is not the only factor which complicates the issue. Woods and Teuber (1978) have pointed out that there is a tendency for investigators since 1940 to report a lower incidence of aphasia following right hemisphere injury than earlier workers. They attribute this to the fact that in older investigations aphasias and hemiplegias were frequently complications of systemic infectious illnesses such as scarlet fever, bacterial pneumonia and diphtheria, which can produce not only focal lesions but also diffuse bilateral encephalopathy. Undoubtedly the frequent reliance on hemiplegia alone as the sign indicating exclusive damage to one hemisphere is likely to result in the inclusion of cases where a less extensive pathology is also present in the hemisphere that is assumed to be intact. Bearing these facts in mind, it would obviously be hazardous to speculate concerning the true incidence of language disturbance following right hemisphere pathology. For the moment it is sufficient to say that the incidence of aphasia following right hemisphere damage may be considerably less than previously thought, perhaps as little as 5 % in those who were previously right-handed (Woods and Teuber, 1978).
  
 +
A finding that has already been mentioned several times is that concerning the capacity of the right hemisphere to acquire language following early left hemisphere injury. There is little doubt that the capacity to transfer language to the right hemisphere is a real factor in the recovery from aphasia in children. However, it cannot be assumed that in every case of childhood aphasia recovery of language is due to transfer to the contralateral hemisphere. Milner (1974) noted, on the basis of the Wada test, that in adults who were left-handed but had sustained early left hemisphere damage, language was present in the left hemisphere in 30 % and bilaterally present in 16 % of cases. Thus, in 46 % of cases who had left hemisphere injury, the left hemisphere was still involved in language to some degree. Whether or not language transferred depended on whether certain critical areas were damaged. In cases where left hemispherectomy is performed, following widespread unilateral damage, it is clear that the presence of linguistic competence is dependent on the remaining hemisphere (Dennis and Whitaker, 1977). When such language transfer does occur, while verbal IQ may not be significantly depressed relative to performance IQ, it should be remembered that such tests do not directly sample knowledge of language structure. Where tests are designed to evaluate grammatical comprehension then deficits appear (Dennis and Kohn, 1975; Teuber, 1975; Dennis and Whitaker, 1976; Day and Ulatowska, 1979). However, with these reservations in mind, children exposed to left hemispherectomy do show an adequate degree of language competence in relation to their overall IQ and it has frequently been remarked that it would be an incredible improvement if each adult aphasic could recover the same level of language competence (Geschwind, 1972).
  
 +
The duration of such plasticity in the developing brain has been the subject of disagreement. Lenneberg (1967) believed that the period of plasticity in regard to language mechanisms lasted until puberty. Krashen (1973) has challenged this view mainly on the basis that right hemisphere damage above the age of 5 does not often produce aphasia whereas below this age it frequently does. However it should be understood that the issue of the degree to which both hemispheres are involved in language acquisition early in life (and evidence has already been cited that right hemisphere aphasia may be quite different in form from left hemisphere aphasia in young children) is quite a different one from the question of whether interhemispheric transfer is possible. Children between 5 and 10 years do show good recovery from aphasia and it would be surprising indeed if language could have survived in the left hemisphere given the extent and severity of the damage in some instances, e.g. right hemiplegia and hemianopsia (Hecaen, 1976). On the balance the evidence would appear to favour a period of plasticity extending to at least 10 years of age. There is even some indication that a period of reduced plasticity may extend far beyond this age although whether it involves inter-hemispheric transfer or improved within-hemisphere recovery is another question. Teuber (1975) noted that an analysis of 167 cases of brain injury sustained during the Korean campaign showed that the population who were under 22 at the time of injury showed better recovery of language than those who were 23 years and over. It may be premature then to try to set rigid cut-off points for recovery.
  
 +
The evidence presented here suggests that aphasia in children is not one syndrome but several. In children of 6 years and below mutism and dysarthria appear as the main symptoms with comprehension being relatively well preserved. Furthermore this pattern appears to occur regardless of whether the lesion is in the left or right hemisphere and also appears to be insensitive to the precise location of the lesion within a hemisphere (whether it is frontal, temporal or parietal). Above 6 years, symptoms which are regarded by many as truly aphasic (comprehension and naming disorders) appear. The symptoms appear to occur largely following left rather than right hemisphere lesions. Between the ages of 6 and 14, jargon aphasia in its adult form is infrequent although the extended circumlocutions that are one of the characteristics of aphasia do occur (Guttman, 1942). The rapidity of the recovery process in some cases and, in very young children, the preservation of comprehension, makes it extremely unlikely that language has been totally relearned by the right hemisphere (Geschwind, 1972). This factor has suggested to some investigators that the right hemisphere must be involved in linguistic processing at an early developmental stage and in fact retains some capacity for comprehension even in the adult after cerebral differentiation (Kinsbourne, 1975).
  
which allow communication between different regions and whose disruption
+
It is possible then that during the early stages of language learning both hemispheres acquire comprehension and share control of the speech mechanism. This may be necessary in the initial stages, because fine bilateral control of the speech mechanism is required since suitable motor synergisms for a culture- specific phoneme system are not yet well established in subcortical structures. The consequence of this arrangement is that a lesion to either hemisphere can disrupt speech production but comprehension is relatively unaffected because the structural basis of language as opposed to speech does not require a bilateral component. However, the establishment of subcortical synergisms for the execution of the basic components of speech production together with the presence of structurally more specialized language mechanisms in the temporoparietal region of the left hemisphere normally leads to left hemisphere capture of the speech output mechanism. This process is probably a gradual one, but as it proceeds there is less functional demand for right hemisphere processing of language and there may even be active inhibition of its linguistic processing by the left hemisphere. Eventually this isolation of the right hemisphere may lead to structural changes at the synaptic level so that the re-establishment of control is no longer possible. To the extent that this isolation process is incomplete transfer of control is still possible. Thus in young children (under 5 years) the loss of the left hemisphere will show itself in only transitory speech output disturbances since this process of capture is just beginning and both hemispheres are still involved. Even at this age however the linguistic superiority of the left hemisphere is already apparent (see Young, Chapter 6, this volume, for a review of the psychophysical literature), and it is in fact this superiority that will allow the eventual suppression of the right hemisphere. In children between the ages of six and ten years the speech mechanism is probably under the control of the left hemisphere but right hemisphere control mechanisms have not yet functionally atrophied. Left hemisphere damage at this age can produce speech disturbances solely and/or truly aphasic disturbances which are transitory, while damage to the right hemisphere only rarely affects these mechanisms. With the passage of time however, the capability of the right hemisphere wanes through disuse and in the majority of cases only a token linguistic capacity remains. Even if in later life the possibility of direct inhibition by the left hemisphere is removed, by severing the corpus callosum, the right hemisphere has residual linguistic comprehension but remains mute (Gazzaniga and Sperry, 1967). This is probably because the process of gaining control of the speech mechanisms involves the regulation of neuromuscular synergisms at subcortical levels, and these remain under left hemisphere control. It should be noted that the control of the vocal apparatus by the left hemisphere may be specific to its use in the context of spoken language. Where lesions of the left hemisphere produce expressive (Broca’s type) aphasia the ability to use the voice in the context of singing including the fluent production of words may be well preserved (Yamadori et al ., 1977). Evidence for a motor capture account of left hemisphere language dominance can also be found in studies of adult aphasics (cf. Kinsbourne, 1975).
leads to many of the bizarre neuropsychological disconnection syndromes
 
(Geschwind, 1965), have prolonged maturational cycles extending into the  
 
second decade of life. Examination of the cortex itself indicates that some regions
 
implicated in linguistic competence (inferior parietal lobule) show a slow onset
 
of myelination and that this process may also continue beyond the second
 
decade of life. It should be emphasized that although the study of the  
 
myelogenetic cycles of maturation shows a complex extended pattern of  
 
development from birth to maturity, a caveat is necessary. Neural conduction
 
can occur in fibres before they become myelinated (Ulett et al , 1944) and indeed
 
myelination may be aided by neural activity (Langworthy, 1933). However,
 
myelin contributes greatly to the efficiency and speed of neural conduction,
 
which underlies the complex analysis and planning characteristics of human
 
cognition and action. The importance of myelin may be appreciated by
 
considering the devastating behavioural effects of demyelination disease in man
 
such as occurs in multiple sclerosis. The myelogenetic analysis emphasizes the  
 
manner in which the brain becomes structurally mature. Phylogenetically older
 
structures, in general, mature earlier than those of recent phyletic origin. There
 
are exceptions to this, for example the reticular formation, whose developmental
 
cycle again extends into the second decade of life, partly no doubt because its
 
final operational capability is not required until cortical systems are completely
 
mature.  
 
  
Both the electrophysiological and neuroanatomical data indicate that the
 
human central nervous system develops over an extended period. Particularly
 
fascinating are the observations that the higher auditory systems (geniculo-
 
temporal pathways) exhibit a developmental cycle that is more than ten times
 
longer than visual structures at the same level of the CNS. It is probable that this
 
reflects the necessity of incorporating into the growing brain the species specific
 
demand of learning the complexities of language via the acoustic mode and
 
allows for the building of the culture-specific phoneme system which is
 
eventually used. However, it is apparent that a considerable part of the
 
developing child’s life is characterized by the presence of cortical structures
 
which are functionally (by electrophysiological and anatomical criteria)
 
immature. The status that these immature structures have in subserving the
 
growing child’s cognitive repertoire is not straightforward. It is possible to
 
envisage the mapping of cognitive growth within the cerebral structures which
 
subserve cognition in the adult in at least two ways. The first view would regard
 
all those structures which are involved in a given functional system in the adult
 
as also being involved in infancy, although the immaturity of the system
 
considered as a whole would limit its capabilities. The limitations seen for
 
instance in perceptual and motor systems in the neonate would be ascribed to
 
the immaturity of the cortical system, which was nevertheless functional, rather
 
  
 +
==The plasticity of the developing brain==
  
 +
It is usually accepted that the younger the individual when the brain sustains injury, the greater the resilience and the greater the capacity for functional restitution. Against this one must set the view that the developing brain is particularly vulnerable and long-term effects emerge if normal development is impaired. These two views may be partially reconciled by proposing that following early brain damage, specific skills may be spared but at a cost that will be seen in the overall lowered cognitive capacity of the brain (Teuber, 1975). Thus language or visuo-spatial skills may be spared following left or right hemisphere injury respectively, but intellectual achievement as measured by IQ tests or by school performance will show depression. Evidence already cited concerning the specific effects of early brain damage makes it clear that the consequences are not just seen in a uniformly lowered total processing capacity but depend on the site of injury. Language achievement is specifically lowered following left hemisphere injury and spatial skills depressed specifically following right hemisphere injury.
  
DETERMINATE AND PLASTIC PRINCIPLES
+
The evidence in favour of a greater degree of plasticity comes from a number of sources. Some animal species show spared sensory capacity following cortical lesions in infancy (Schneider, 1969) while in other species age at time of injury does not appear to affect the magnitude of the deficit (Doty, 1973). Even where pattern vision is spared following early lesions of the striate cortex, the animals may still take longer to pretrain before formal testing can commence (Schneider, 1970). In man there is evidence of age-related sparing of sensory function. Rudel et al (1974) noted minimal impairment in brain damaged children on somaesthetic thresholds but these children were still impaired on tactile object recognition. Elementary motor function in children may also show greater savings following early massive unilateral injury (Cairns and Davidson, 1951), but such abilities as are preserved, are rudimentary. In man following early unilateral damage that is extensive enough to destroy large areas of the striate cortex, the visual field defects are similar to those produced in adults with similar pathology (Paine, 1960). In this case it might be expected that savings would be possible given the existence of a second, phylogenetically older, visual structure in the midbrain. Where lesions are more restricted, however, savings on visual (in terms of shrinkage of the size of scotoma), somatosensory and motor functions are age-related and show relatively better recovery even when damage occurs early in the third decade of life as compared to later (Teuber, 1975). Without doubt however, the most outstanding examples of functional recovery are those which occur in the areas of language and spatial skills in man following early injury.
  
 +
The explanation of the functional recovery that does occur following early brain damage is not straightforward. As discussed above, part of the restitu- tional capacity may lie in mechanisms that enable individual neurones to withstand injury so the functional extent of a lesion may be less than in the mature system. It may also lie in neural regeneration per se, although Schneider (1979) has provided evidence that such anomalous regeneration, when it occurs, may actually result in greater behavioural deficit. In the case of the somatosensory and motor systems, while the greater volume of neural circuitry is concerned with analysis and control of the contralateral side of the body, ipsilateral pathways do exist. In the case of the motor system there is even evidence that hypertrophy of ipsilateral pathways occurs after early hemi- spherectomy (Hicks and D’Amato, 1970). These ipsilateral pathways may assume greater functional importance in the case of unilateral brain damage and sustain the limited behavioural savings that occur. The continued development of linguistic and spatial skills after early brain damage are however of a different order. It has been suggested that the survival of these skills in one hemisphere is due to the fact that the necessary processors exist initially in each hemisphere but that during development one hemisphere suppresses the influence of the other. This suppression of the influence of the contralateral hemisphere may be a necessary prerequisite for the development of higher cognitive skills, since processing space may be at a premium. When both language and spatial skills are acquired by only one hemisphere (following early hemispherectomy) neither skill reaches its full potential (Teuber, 1975). Where the corpus callosum is absent during development, and normal interhemispheric communication is consequently impossible, a rather bizarre pattern of cognitive development is seen. In such cases of callosal agenesis it appears that either performance IQ or verbal IQ becomes pre-eminent despite the existence of functional capacity in two hemispheres (Dennis, 1977). Extreme discrepancies do not in these cases appear to be predictable from age of the subject at the time of testing, sex, type of agenesis, handedness or specific neurological signs. It appears rather that a mechanism which enables a normal balance of cognitive skills to occur is absent. In the normal individual then the existence of two intact hemispheres may not be sufficient for normal cognitive growth. Some additional mechanism which ensures that unnecessary duplication does not occur and enables an efficient use of available processing capacity seems to be necessary. The consequence of the presence of such a mechanism during development is that usually specific skills become established predominantly in one hemisphere or the other and once they are so established there is little opportunity to recapitulate the process. The failure of the adult brain to fully re-establish linguistic or spatial skills following damage is a consequence of the presence of a mechanism (whose effector path is the corpus callosum) that enables a balanced and complete cognitive growth to occur.
  
209
 
  
 +
==Conclusions==
  
than to the fact that lower but morphologically more mature structures are
+
Consideration of the evidence concerning the outcome of brain injury in the developing nervous system leads to the inescapable conclusion that age at the time of injury is a critical factor in determining both the initial syndrome and the pattern of adaptation that follows. Certain abilities such as early maturing spatial skills, language and various elementary sensory and motor functions may show relative recovery, the extent being determined by the location and size of the lesion. Other abilities, particularly those involving fine motor coordination, late maturing spatial skills as well as the overall level of intellectual attainment, may show more profound defects. These latter effects may be partly ascribed to a lower overall processing capacity, but in the case of general intellectual attainment, more profound effects are seen following damage to the right hemisphere before (compared with after) one year of age, a factor which argues that volume of tissue damaged is not the sole consideration. Differing patterns of language disturbances are also seen in children depending on the child’s age at the time pathology develops. These considerations, which emphasize that damage is occurring within a system whose state is continually changing, present particular difficulties for those with interests in the outcome of early brain damage. As Teuber and Rudel (1962) point out: ‘Whether we are working with infrahuman forms or with children, we must define (1) those aspects of behaviour in which the effects of early injury appear only with a delay, as development progresses; (2) those other aspects of performance in which there will be impairment at all ages; and finally, (3) those aspects of performance where there is an immediate effect which, however, disappears as development proceeds’. The interpretation of research which finds age-dependent differences is often far from clear. Reports that the patterning of IQ subtests is insensitive to the location of injury in young children may be a genuine indication of an age- dependent difference, despite the fact that such tests were not specifically designed to assess brain damage. However, since it is found that in adults that IQ tests are only indicative of lesion laterality in the acute but not the chronic phase (Fitzhugh et al ., 1962), the failure to find specific indication of lesion location in children with infantile injury may be attributable to the interval between injury and testing rather than an age-related difference in functional organization.
controlling the behaviour. The alternative view would regard neurobehavioural
 
development as a process beginning with relatively primitive analysis and  
 
response control systems residing in phylogenetically older structures which
 
mature earlier in the developmental sequence. As development proceeds,  
 
phylogenetically newer structures, which attain maturity later in the developmental sequence, will capture and modulate the activity of the older systems as  
 
well as adding more complex control processes. This process will not have a  
 
uniform time course across all systems. In the case of the visual system this
 
transition may occur relatively early in development at two to three months of  
 
age since the cortical network in this case has a short developmental cycle. In the  
 
case of audition the whole process may be more protracted with cortical control
 
becoming ascendant in the period of 2-4 years, whilst in the complex action
 
systems controlled by the frontal lobe, the processes may take even longer, given
 
the differential growth of the region beyond 6 years of age (Turner, 1948, 1950).  
 
Evidence that it is this latter view which is the more reasonable description of  
 
neurobehavioural development comes from a number of observations that will
 
be subsequently outlined, but it must be said in advance that the case is by no
 
means proven.  
 
  
 +
The emergence of specific functional deficit following early brain injury stresses the importance of critical structures for cognitive achievement. Just how extensively the predesignated structures of the nervous system determine the detailed characteristics of cognitive development remains to be seen. It is only relatively recently that explorations of the specific patterns of loss, as measured by specially developed tests, have begun. It is also apparent that much of the research has been concerned with hemispheric asymmetry where the structural similarity of the hemispheres means that the capacity for interhemispheric reorganization may lead to an over-valuation of the plastic capacities of the developing brain. Cases where bilateral loss of a structure is involved give one much less confidence in the restitutional capacity of the young brain. Bilateral frontal lobe damage in childhood appears to have effects at least as serious as equivalent damage in adults (Russell, 1959; Ackerly, 1964) although the paucity of research in this area and the anecdotal nature of some of the findings make conclusions tentative. There is a scarcity of unequivocal evidence that areas of the brain not normally involved in the development or performance of specific functions may assume those functions when other areas are damaged. Goldman and Lewis’s (1978) demonstration that the dorsolateral prefrontal cortex in the macaque may assume some of the functional capability of the orbitofrontal cortex, provided damage occurs early in development, remains one of the few clear demonstrations of such effects in the CNS of primates following bilateral lesions. However, the fact that the normal limits of plasticity and the extent to which they may be influenced by specific experience remain undetermined, gives developmental neuropsychologists particular problems in understanding the precise nature of brain-behaviour interrelations. Nevertheless, the fact that plasticity is a real phenomenon and may be influenced by specific experience (Goldman and Lewis, 1978) gives some hope that understanding of its nature may lead to more effective remediation regimes designed to capitalize on its characteristics.
  
Neuropsychological evidence concerning functional maturation
+
Acknowledgements
  
When damage occurs in the mature brain the effects are usually immediate; the
+
I am grateful to H. D. Ellis and E. A. Salzen for advice and discussion during preparation of this manuscript.
degree of functional loss, whether it be sensory, motor or cognitive, is greatest
 
immediately after the lesion and usually shows some remission over time. In the
 
immature brain in a number of instances the pattern is almost the reverse of this.  
 
In the case of hemiplegia, sustained as a consequence of prenatal or perinatal
 
injury, the symptoms of the disorder frequently emerge gradually over a
 
prolonged period. Abnormalities in the use of the hand and arm may emerge at
 
between 4 and 6 months, whilst differences in the behaviour of the legs may not
 
become apparent until 10 months of age or more. Deficits in the use of the lower
 
limbs may only become apparent when the child begins to walk, a milestone that
 
is frequently attained in the normal age range (Lyon, 1961). Finally, athetoid
 
movements do not make their appearance until much later, typically between
 
three and four years of age (Lenneberg, 1968). Thus the developmental pattern is
 
seen to move through a series of stages: for example, the grasp reflex is present
 
initially in both the affected and the normal hand, but it persists on the affected
 
side and usually the hand becomes clenched into a tight fist. Individual finger
 
movements do not appear on the hemiplegic side, although movement of the
 
thumbs may be possible. As the child grows, then, the deficit becomes more
 
severe. However, it is noticeable that these children escape some of the more
 
drastic consequences of hemiplegia resulting from cerebral injury at maturity.  
 
  
  
 +
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Annet, M., Lee, D. and Oimsted, C. (1961) Intellectual disabilities in relation to lateralised features of the EEG. Little Club Clin. Devel. Med., 4, 86-112.
  
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Basser, L. S. (1962) Hemiplegia of early onset and the faculty of speech with special references to the effects of hemispherectomy. Brain, 85, 427-459.
  
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Bay, E. (1975) ‘Ontogeny of stable speech areas in the human brain’, in Foundations of Language Development, Yol. 2 (eds. E. H. Lenneberg and E. Lenneberg), Academic Press, London, 21-29.
  
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Bishop, N. (1967) ‘Speech in the hemiplegic child’, in Proc. 8th Medical and Educational Conference of the Australian Cerebral Palsy Association, Tooronga Press, Melbourne, 141-153.
  
The severity of paralysis in the upper limb is less and the lower limb is capable of
+
Boll, T. J. and Reitan, R. M. (1972) Comparative ability interrelationships in normal and brain injured children. J. Clin. Psychol, 28, 152-156.
greater use than after comparable damage in adults. That the residual function
 
on the affected side is not attributable to surviving undamaged tissue in the
 
diseased hemisphere is shown by the fact that removing the diseased hemisphere
 
later in development does not cause further impairment and may frequently
 
result in improvement (Cairns and Davidson, 1951).  
 
  
Two features then are apparent in these cases. The first is the greater capacity
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of the young brain to compensate and escape some of the consequences of
 
equivalent injury in adulthood—its plastic propensity. The second feature is
 
cogently described by Lenneberg (1968): ‘one may say that the child with a
 
perinatal cerebral injury only gradually grows into his symptoms’. This
 
emergence of deficit with age is compatible with the view that certain systems are
 
pre-programmed to appear at certain stages in development and injury to them
 
will only become apparent when they fail to appear. Similar affects in the motor
 
sphere were observed by Kennard (1940) in macaque monkeys where ablation of
 
the motor cortex in infancy resulted in surprisingly little immediate effect, but
 
precluded the development of fine manipulatory skills, and this, together with
 
signs of dyskenesia, became more apparent as the animals grew older. It appears
 
that the motor cortex only begins to exert its influence gradually and its loss or
 
malfunction may not become apparent until a later stage of development.  
 
  
Further support for the notion that behaviour early in development may be
+
Bronson, G. (1974) The postnatal growth of visual capacity. Child Devel, 45, 873-890.
mediated exclusively by subcortical structures, with cortical processors
 
becoming involved later, has been provided by Goldman (1976). It has been
 
apparent for some time that tasks which require a monkey to remember the
 
location of a stimulus over a brief interval of time are drastically affected by
 
damage to the dorsolateral prefrontal cortex (Chow and Hutt, 1953). These are
 
known as the delayed-response and delayed-alternation tasks. When the
 
dorsolateral frontal cortex is removed within the first 2 months of life however,
 
the operated animals perform as well on this task as unoperated controls as long
 
as testing is carried out within the first year of life (Harlow et al , 1970). If these
 
monkeys are followed into the second year of life they show evidence of
 
increasing impairment of delayed response tasks. Lesions in subcortical
 
structures which are functionally connected with the dorsolateral prefrontal
 
cortex (dorsomedial nucleus of the thalamus and the head of the caudate
 
nucleus), indicate that the monkeys operated on as juveniles show the same
 
pattern of deficit as adults, i.e. failure on delayed alternation tasks (Goldman,
 
1974). These results emphasize that not only may the effects of brain damage fail
 
to appear early in development and only reveal themselves as the animal grows,  
 
they also show that structures which are required for the adequate performance
 
of a task in adulthood (the dorsolateral prefrontal cortex), are not necessary for
 
the performance of the same task when the animal is an infant or a juvenile.  
 
  
These experiments contribute a salutary warning to those who would assume
+
Bryan, G. E. and Brown, M. H. (1957) A method for differential diagnosis of brain damage in adolescents. J. Nerv. Ment. Dis., 125, 69-72.
  
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Byers, R. K. and McLean, W. T. (1962) Etiology and course of certain hemiplegias with aphasia in childhood. Pediatrics, 29, 376-383.
  
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Cairns, H. and Davidson, M. A. (1951) Hemispherectomy in the treatment of infantile hemiplegia. Lancet, ii, 411-415.
  
DETERMINATE AND PLASTIC PRINCIPLES
+
Chase, H. P. (1973) The effects of intrauterine and postnatal undernutrition on normal brain development. Ann. New York Acad. Sci., 205, 231-244.
  
 +
Chow, K. L. and Hutt, P. (1953) The association cortex of Macaca mulatta: a review of recent contributions to its anatomy and functions. Brain, 76, 625-677.
  
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Cobrinik, L. (1959) The performance of brain-injured children on hidden figure tasks. Amer. J. Psychol, 72, 566-571.
  
 +
Day, P. S. and Ulatowska, H. (1979) Perceptual, cognitive and linguistic development after early hemispherectomy: two case studies. Brain and Lang., 1, 17-33.
  
that, because a cortical structure is implicated in a functional system in
+
Dejerine, J. (1892) Contribution a l’etude anatomopathologique et clinique des differentes varieties de cecite verbale. C. R. Soc. Biol, 4, 61-90.
adulthood it must of necessity be involved in performance of those same
 
functions at an earlier developmental stage. In infant and juvenile macaques
 
subcortical systems are capable of mediating responses which in adults require
 
the participation of the cortex. Furthermore, evidence is available which
 
indicates that the time course over which the effects of cortical lesions become
 
apparent during development differs for different regions. While monkeys aged
 
2\ months with orbital frontal cortex lesions are equivalent to unoperated
 
controls in the performance of object reversal learning, deficits in performance
 
became apparent by the time the animals are one year old (Goldman, 1974).  
 
Thus, while the effects of dorsolateral frontal cortex damage sustained in infancy
 
on delayed alternation tasks do not become apparent until after one year of age,  
 
the effects of orbitofrontal damage in infancy on object reversal learning
 
become apparent before one year of age. In the case of both delayed alternation
 
and object reversal learning early in development subcortical structures are
 
capable of mediating the behaviour successfully. With respect to these studies it
 
should be pointed out that macaque monkeys attain sexual maturity between 24
 
and 30 months of age, so the effects of early brain damage may take a
 
considerable proportion of the developmental cycle before they become
 
apparent.  
 
  
The evidence cited so far has argued for a model of development in which the
+
Dejerine, J. and Andre-Thomas, J. (1912) Contribution a l’etude de l’aphasie chez les gauchers. Rev. Neurol, 24, 213-226.
complete maturational cycle is prolonged, but within which different systems
 
may attain functional maturity at widely divergent times. Initially, behaviour
 
may be controlled by subcortical systems, and depending on the time-course of
 
the maturational cycle in the higher reaches (cortical) of each system so control
 
will pass to the phylogenetically newer and more adaptive system. Bronson
 
(1974) has argued, on the basis of changes in the pattern of visual behaviour in
 
infants, that in the case of the visual system a transfer of control passes from the
 
superior colliculus to the striate cortex, from the ‘ambient’ to the ‘focal’ system
 
(Trevarthen, 1968), during the 2nd and 3rd postnatal month. Such a view is
 
certainly compatible with the rapid postnatal development of the geniculo-  
 
striate system (Yakovlev and Lecours, 1967). In the case of motor function the
 
longer maturational cycle of the medullary pyramids (up to 12 months), which
 
carry the axons of the Betz cells of the motor cortex to the spinal cord and are
 
required for control of individual fingers and skilled sequences (Lawrence and
 
Hopkins, 1972), leads one to expect that transition of control in this case may
 
take place over a more protracted period. The emergence of comparative motor
 
deficit between affected and normal side, in cases in infantile hemiplegia, between
 
4 and 12 months of age (Lyon, 1961) appears to reflect this longer cycle of
 
development. In man, however, the long-term emergence of a deficit in
 
previously established skills after early brain injury akin to that reported by
 
Goldman (1974, 1976) for the macaque monkey, has not as yet been reported.  
 
  
 +
Dennis, M. (1977) ‘Cerebral dominance in three forms of early brain disorder’, in Topics in Child Neurology (eds. M. E. Blaw, I. Rapin and M. Kinsbourne), Spectrum Publications, London, 189-212.
  
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Dennis, M. and Whitaker, H. A. (1976) Language acquisition following hemidecortication: linguistic superiority of the left over the right hemisphere. Brain and Lang., 3, 404-433.
  
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Dennis, M. and Whitaker, H. A. (1977) ‘Hemispheric equipotentiality and language acquisition’, in Language Development and Neurological Theory (eds. S. J. Segalowitz and F. A. Gruber), Academic Press, London, 93-106.
  
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Dobbing, J. (1968) ‘Vulnerable periods in developing brain’, in Applied Neuro chemistry (eds. A. N. Davidson and J. Dobbing), Blackwell, Oxford, 287-316.
  
 +
Doty, R. W. (1973) ‘Ablation of visual areas in the central nervous system’, in Handbook of Sensory Physiology, Vol. Ill, 3B, Central Processing of Visual Information (ed. R. Jung), Springer Verlag, Berlin, 438-541.
  
 +
Dunsdon, M. I. (1952) The Educability of Cerebral Palsied Children. Newnes, London.
  
Nevertheless, evidence is available which indicates that, on some perceptual
+
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tasks, brain-damaged children may show either a consistent difference from
 
controls over a wide age range (Cobrinik, 1959), or a progressive change, which
 
either diverges from or converges to control values between the ages of 5 and 15
 
years depending on the particular measure being considered (Teuber and Rudel,
 
1962). Thus, slowly emerging effects of early brain damage in man are not
 
unknown, but long-term effects, with an intervening ‘silent’ interval, have not, to
 
the present author’s knowledge, been described.  
 
  
 +
Fitzhugh, K. B., Fitzhugh, L. C. and Reitan, R. M. (1962) Wechsler-Bellevue comparisons in groups of‘chronic’ and ‘current’ lateralized and diffuse brain lesions. J. Consult. Psychol, 26, 306-310.
  
Interactive effects and their interpretation
+
Flourens, P. (1824) Recherches Experiment ales sur les Proprietes et les Fonctions du Systeme Nerveux dans les Animaux Vertebres. Crevot, Paris.
  
Generalized effects on intelligence that result from presumed structural
+
Galaburda, A. M., Le May, M., Kemper, T. L. and Geschwind, N. (1978) Right-left asymmetries in the brain. Science, 199, 852-856.
incapacity (Hebb, 1942) or following localized injury (Thompson, 1978) have
 
indicated that while early injury may produce generalized depression of full-
 
scale IQ, late injury produces a more specific pattern of deficit, with less
 
depression of full-scale IQ. Research findings of this nature can be seen as
 
support either for a model of brain development in which neural structures only
 
gradually attain their mature state, or alternatively, as support for the view that
 
reorganizational capacities are at work during development which allow savings
 
on specific skills but at the cost of overall depression in intellectual attainment.  
 
However, there is no doubt that both views are valid and have independent
 
evidence to support them. The developing brain is more vulnerable than the
 
mature brain and this can be seen in the long term generalized deleterious
 
consequences of nutritional deprivation during the brain-growth spurt, as
 
measured by both neurochemical and anatomical criteria (Dobbing, 1968), and
 
by behavioural criteria (Chase, 1973). However, it is also clear that substantial
 
left hemisphere damage, which usually leads to long-term severe dysphasia in
 
adulthood, results in only transitory dysphasic symptoms when the damage
 
occurs early in childhood (Hecaen, 1976), and there is evidence of savings in
 
visuo-spatial skills following early right hemisphere dysfunction, which is not
 
apparent with equivalent damage at maturity (Kohn and Dennis, 1974).  
 
  
These findings provide unequivocal evidence of the reorganizational and
+
Gascon, G., Victor, D., Lombrosso, C. T. and Goodglass, H. (1973) Language disorder, convulsive disorder and electroencephalographic abnormalities. Arch. Neurol, 28, 156-162.
plastic capacities of the developing brain. However, it is also evident that the
 
usual predetermined pattern of left hemisphere specialization for language and
 
right hemisphere specialization for visuo-spatial skills set limits to this plastic
 
capacity. Where one hemisphere has sustained early injury, the language skills
 
exhibited by a remaining and intact right hemisphere are less proficient than
 
those exhibited by a remaining intact left hemisphere (Dennis and Kohn, 1975).  
 
It also appears that visuospatial abilities are better developed in an intact right
 
hemisphere than when the left hemisphere alone remains fully functional (Kohn
 
and Dennis, 1974). Thus, while reorganization is possible following early brain
 
injury, this may be more limited than has been previously thought. Indeed, given
 
  
 +
Gazzaniga, M. S. and Sperry, R. W. (1967) Language after section of the cerebral commissures. Brain, 90, 131-148.
  
 +
Geschwind, N. (1965) Disconnexion syndromes in animals and man. Brain , 88, 237-294 and 585 644.
  
DETERMINATE AND PLASTIC PRINCIPLES
+
Geschwind, N. (1970) The organisation of language and the brain. Science, 170, 940-944.
  
 +
Geschwind, N. (1972) Disorders of higher cortical functions in children. Clin. Proc. Child. Hosp., 28, 261-272.
  
213
+
Gloning, I., Gloning, K. and Hoff, H. (1963) ‘Aphasia—a clinical syndrome’, in Problems of Dynamic Neurology (ed. L. Halpern), Jerusalem Post Press, Jerusalem, 63-70.
  
 +
Goldman, P. S. (1974) ‘An alternative to developmental plasticity: heterology of CNS structures in infants and adults’, in Plasticity and Recovery of Function in the Central Nervous System (eds. D. G. Stein, J. J. Rosen and N. Butters), Academic Press, New York, 149-174.
  
the anatomical asymmetry present in the neonatal brain (Wada et al, 1975) it
+
Goldman, P. S. (1976) ‘Maturation of the mammalian nervous system and the ontogeny of behavior’, in Advances in the Study of Behavior, Vol. 7 (eds. J. S. Rosenblatt, R. A. Hinde, E. Shaw and C. Beer), Academic Press, London, 1-90.
would be surprising if this structural specialization were not detectable at some
 
stage in the behavioural effects of unilateral brain injury. The results of unilateral
 
brain injury in early development nicely juxtapose two major tendencies which
 
emerge from neurobehavioural research: on the one hand, the trend towards
 
carrying through the construction of a preprogrammed system over a protracted
 
time period and, on the other, an adaptive plastic capacity which allows the
 
partial redirection of functional systems should damage occur.  
 
  
The complexity of the processes involved in the analysis of sensory information (Hubei and Wiesel, 1963; Werner and Whitsell, 1973) that has emerged
+
Goldman, P. S. and Lewis, M. E. (1978) ‘Developmental biology of brain damage and experience’, in Neuronal Plasticity (ed. C. W. Cotman), Raven Press, New York, 291-310.
from single neurone recording makes it clear why a great deal of preprogramming must be involved in the construction of complex adaptive neural
 
systems. It is less easy to describe the mechanisms which allow complex brain
 
systems to exhibit the degree of plasticity that they evidently do in early
 
development. The explanation may reside in the fact that younger individuals
 
are less susceptible to transneural degeneration effects and also show higher
 
levels of biosynthetic activity in brain tissue, which may allow damaged
 
networks greater restitutional capacity (see Goldman and Lewis, 1978, for
 
review). It is also evident that behavioural recovery, seen after early injury in
 
some cases, depends on the ability of young animals to profit from experience in
 
a way not available to the adult. Monkeys sustaining brain injury in infancy
 
show greater recovery the earlier training experience is given in development,  
 
although the ability to profit from this experience depends on the nature of the
 
task and the site of the lesion in the brain (Goldman and Lewis, 1978). The
 
results of this study gave some indication that it was the nonspecific stimulation
 
effects of the training which were important in recovery, rather than specific
 
carry-over from common features of the task.  
 
  
The fact that experience per se may be an important factor in promoting
+
Goldstein, K. (1939) The Organism. American Book Publishers, New York.
recovery is of considerable importance, since there has been suspicion about the
 
value of training programmes in the recovery from brain damage (Byers and
 
McLean, 1962). Given the intricacy of the neurobiological factors involved in
 
early brain injury it may be too easy to forget about the cognitive dimension.
 
During development a child moves from a relatively primitive analysis and
 
interaction with the external world to a stage where his conceptual structures are
 
complex and enable sophisticated analysis and prediction of the environment.
 
The cognitive capacities evident at maturity have been built on simpler ones
 
gathered progressively during childhood. Thus, impairment of systems which
 
gather and utilize information as a consequence of cerebral damage could result
 
in diminished intellectual achievement, not through injury to critical higher-level
 
systems, but because essential ‘feeder’ mechanisms have malfunctioned. An adult
 
with a subcortical lesion which destroys the left auditory radiation and the
 
callosal input from the contralateral hemisphere may show a normal audiogram
 
  
 +
Goltz, F. (1892) Uber die Verrichtungen des Grosshirns. Pflugers Arch. Ges. Physiol., 51, 570- 614.
  
 +
Guttman, E. (1942) Aphasia in children. Brain, 65, 205-219.
  
214
+
Harlow, H. F., Thompson, C. I., Blomquist, A. J. and Schiltz, K. A. (1970) Learning in rhesus monkeys after varying amounts of prefrontal lobe destruction during infancy and adolescence. Brain Res., 18, 343-353.
  
 +
Hebb, D. O. (1942) The effects of early and late brain injury upon test scores and the nature of normal adult intelligence. Proc. Amer. Phil. Soc., 85, 275-292.
  
 +
Hecaen, H. (1976) Acquired aphasia in children and the ontogenesis of hemispheric functional specialisation. Brain and Lang., 3, 114-134.
  
 +
Hecaen, H. and Albert, M. L. (1978) Human Neuropsychology. John Wiley and Son, New York.
  
 +
Henry, C. E. (1944) Electroencephalograms of normal children. Mon. Soc. Res. Child. Devel, 9, Serial No. 39.
  
but be incapable of interpreting spoken language (Gloning et al ., 1963).  
+
Henschen, S. E. (1926) On the function of the right hemisphere of the brain in relation to the left hemisphere in speech, music and calculation. Brain, 49, 110-123.
Nevertheless, speech, reading and writing may be normal since their associated
 
cortical circuitry is undamaged and language has been previously established. In
 
a child, bilateral disruption of the auditory radiations by a lesion damaging the
 
lips of the sylvian fissures and the insulae can preclude the normal development
 
of language, despite evidence of hearing in the normal range (Landau et al ,
 
1960). Even children who become peripherally deaf after acquiring speech may
 
not only show arrested language development but lose previously acquired
 
linguistic skills (Bay, 1975). This ‘cognitive starvation’ effect, which is easy to
 
comprehend in the instances cited, may also operate within association areas of
 
the cortex and may underlie the tendency of early brain pathology to produce
 
more global intellectual depression effects than are seen with lesions in
 
adolescence and adulthood.  
 
  
The data briefly reviewed in this section emphasize that the effects of brain
+
Hicks, S. F. and D’Amato, C. S. (1970) Motor-sensory and visual behavior after hemispherectomy in newborn and mature rats. Exp. Neurol, 29, 416-438.
injury in the developing nervous system are particularly complex. When injury
 
occurs, it is within a system whose functional capacities are still unfolding, and  
 
the effects of injury are sometimes not immediately apparent. The plastic
 
capacity of the system may also mask the extent of any physical injury and lead
 
to a false assumption that effects have been transitory. There is also the added
 
complication that, whilst injury may not have damaged structures critical for the
 
attainment of certain cognitive skills, because critical ‘feeder’ systems have been
 
impaired, these cognitive mechanisms may not have the experiental basis upon
 
which to build.  
 
  
The consequences of early brain damage
+
Hubei, D. H. and Wiesel, T. N. (1963) Receptive fields of cells in the striate cortex of very young, visually inexperienced kittens. J. Neurophysiol., 26, 994-1002.
  
Global and specific processing
+
Ingram, T. T. S. (1964) Pediatric Aspects of Cerebral Palsy. E. and S. Livingstone, Edinburgh.
  
In 1942 Hebb drew attention to the different patterns seen following brain
+
Ingram, T. T. S. (1965) Specific retardation of speech development. Speech Pathol Ther., 8, 3-11.
damage in both mature and immature nervous systems. Adults, he found, could
 
be considered to be either aphasic or non-aphasic types (Hebb, 1942). The
 
aphasic type showed obvious evidence of deterioration on verbal tasks and some
 
also showed evidence of impairment on such non-verbal tasks as detecting
 
absurd errors in pictures and block manipulation performance. However, some
 
of the aphasic patients showed evidence of almost normal performance on nonverbal tasks, and Hebb remarked on the wide disparity of abilities seen on
 
particular tests in individual aphasic patients. This conclusion of Hebb’s (that
 
non-verbal skills may be retained to a remarkable extent in some cases of
 
aphasia) is reinforced by more recent research on this topic (Zangwill, 1964;
 
Kertesz and McCabe, 1975). In the non-aphasic type of brain injury on the other
 
hand many verbal tasks could be adequately completed, but there was usually
 
severe impairment on maze learning, block manipulation and picture absurdity
 
tasks, as well as impairment on some verbal tasks, e.g. the defining of abstract
 
  
 +
Kennard, M. A. (1940) Relation of age to motor impairment in man and in subhuman primates. Arch. Neurol. Psychiat., 44 , 377-397.
  
 +
Kertesz, A. and McCabe, P. (1975) Intelligence and aphasia: performance of aphasics on Raven’s coloured progressive matrices (RCPM). Brain and Lang., 2, 387-395.
  
DETERMINATE AND PLASTIC PRINCIPLES
+
Kinsbourne, M. (1975) ‘Minor hemisphere language and cerebral maturation’, in Foundations of Language Development, Vol. 2 (eds. E. H. Lenneberg and E. Lenneberg), Academic Press, London, 107-116.
  
 +
Kohn, B. and Dennis, M. (1974) Selective impairment of visuo-spatial abilities in infantile hemiplegics after right cerebral hemidecortication. Neuropsychologia, 12, 505-512.
  
215
+
Krashen, S. (1973) Lateralisation, language learning and the critical period. Lang. Learning, 23, 63-74.
  
 +
Landau, W. M. and Kleffner, F. R. (1957) Syndrome of acquired aphasia with convulsive disorder in children. Neurol., 7, 523-530.
  
words, or naming opposites. The two types were, however, sufficiently different
+
Landau, W. M., Goldstein, R. and Kleffner, F. R. (1960) Congenital aphasia: a clinicopathologic study. Neurol, 10, 905-921.
for Hebb to state that following adult brain injury a reasonably specific pattern
 
of deficit often emerges—some skills showing deterioration and others being
 
relatively intact. In contrast, a group of children with what he termed
 
‘exogenous’ brain injury showed no evidence of a dual pattern, that is the
 
‘aphasic’ and ‘non-aphasic’ types did not occur as a consequence of early brain
 
injury. The group as a whole showed depression of verbal IQ, but since he
 
thought it unlikely that every case of brain injury in infancy involved damage to
 
the language areas it must be that ‘low verbal test scores are produced by early
 
lesions outside the speech areas’ (Hebb, 1942, p. 286). He went on to argue that
 
the more global pattern of intellectual depression seen after early brain injury
 
occurs as a result of the differing demands being made on the adult and the child
 
after cerebral damage. The adult has merely to make use of skills which have
 
already been acquired, whereas the child has still to assimilate a range of skills.  
 
Since a greater cognitive demand is made during the acquisition of a skill than
 
by the performance of one already acquired, the growing child is at a greater loss
 
than the adult when an equivalent amount of brain tissue has been lost in both.  
 
Hebb went further and argued—following Lashley (1929)—that some degree of
 
equipotentiality must exist in the cortex and that areas outside the classical
 
language areas must be involved in the development, but not the maintenance, of
 
linguistic skills once they have been mastered.  
 
  
Two major hypotheses then emerge from Hebb’s work (1942). The first is that
+
Langworthy, O. R. (1933) Development of behavior patterns and myelinisation of the nervous system in the human foetus and infant. Carnegie Instit. Pub. No. 139, Washington.
early, rather than late, brain damage has a more global depressive effect upon
 
intellectual development. The second hypothesis is that the developing nervous
 
system is characterized by a greater degree of equipotentiality than that of the
 
adult, since the attainment of normal adult performance on a range of specific
 
skills seems to depend on the integrity of whole cerebrum. The first hypothesis
 
has, in general, received support from subsequent research. Bryan and Brown
 
(1957) found that there is a strong relation between the age of injury and mean
 
IQ, so that those with an injury present at birth averaged a score of 62, those
 
injured in infancy averaged 66 while those with injuries occurring between 3 and
 
10 years and between 10 and 20 years averaged 71 and 85 respectively.
 
Thompson (1978) reported that in 282 subjects who sustained localized cerebral
 
injury in childhood, there was a linear relationship between age of injury and
 
full-scale IQ with those injured before 5 scoring 97 and those injured above 15
 
years scoring 106.5. It should be noted, however, that whilst McFie (1961a)
 
found a rise in mean IQ between those injured in the age bands 1-4 and 5-9
 
years from 88.8 to 106.0, he found a fall in IQ with those sustaining injury
 
between 10 and 15 years (82.7). However, on balance the findings would seem to
 
support Hebb’s initial contention.  
 
  
The second hypothesis emerging from Hebb’s (1942) study, that the
+
Lashley, K. S. (1929) Brain Mechanisms and Intelligence: A Quantitative Study. Univ. Chicago Press, Chicago.
developing nervous system is characterized by a greater degree of equi-
 
  
 +
Lawrence, D. G. and Hopkins, D. A. (1972) Developmental aspects of pyramidal motor control in the rhesus monkey. Brain Res., 40, 117-118.
  
 +
Lecours, A. R. (1975) ‘Myelogenetic correlates of the development of speech and language’, in Foundations of Language Development, Vol. 1 (eds. E. H. Lenneberg and E. Lenneberg), Academic Press, New York, 121-135.
  
216
+
Lenneberg, E. H. (1967) Biological Foundations of Language. John Wiley and Sons, New York.
  
 +
Lenneberg, E. H. (1968) The effect of age on the outcome of central nervous system disease in children’, in The Neuropsychology of Development (ed. R. L. Isaacson), John Wiley and Sons London, 147- 170.
  
 +
Liepmann, H. (1908) Drei Aufsatze aus dem Apraxiegebeit. Karger, Berlin.
  
 +
Lissauer, H. (1890) Ein Fall von Seelenblindheit nebst einen Beitrag zur Theorie derselben. Arch. F. Psychiat, 21, 222-270.
  
 +
Lyon, G. (1961) First signs and mode of onset of congenital hemiplegia. Little Club Clin. Dev. Med., 4 , 33-38.
  
potentiality than that of the adult, is rather more contentious since it is more
+
Marshall, W. A. (1968) Development of the Brain. Oliver and Boyd, Edinburgh.
difficult to test than it might appear at first sight. It has already been pointed out
 
that general depression of IQ cannot be used as evidence for a type of mass
 
action operating during development, since it may also argue for an interdependence of separate capabilities being required for the construction of more
 
complex schemata. It is also apparent that brain-damaged children show widely
 
differing patterns of impairment, which would be difficult to comprehend if there
 
were a tendency for the brain to act uniformly in the acquisition of cognitive
 
skills (Strauss and Lehtinen, 1968). There is also the added difficulty that IQ
 
tests may be rather insensitive to specific patterns of disability produced by brain
 
injury, both in children (Boll and Reitan, 1972) and adults (Walsh, 1978), a
 
factor which has resulted in the construction of specialized test batteries.  
 
  
However, instead of asking whether the general depressive effect of early brain
+
McFie, J. (1961a) Intellectual impairment in children with localized post-infantile cerebral lesions. J. Neurol. Neurosurg. Psychiat., 24, 361-365.
damage on IQ is due to a greater degree of global processing in the immature
 
CNS, it might be more fruitful to consider whether a similar pattern of
 
impairment emerges on specific skills after similar damage in the child and the
 
adult. McFie (1961a), in an investigation of the effects of localized post-infantile  
 
cerebral lesions in children, found that there was a tendency for Wechsler verbal
 
scores to be lower following left hemisphere injury and performance scores to be
 
lower following damage to the right hemisphere. He also noted a similarity in the
 
pattern of impairment shown on the Memory for Designs component of the
 
Terman-Merrill scale (1937) between children and adults when comparing the
 
effects of frontal, temporal and parietal injury. He reported that the greatest
 
deficit is to be found in both groups following right parietal damage. Fedio and
 
Mirsky (1969) examined the pattern of impairment exhibited by children with
 
either unilateral temporal lobe or with centrencephalic epilepsy on a test battery
 
designed to measure performance on both verbal and non-verbal tasks, and a
 
task of sustained attention. The children, who had a history of illness dating from
 
early school years, showed similar impairment profiles to those of adults with
 
similar pathology. Those with left temporal epileptiform foci required a greater
 
number of trials to learn lists of ten words and showed greater loss after a 5-  
 
minute interval than those with right temporal or centrencephalic pathology.
 
Those with right temporal pathology showed greatest impairment on the recall
 
of the order of random shapes and on production of the Rey-Osterrieth figure.
 
The centrencephalic group showed the greatest deficit on a task requiring
 
sustained attention. Annet et al (1961) also found a similar pattern of verbal
 
and spatial difficulties in children classified on the basis of lateralized EEG
 
abnormalities. These results would suggest that children show impairments of
 
the same type as those found in adults with similar pathology. It may be objected
 
however, that in these cases the damage is characteristic of juvenile rather than
 
infant brain damage, and, if adult cortical specialization appears gradually, then
 
patterns of specific loss will also begin to appear, producing the observed
 
  
 +
McFie, J. (1961b) The effects of hemispherectomy on intellectual functioning in cases of infantile hemiplegia. J. Neurol. Neurosurg. Psychiat., 24, 240-249.
  
 +
Mein, R. (1960) A study of the oral vocabularies of severely subnormal patients. J. Ment. Def. Res., 4, 130-143.
  
DETERMINATE AND PLASTIC PRINCIPLES
+
Milner, B. (1973) ‘Hemispheric specialisation: scope and limits’, in The Neurosciences: Third Study Program (eds. F. O. Schmitt and F. G. Worden), M.I.T. Press, Cambridge, 75-89.
  
 +
Milner, B. (1974) ‘Sparing of language function after early unilateral brain damage’, in Functional Recovery After Lesions of the Nervous System (eds. E. Eidelberg and D. G. Stein), Neurosci. Res. Prog. Bull., 12, 213-217.
  
217
+
Milner, E. (1976) ‘CNS maturation and language acquisition’, in Studies in Neurolinguistics, Vol. 2 (eds. H. Whitaker and H. A. Whitaker), Academic Press, London, 31-102.
  
 +
Molfese, D. L. (1977) ‘Infant cerebral asymmetry’, in Language Development and Neurological Theory (eds. S. J. Segalowitz and F. A. Gruber), Academic Press, London, 21—35.
  
similarity to the adult type by middle childhood. However, evidence does exist
+
Paine, R. (1960) Disturbances of sensation in cerebral palsy. Little Club Clin. Dev. Med., 2, 105- 109.
which would suggest that there is hemisphere specialization, even when damage
 
occurs perinatally or in infancy.  
 
  
Damage to the left, but not the right, hemisphere before the end of the first
+
Piaget, J. (1979) ‘Correspondences and transformations’, in The Impact of Piagetian Theory (ed. F. B. Murray), University Park Press, Baltimore, 17-27.
year of life results in impairment in the rate at which combinations of words
 
(elementary syntax), but not single words, are learned (Bishop, 1967). Furthermore, children who have had either a left or right hemisphere removed as a
 
consequence of damage sustained during the first year of life show differential
 
effects depending on which hemisphere is involved. Those with left hemisphere
 
removal show greater difficulty in the comprehension of syntax than right hemi-
 
decorticates (Dennis and Kohn, 1975). In particular, difficulties as shown by a
 
greater number of errors are apparent in comprehension of the passive negative,
 
e.g. ‘the girl is not pushed by the boy’, as opposed to the active affirmative, ‘the
 
boy pushes the girl’. In these experiments comprehension was assessed by having
 
the child choose a picture which depicted the sentence. The greater difficulty in
 
the comprehension of passive sentences was also apparent in longer response
 
latencies. Children with early right hemisphere damage followed by hemi-
 
spherectomy show difficulties on spatial tasks (Kohn and Dennis, 1974). The
 
types of spatial task on which they show relative deficit are those which continue
 
to show improvements in normal subjects through the teens, e.g. the WISC and
 
Porteus mazes, and map reading tasks, which require a subject either to state the
 
direction to be taken or to follow a route through markers placed on the floor.
 
Early maturing skills, such as tactile form matching and visual closure, were
 
unaffected in contrast to right hemisphere injury at maturity which severely
 
depresses these abilities. Further analyses of three cases where hemispherectomy
 
antedated the beginnings of speech were presented by Dennis and Whitaker
 
(1976) and two cases where hemispherectomy for unilateral pathology was
 
carried out at ages 3 and 4 years respectively were reported by Day and
 
Ulatowska (1979). In these cases the pattern of deficit is similar to those
 
previously reported and supports the view that the hemispheres are differentially
 
involved in different aspects of cognition. Specialization would appear to be an
 
early-established characteristic of the child’s brain although its potential for
 
reorganization complicates the issue (see p. 225).  
 
  
Given that differences in the patterning of intelligence subtest scores only
+
Rudel, R. G., Teuber, H.-L. and Twitched, T. E. (1974) Levels of impairment of sensori-motor functions in children with early brain damage. Neuropsychologia, 12, 95-108.
really become obvious during adolescence and beyond (Thompson, 1978),
 
whereas specific deficits are detectable by specially devised tests in younger
 
children, IQ tests appear to be insensitive instruments on which to base theories
 
concerning brain development. One obvious factor which will lessen the
 
sensitivity of IQ tests to brain damage early in development is the capacity to
 
transfer the development of linguistic and spatial skills to the contralateral
 
hemisphere should damage occur. This plastic capacity should not however be
 
confused with ideas about mass action or equipotentiality. These latter ideas
 
  
 +
Russell, W. R. (1959) Brain, Memory and Learning: A Neurologist's View. Clarendon Press, Oxford.
  
 +
Schneider, G. E. (1969) Two visual systems. Science, 163, 895-902.
  
218
+
Schneider, G. E. (1970) Mechanisms of functional recovery following lesions of visual cortex or superior colliculus in neonate and adult hamster. Brain Behav. EvoL, 3, 295-323.
  
 +
Schneider, G. E. (1979) Is it really necessary to have your brain lesions early? A revision of the ‘Kennard Principle’. Neuropsychologia, 17, 557-583.
  
 +
Shagass, C. (1972) ‘Electrical activity of the brain’, in Handbook of Psychophysiology (eds. N. S. Greenfield and R. A. Sternback), Holt, Rinehart and Winston Inc., London, 263-328.
  
 +
Strauss, A. A. and Lehtinen, L. E. (1950) Psychopathology and the Education of the Brain Injured Child. Grune and Stratton, New York.
  
 +
Terman, L. M. and Merrill, M. A. (1937) Measuring Intelligence. Harrap, London.
  
imply the existence of a type of diffuse processing network to which the
+
Teuber, H.-L. (1975) ‘Recovery of function after brain injury in man’, in Outcome of Severe Damage to
association cortex within each hemisphere contributes uniformly (Lashley,  
+
the Central Nervous System (Ciba Foundation Symposium No. 34), Elsevier, Amsterdam, 159-186.
1929). The transfer of functional capability from one hemisphere to the other,
 
however, is to be understood in a rather different context. Each cerebral
 
hemisphere contains anatomical structures which are essentially duplicates of
 
those found in the other, with the difference that certain cytoarchitectonic areas
 
may be relatively larger or smaller. In some instances, particularly in the
 
language area, these cytoarchitectonic differences in size may be as great as
 
700% in favour of the left hemisphere (Galaburda et al ., 1978). However, each
 
specialized cortical area has a pattern of connections to the rest of the brain  
 
which, in essence, is a lateral reversal of those found in the other hemisphere.
 
The ability of these ‘duplicates’ to assume some of the functional capacities
 
previously assumed by their cytoarchitectonic counterparts is perhaps not too
 
surprising. Indeed, the puzzling feature is that in a substantial majority of the
 
adult population this ability is lost. The assumption that somehow the areas
 
within each hemisphere act as a kind of equipotential unit, is not supported by
 
the available evidence. If such a diffusely organized system were operative in the
 
left hemisphere during development, then it would be reasonable to assume that
 
unilateral damage, resulting in suboptimal processing capacity, would be
 
sufficient reason to transfer linguistic processing to the remaining intact
 
hemisphere. Milner (1973) has provided evidence, based on language lateralization, tested by the Wada (intracarotid injection of sodium amytal) technique,  
 
that only when early injury invades those areas shown to be important for
 
linguistic processing in the adult, will language transfer to the right hemisphere.
 
These results suggest that certain key regions, not the global processing capacity
 
or total operational mode of one hemisphere, promote the establishment of
 
language within that hemisphere.  
 
  
In considering the question of global or specific processing in development,  
+
Teuber, H.-L. and Rudel, R. G. (1962) Behavior after cerebral lesions in children and adults. Dev. Med. Child Neurol ., 4, 3-20.
the evidence on balance suggests a specific processing configuration not
 
dissimilar to that found in the adult brain. It has also been argued that one of the
 
reasons why early brain damage often has a markedly depressive effect on
 
intellectual growth may be that the substrate of complex cognitive processes
 
may require the integrity of fundamental systems in order to attain their full
 
potential. One line of evidence which supports this is the finding that right
 
hemisphere damage, which occurs before one year of age, may have more
 
depressive effects on cognitive growth than damage to the left hemisphere at an
 
equivalent age, or damage to either hemisphere after one year of age (McFie,
 
1961 b; Woods, 1980). This greater deleterious effect of early right hemisphere
 
pathology on both verbal and performance IQ scores argues for the participation of the right hemisphere in certain fundamental processes that may
 
underlie both linguistic and spatial competence. Given the specialization of the
 
right hemisphere for the acquisition of spatial skills it appears possible that a
 
  
 +
Thompson, J. (1978) ‘Cognitive effects of cortical lesions’, in Psychology Survey No. 1 (ed. B. M. Foss), Allen and Unwin, London, 86-98.
  
 +
Trevarthen, C. B. (1968) Two mechanisms of vision in primates. Psychol. Forsch., 31, 299-337.
  
DETERMINATE AND PLASTIC PRINCIPLES 219
+
Tsang, Y.-C. (1937) Maze learning in rats hemidecorticated in infancy. J. Comp. Psychol., 24, 221-254.
  
certain elementary sensori-motor coordinate system may normally be established by the right hemisphere, and in some way aid the differentiation of more
+
Turner, O. A. (1948) Growth and development of cerebral cortical pattern in man. Arch. Neurol. Psychiat., 59, 1-12.
complex skills which do not, at first sight, appear directly connected to it. The
 
importance of elementary sensori-motor expedience in evolving more complex
 
cognitive operations has been stressed by many theorists, and by Piaget (1979)  
 
in particular. However, regardless of whether or not the presence of this
 
correspondence between theories of cognitive development and neuropsychological research finding is accepted, the results obtained by McFie (1971a, b) and
 
Woods (1980) emphasize the importance of the presence of a particular structure
 
at a particular stage during development rather than supporting the view that
 
different structures are functionally equivalent.  
 
  
 +
Turner, O. A. (1950) Postnatal growth of the cortical surface area. Arch. Neurol. Psychiat., 64, 378-384.
  
Aphasia in children
+
Ulett, G., Dow, R. S. and Landsell, O. (1944) The inception of conductivity in the corpus callosum and the corticoponto-cerebellar pathway of young rabbits with reference to myelinisation. J. Comp. Neurol., 80, 1-10.
  
The study of language disorders in children is important to a number of
+
Wada, J. A., Clark, R. and Hamm, A. (1975) Cerebral hemispheric asymmetry in humans: cortical speech zones in 100 adult and 100 infant brains. Arch. Neurol, 32, 239-246.
problems in developmental neuropsychology. It has provided evidence concerning the extent of functional specialization in the cerebral hemispheres during
 
maturation; data concerning the reorganizational or plastic capacity of the
 
developing brain; and a third, equally important, question, evidence as to the
 
manner in which language becomes established in cortical structures. This
 
question is, in fact, separate from those of hemispheric specialization and  
 
plasticity. Here we are concerned with the similarity between the aphasic
 
symptoms of the child and the adult. The greater the similarity of the syndromes
 
the more likely it is that the adult structural pattern has become established,  
 
even if subsequently the recovery of the child is more complete because
 
duplication of function in the contralateral hemisphere is still possible. In the
 
present section each of these three topics will be examined, but the characteristics of childhood aphasia will be examined first.  
 
  
The clinical picture found in childhood aphasia was described by Guttman
+
Walsh, K. W. (1978) Neuropsychology: A Clinical Approach. Churchill Livingstone, Edinburgh.
(1942), who noted that despite claims that the syndrome was rare, he had found
 
it not an unusual accompaniment of head injury or intracranial pathology. In
 
contrast to the adult, where complaints with speech difficulties, failures to name
 
objects and paraphrasia are common, the aphasic child is usually apathetic and
 
morose with such extreme poverty of speech that it approaches mutism. Absence
 
of spontaneous speech, lack of willingness to speak, and a hesitant dysarthric
 
telegrammatic-style speech are frequently noted, these symptoms being more
 
common in the younger child. In contrast to the extreme poverty of speech
 
production, comprehension of simple instructions is evident so that parts of the
 
body or objects can be appropriately indicated when a request is made. When
 
prompted to speak difficulties in the manipulation of lips and tongue may be
 
apparent together with failure to produce sound. As recovery progresses,  
 
initially the child will speak single words when prompted. It will then move to
 
  
 +
Walter, W. G. (1950) ‘Normal rhythms—their development, distribution and significance’, in Electroencephalography (eds. D. Hill and G. Parr), Macdonald and Co., London, 203-227.
  
 +
Werner, G. and Whitsell, B. L. (1973) ‘Functional organisation of the somatosensory cortex’, in Somatosensory Systems, Handbook of Sensory Physiology, Vol. 2 (ed. A Iggo), Springer Verlag, New York, 621-700.
  
220
+
Wernicke, C. (1874) Der Aphasische Symptomenkomplex. Cohn and Weigert, Breslau, Poland.
  
 +
Woods, B. T. (1980) The restricted effects of right-hemisphere lesions after age one; Wechsler test data. Neuropsychologia, 18, 65-70.
  
 +
Woods, B. T. and Teuber, H.-L. (1978) Changing patterns of childhood aphasia. Ann. Neurol, 3, 273-280.
  
 +
Worster-Drought, C. (1971) An unusual form of acquired aphasia in children. Dev. Med. Child Neurol, 13, 563-571.
  
 +
Yakovlev, P. I. and Lecours, A. R. (1967) ‘The myelogenetic cycles of regional maturation of the brain’, in Regional Development of the Brain in Early Life (ed. A. Minkowski), Blackwell, Oxford, 3-70.
  
sparse spontaneous utterances before speech moves into a stage when
+
Yamadori, A., Osumi, Y., Masuhara, S. and Okubo, M. (1977) Preservation of singing in Broca’s aphasia. J. Neurol. Neurosurg. Psychiat., 40, 221-224.
impoverished but spontaneous conversation occurs with persistent dysarthria.  
 
This pattern, which bears the imprint of an almost exclusively motor disorder,  
 
occurred in all cases below 10 years of age and occurred regardless of the
 
location of the lesion within a hemisphere. Where damage occurred after the
 
tenth year in some cases speech showed a lack of spontaneity but symptoms
 
more characteristic of the adult pattern with impaired auditory comprehension,  
 
syntactical and paraphrasic errors, together with difficulties of naming were
 
found. Dysarthria may or may not accompany these symptoms.  
 
  
This picture of aphasia in childhood has been supported by subsequent
+
Zangwill, O. L. (1964) ‘Intelligence in aphasics’, in Disorders of Language (eds. A. V. S. de Reuck and M. O’Connor), Ciba Symposium, Little Brown and Co., Boston, 261-284.
research in which the onset of the language loss is sudden following external
 
injury or internal pathology. In Guttman’s cases the five instances of injury
 
which produced aphasia in which the symptom was exclusively one of speech
 
production difficulty were aged 8 years or below, and the two instances in which
 
speech output was not affected but other aphasic symptoms were present were
 
over 10 years of age. The series of cases reported by Hecaen (1976) show that in  
 
two instances where the disorder was exclusively one of speech production the
 
children were aged 6, and in the remaining case 3j years. In children aged 7 years
 
and more, comprehension, naming and paraphrasic disorders were more likely
 
to occur. Both Guttman (1942) and Hecaen (1976) stress the fact that recovery
 
may be extremely rapid, marked improvement sometimes being noted in as little
 
as 6 weeks. In children aged over 10 years however, the time course of the
 
disability may sometimes be prolonged. In middle to late childhood the aphasic
 
symptoms begin to mimic the adult pattern, whereas in early childhood the
 
disorder appears to be purely expressive. In adults expressive aphasia is often
 
produced by lesions located in the anterior region of the hemisphere and
 
difficulties in comprehension occur more frequently with temporal and inferior
 
parietal damage (Geschwind, 1970). However, in children below 10 years,
 
disorders of expression appear to occur regardless of the location of the lesion
 
(Guttman, 1942). A second distinctive feature of the aphasic syndrome in young
 
children is the absence of cases of jargon aphasia, where the speech output is
 
rapid with relatively normal articulation but contains many circumlocutions
 
and paraphrasias (Geschwind, 1972). Woods and Teuber (1978) claim to have
 
one documented case of jargon aphasia in a 5-year-old child, but the clinical
 
description is unlike the adult form. The child produced a stream of meaningless
 
sounds, but when recognizable words were uttered they were most often the
 
names of objects. The child also showed evidence of a purely apraxic disturbance, e.g. sticking out his tongue when asked to blow out a light. To the
 
present author, the picture is too dissimilar to the adult form to be classed as an
 
instance of jargon aphasia, the only feature in common being the high rate of
 
vocal, as opposed to verbal, output.  
 
  
The cases of language loss in childhood so far described were instances where
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DETERMINATE AND PLASTIC PRINCIPLES
 
 
 
 
 
221
 
 
 
 
 
loss was abrupt, following external or internal injury, and where injury was
 
usually confined to one cerebral hemisphere. A rather different type of childhood
 
aphasia occurs when the language loss is associated with either the onset or
 
development of bilateral epileptiform abnormalities (Landau and Kleffner,
 
1957; Worster-Drought, 1971; Gascon et al , 1973). In these cases, the loss of
 
language is associated with difficulties in understanding speech, which, in some
 
cases, may evolve over a matter of days or weeks. The child shows lack of
 
response to speech, which may be mistaken for peripheral deafness. Audiometric
 
testing reveals either mild or moderate hearing loss, but this loss is insufficient to
 
account for the comprehension disorder and, in any case, hearing usually shows
 
progressive improvement after an initial depression. In some cases auditory
 
evoked potentials to pure tones may be normal, but evoked potentials to speech
 
show abnormalities (Gascon et al ., 1973). Loss of language is gradual and
 
persistent, and while in some cases recovery may occur over a period of years
 
(Landau and Kleffner, 1957), in other cases it appears to be permanent (Worster-
 
Drought, 1971). In some cases loss of speech may be almost total and auditory
 
comprehension limited to less than a dozen words. Despite gross impairment in
 
the development of language, frequently these children do not show impairment
 
on non-verbal tasks in intelligence tests. Of the 14 cases described by Worster-
 
Drought (1971), performance IQ ranged from 96 to 140, with only one case
 
falling below 100. This remains true despite the fact that, in many cases, the onset
 
of pathology is at less than 5 years of age. These cases of bilateral abnormality
 
are in contrast to cases where a unilateral lesion produces aphasia, from which
 
the child subsequently recovers yet shows a low overall IQ (Hecaen, 1976).
 
 
 
When damage to a single hemisphere produces aphasia the child usually
 
recovers language, and in the young child this recovery is usually better than
 
when damage occurs above 10 years (Lenneberg, 1967). This has often been seen
 
as evidence that the two cerebral hemispheres are initially equipotential as far as
 
the development of language is concerned. Further, it has sometimes been
 
claimed that both cerebral hemispheres are involved initially in language
 
development with lateralization increasing with age (see Dennis and Whitaker,
 
1977 for a review). It has already been noted that as far as attainment on certain
 
language tests is concerned the two hemispheres are not equivalent. The view
 
that the right hemisphere is involved in language acquisition in the infant and
 
young child comes from reports of the high incidence of speech disturbances
 
following right hemisphere damage. The incidence of language disorders with
 
lesions of the left and right hemispheres described by different researchers varies
 
widely. In the case of the left hemisphere, damage has been estimated to produce
 
language disorder with an incidence varying from 25% (Ingram, 1964) to over
 
90% (Dunsdon, 1952). In the case of the right hemisphere the estimated
 
incidence has varied from less than 1 % (Ingram, 1964) to nearly 38 % (Dunsdon,
 
1952). Only one investigator has claimed an equal frequency of language dis-
 
 
 
 
 
 
 
222
 
 
 
 
 
 
 
 
 
 
 
order following either left or right cerebral damage (Basser, 1962). The discrepancies seem too large to attribute to statistical sampling fluctuations. One of the
 
problems encountered in this area is the definition of what constitutes an aphasic
 
language disturbance. Language difficulties are associated with depressed
 
general intelligence (Mein, 1960) so that severe brain damage which produces
 
severe retardation may produce language disturbance indirectly. There is also
 
the problem of whether speech disturbance should be considered an aphasic
 
disturbance (Ingram, 1965). It is already apparent that the syndrome of aphasia •
 
in children may vary from almost total mutism to a clinical picture similar to
 
that of the adult with comprehension disturbance and naming impairment. That
 
the type of impairment can vary not just with age of the child but also be related
 
to the damaged hemisphere can be seen by examining the series of Hecaen
 
(1976). Of 6 cases of right hemisphere damage, only the two youngest (6 and 3^
 
years) showed any disturbance and this was articulatory. Bishop (1967) has
 
reported that in cases of infantile hemiplegia, articulatory disturbances are
 
equally likely following damage to either hemisphere, but that left hemisphere
 
damage additionally delays the acquisition of word combinations rather than
 
single words.
 
 
 
The possibility of a different pattern of impairment following left and right
 
hemisphere injury is not the only factor which complicates the issue. Woods and
 
Teuber (1978) have pointed out that there is a tendency for investigators since
 
1940 to report a lower incidence of aphasia following right hemisphere injury
 
than earlier workers. They attribute this to the fact that in older investigations
 
aphasias and hemiplegias were frequently complications of systemic infectious
 
illnesses such as scarlet fever, bacterial pneumonia and diphtheria, which can
 
produce not only focal lesions but also diffuse bilateral encephalopathy.
 
Undoubtedly the frequent reliance on hemiplegia alone as the sign indicating
 
exclusive damage to one hemisphere is likely to result in the inclusion of cases
 
where a less extensive pathology is also present in the hemisphere that is
 
assumed to be intact. Bearing these facts in mind, it would obviously be
 
hazardous to speculate concerning the true incidence of language disturbance
 
following right hemisphere pathology. For the moment it is sufficient to say that
 
the incidence of aphasia following right hemisphere damage may be considerably less than previously thought, perhaps as little as 5 % in those who were
 
previously right-handed (Woods and Teuber, 1978).
 
 
 
A finding that has already been mentioned several times is that concerning the
 
capacity of the right hemisphere to acquire language following early left
 
hemisphere injury. There is little doubt that the capacity to transfer language to
 
the right hemisphere is a real factor in the recovery from aphasia in children.
 
However, it cannot be assumed that in every case of childhood aphasia recovery
 
of language is due to transfer to the contralateral hemisphere. Milner (1974)
 
noted, on the basis of the Wada test, that in adults who were left-handed but had
 
 
 
 
 
 
 
DETERMINATE AND PLASTIC PRINCIPLES
 
 
 
 
 
223
 
 
 
 
 
sustained early left hemisphere damage, language was present in the left
 
hemisphere in 30 % and bilaterally present in 16 % of cases. Thus, in 46 % of cases
 
who had left hemisphere injury, the left hemisphere was still involved in language
 
to some degree. Whether or not language transferred depended on whether
 
certain critical areas were damaged. In cases where left hemispherectomy is
 
performed, following widespread unilateral damage, it is clear that the presence
 
of linguistic competence is dependent on the remaining hemisphere (Dennis and
 
Whitaker, 1977). When such language transfer does occur, while verbal IQ may
 
not be significantly depressed relative to performance IQ, it should be remembered that such tests do not directly sample knowledge of language structure.
 
Where tests are designed to evaluate grammatical comprehension then deficits
 
appear (Dennis and Kohn, 1975; Teuber, 1975; Dennis and Whitaker, 1976;
 
Day and Ulatowska, 1979). However, with these reservations in mind, children
 
exposed to left hemispherectomy do show an adequate degree of language
 
competence in relation to their overall IQ and it has frequently been remarked
 
that it would be an incredible improvement if each adult aphasic could recover
 
the same level of language competence (Geschwind, 1972).
 
 
 
The duration of such plasticity in the developing brain has been the subject of
 
disagreement. Lenneberg (1967) believed that the period of plasticity in regard to
 
language mechanisms lasted until puberty. Krashen (1973) has challenged this
 
view mainly on the basis that right hemisphere damage above the age of 5 does
 
not often produce aphasia whereas below this age it frequently does. However it
 
should be understood that the issue of the degree to which both hemispheres are
 
involved in language acquisition early in life (and evidence has already been
 
cited that right hemisphere aphasia may be quite different in form from left
 
hemisphere aphasia in young children) is quite a different one from the question
 
of whether interhemispheric transfer is possible. Children between 5 and 10 years
 
do show good recovery from aphasia and it would be surprising indeed if
 
language could have survived in the left hemisphere given the extent and severity
 
of the damage in some instances, e.g. right hemiplegia and hemianopsia (Hecaen,
 
1976). On the balance the evidence would appear to favour a period of plasticity
 
extending to at least 10 years of age. There is even some indication that a period
 
of reduced plasticity may extend far beyond this age although whether it
 
involves inter-hemispheric transfer or improved within-hemisphere recovery is
 
another question. Teuber (1975) noted that an analysis of 167 cases of brain
 
injury sustained during the Korean campaign showed that the population who
 
were under 22 at the time of injury showed better recovery of language than
 
those who were 23 years and over. It may be premature then to try to set rigid
 
cut-off points for recovery.
 
 
 
The evidence presented here suggests that aphasia in children is not one
 
syndrome but several. In children of 6 years and below mutism and dysarthria
 
appear as the main symptoms with comprehension being relatively well
 
 
 
 
 
 
 
224
 
 
 
 
 
 
 
 
 
 
 
preserved. Furthermore this pattern appears to occur regardless of whether the
 
lesion is in the left or right hemisphere and also appears to be insensitive to the
 
precise location of the lesion within a hemisphere (whether it is frontal, temporal
 
or parietal). Above 6 years, symptoms which are regarded by many as truly
 
aphasic (comprehension and naming disorders) appear. The symptoms appear
 
to occur largely following left rather than right hemisphere lesions. Between the
 
ages of 6 and 14, jargon aphasia in its adult form is infrequent although the
 
extended circumlocutions that are one of the characteristics of aphasia do occur
 
(Guttman, 1942). The rapidity of the recovery process in some cases and, in very
 
young children, the preservation of comprehension, makes it extremely unlikely
 
that language has been totally relearned by the right hemisphere (Geschwind,
 
1972). This factor has suggested to some investigators that the right hemisphere
 
must be involved in linguistic processing at an early developmental stage and in
 
fact retains some capacity for comprehension even in the adult after cerebral
 
differentiation (Kinsbourne, 1975).
 
 
 
It is possible then that during the early stages of language learning both
 
hemispheres acquire comprehension and share control of the speech mechanism.
 
This may be necessary in the initial stages, because fine bilateral control of the
 
speech mechanism is required since suitable motor synergisms for a culture-
 
specific phoneme system are not yet well established in subcortical structures.
 
The consequence of this arrangement is that a lesion to either hemisphere can
 
disrupt speech production but comprehension is relatively unaffected because
 
the structural basis of language as opposed to speech does not require a bilateral
 
component. However, the establishment of subcortical synergisms for the
 
execution of the basic components of speech production together with the
 
presence of structurally more specialized language mechanisms in the temporoparietal region of the left hemisphere normally leads to left hemisphere capture
 
of the speech output mechanism. This process is probably a gradual one, but as it
 
proceeds there is less functional demand for right hemisphere processing of
 
language and there may even be active inhibition of its linguistic processing by
 
the left hemisphere. Eventually this isolation of the right hemisphere may lead to
 
structural changes at the synaptic level so that the re-establishment of control is
 
no longer possible. To the extent that this isolation process is incomplete transfer
 
of control is still possible. Thus in young children (under 5 years) the loss of the
 
left hemisphere will show itself in only transitory speech output disturbances
 
since this process of capture is just beginning and both hemispheres are still
 
involved. Even at this age however the linguistic superiority of the left
 
hemisphere is already apparent (see Young, Chapter 6, this volume, for a review
 
of the psychophysical literature), and it is in fact this superiority that will allow
 
the eventual suppression of the right hemisphere. In children between the ages of
 
six and ten years the speech mechanism is probably under the control of the left
 
hemisphere but right hemisphere control mechanisms have not yet functionally
 
 
 
 
 
 
 
DETERMINATE AND PLASTIC PRINCIPLES
 
 
 
 
 
225
 
 
 
 
 
atrophied. Left hemisphere damage at this age can produce speech disturbances
 
solely and/or truly aphasic disturbances which are transitory, while damage to
 
the right hemisphere only rarely affects these mechanisms. With the passage of
 
time however, the capability of the right hemisphere wanes through disuse and
 
in the majority of cases only a token linguistic capacity remains. Even if in later
 
life the possibility of direct inhibition by the left hemisphere is removed, by
 
severing the corpus callosum, the right hemisphere has residual linguistic
 
comprehension but remains mute (Gazzaniga and Sperry, 1967). This is
 
probably because the process of gaining control of the speech mechanisms
 
involves the regulation of neuromuscular synergisms at subcortical levels, and
 
these remain under left hemisphere control. It should be noted that the control of
 
the vocal apparatus by the left hemisphere may be specific to its use in the
 
context of spoken language. Where lesions of the left hemisphere produce
 
expressive (Broca’s type) aphasia the ability to use the voice in the context of
 
singing including the fluent production of words may be well preserved
 
(Yamadori et al ., 1977). Evidence for a motor capture account of left hemisphere
 
language dominance can also be found in studies of adult aphasics (cf.
 
Kinsbourne, 1975).
 
 
 
 
 
The plasticity of the developing brain
 
 
 
It is usually accepted that the younger the individual when the brain sustains
 
injury, the greater the resilience and the greater the capacity for functional
 
restitution. Against this one must set the view that the developing brain is
 
particularly vulnerable and long-term effects emerge if normal development is
 
impaired. These two views may be partially reconciled by proposing that
 
following early brain damage, specific skills may be spared but at a cost that will
 
be seen in the overall lowered cognitive capacity of the brain (Teuber, 1975).
 
Thus language or visuo-spatial skills may be spared following left or right
 
hemisphere injury respectively, but intellectual achievement as measured by IQ
 
tests or by school performance will show depression. Evidence already cited
 
concerning the specific effects of early brain damage makes it clear that the
 
consequences are not just seen in a uniformly lowered total processing capacity
 
but depend on the site of injury. Language achievement is specifically lowered
 
following left hemisphere injury and spatial skills depressed specifically
 
following right hemisphere injury.
 
 
 
The evidence in favour of a greater degree of plasticity comes from a number
 
of sources. Some animal species show spared sensory capacity following cortical
 
lesions in infancy (Schneider, 1969) while in other species age at time of injury
 
does not appear to affect the magnitude of the deficit (Doty, 1973). Even where
 
pattern vision is spared following early lesions of the striate cortex, the animals
 
may still take longer to pretrain before formal testing can commence (Schneider,
 
 
 
 
 
 
 
226
 
 
 
 
 
 
 
 
 
 
 
1970). In man there is evidence of age-related sparing of sensory function.
 
Rudel et al (1974) noted minimal impairment in brain damaged children on
 
somaesthetic thresholds but these children were still impaired on tactile object
 
recognition. Elementary motor function in children may also show greater
 
savings following early massive unilateral injury (Cairns and Davidson, 1951),
 
but such abilities as are preserved, are rudimentary. In man following early
 
unilateral damage that is extensive enough to destroy large areas of the striate
 
cortex, the visual field defects are similar to those produced in adults with similar
 
pathology (Paine, 1960). In this case it might be expected that savings would be
 
possible given the existence of a second, phylogenetically older, visual structure
 
in the midbrain. Where lesions are more restricted, however, savings on visual
 
(in terms of shrinkage of the size of scotoma), somatosensory and motor
 
functions are age-related and show relatively better recovery even when damage
 
occurs early in the third decade of life as compared to later (Teuber, 1975).
 
Without doubt however, the most outstanding examples of functional recovery
 
are those which occur in the areas of language and spatial skills in man following
 
early injury.
 
 
 
The explanation of the functional recovery that does occur following early
 
brain damage is not straightforward. As discussed above, part of the restitu-
 
tional capacity may lie in mechanisms that enable individual neurones to
 
withstand injury so the functional extent of a lesion may be less than in the
 
mature system. It may also lie in neural regeneration per se, although Schneider
 
(1979) has provided evidence that such anomalous regeneration, when it occurs,
 
may actually result in greater behavioural deficit. In the case of the somatosensory and motor systems, while the greater volume of neural circuitry is
 
concerned with analysis and control of the contralateral side of the body,
 
ipsilateral pathways do exist. In the case of the motor system there is even
 
evidence that hypertrophy of ipsilateral pathways occurs after early hemi-
 
spherectomy (Hicks and D’Amato, 1970). These ipsilateral pathways may
 
assume greater functional importance in the case of unilateral brain damage and
 
sustain the limited behavioural savings that occur. The continued development
 
of linguistic and spatial skills after early brain damage are however of a different
 
order. It has been suggested that the survival of these skills in one hemisphere is
 
due to the fact that the necessary processors exist initially in each hemisphere but
 
that during development one hemisphere suppresses the influence of the other.
 
This suppression of the influence of the contralateral hemisphere may be a
 
necessary prerequisite for the development of higher cognitive skills, since
 
processing space may be at a premium. When both language and spatial skills
 
are acquired by only one hemisphere (following early hemispherectomy) neither
 
skill reaches its full potential (Teuber, 1975). Where the corpus callosum is
 
absent during development, and normal interhemispheric communication is
 
consequently impossible, a rather bizarre pattern of cognitive development is
 
 
 
 
 
 
 
DETERMINATE AND PLASTIC PRINCIPLES
 
 
 
 
 
227
 
 
 
 
 
seen. In such cases of callosal agenesis it appears that either performance IQ or
 
verbal IQ becomes pre-eminent despite the existence of functional capacity in
 
two hemispheres (Dennis, 1977). Extreme discrepancies do not in these cases
 
appear to be predictable from age of the subject at the time of testing, sex, type of
 
agenesis, handedness or specific neurological signs. It appears rather that a
 
mechanism which enables a normal balance of cognitive skills to occur is absent.
 
In the normal individual then the existence of two intact hemispheres may not be
 
sufficient for normal cognitive growth. Some additional mechanism which
 
ensures that unnecessary duplication does not occur and enables an efficient use
 
of available processing capacity seems to be necessary. The consequence of the
 
presence of such a mechanism during development is that usually specific skills
 
become established predominantly in one hemisphere or the other and once
 
they are so established there is little opportunity to recapitulate the process. The
 
failure of the adult brain to fully re-establish linguistic or spatial skills following
 
damage is a consequence of the presence of a mechanism (whose effector path is
 
the corpus callosum) that enables a balanced and complete cognitive growth to
 
occur.
 
 
 
 
 
Conclusions
 
 
 
Consideration of the evidence concerning the outcome of brain injury in the
 
developing nervous system leads to the inescapable conclusion that age at the
 
time of injury is a critical factor in determining both the initial syndrome and the
 
pattern of adaptation that follows. Certain abilities such as early maturing
 
spatial skills, language and various elementary sensory and motor functions may
 
show relative recovery, the extent being determined by the location and size of
 
the lesion. Other abilities, particularly those involving fine motor coordination,
 
late maturing spatial skills as well as the overall level of intellectual attainment,
 
may show more profound defects. These latter effects may be partly ascribed to a
 
lower overall processing capacity, but in the case of general intellectual
 
attainment, more profound effects are seen following damage to the right
 
hemisphere before (compared with after) one year of age, a factor which argues
 
that volume of tissue damaged is not the sole consideration. Differing patterns of
 
language disturbances are also seen in children depending on the child’s age at
 
the time pathology develops. These considerations, which emphasize that
 
damage is occurring within a system whose state is continually changing, present
 
particular difficulties for those with interests in the outcome of early brain
 
damage. As Teuber and Rudel (1962) point out: ‘Whether we are working with
 
infrahuman forms or with children, we must define (1) those aspects of
 
behaviour in which the effects of early injury appear only with a delay, as
 
development progresses; (2) those other aspects of performance in which there
 
will be impairment at all ages; and finally, (3) those aspects of performance
 
 
 
 
 
 
 
228
 
 
 
 
 
 
 
 
 
 
 
where there is an immediate effect which, however, disappears as development
 
proceeds’. The interpretation of research which finds age-dependent differences
 
is often far from clear. Reports that the patterning of IQ subtests is insensitive to
 
the location of injury in young children may be a genuine indication of an age-
 
dependent difference, despite the fact that such tests were not specifically
 
designed to assess brain damage. However, since it is found that in adults that IQ
 
tests are only indicative of lesion laterality in the acute but not the chronic phase
 
(Fitzhugh et al ., 1962), the failure to find specific indication of lesion location in
 
children with infantile injury may be attributable to the interval between injury
 
and testing rather than an age-related difference in functional organization.
 
 
 
The emergence of specific functional deficit following early brain injury
 
stresses the importance of critical structures for cognitive achievement. Just how
 
extensively the predesignated structures of the nervous system determine the
 
detailed characteristics of cognitive development remains to be seen. It is only
 
relatively recently that explorations of the specific patterns of loss, as measured
 
by specially developed tests, have begun. It is also apparent that much of the
 
research has been concerned with hemispheric asymmetry where the structural
 
similarity of the hemispheres means that the capacity for interhemispheric
 
reorganization may lead to an over-valuation of the plastic capacities of the
 
developing brain. Cases where bilateral loss of a structure is involved give one
 
much less confidence in the restitutional capacity of the young brain. Bilateral
 
frontal lobe damage in childhood appears to have effects at least as serious as
 
equivalent damage in adults (Russell, 1959; Ackerly, 1964) although the paucity
 
of research in this area and the anecdotal nature of some of the findings make
 
conclusions tentative. There is a scarcity of unequivocal evidence that areas of
 
the brain not normally involved in the development or performance of specific
 
functions may assume those functions when other areas are damaged. Goldman
 
and Lewis’s (1978) demonstration that the dorsolateral prefrontal cortex in the
 
macaque may assume some of the functional capability of the orbitofrontal
 
cortex, provided damage occurs early in development, remains one of the few
 
clear demonstrations of such effects in the CNS of primates following bilateral
 
lesions. However, the fact that the normal limits of plasticity and the extent to
 
which they may be influenced by specific experience remain undetermined, gives
 
developmental neuropsychologists particular problems in understanding the
 
precise nature of brain-behaviour interrelations. Nevertheless, the fact that
 
plasticity is a real phenomenon and may be influenced by specific experience
 
(Goldman and Lewis, 1978) gives some hope that understanding of its nature
 
may lead to more effective remediation regimes designed to capitalize on its
 
characteristics.
 
 
 
Acknowledgements
 
 
 
I am grateful to H. D. Ellis and E. A. Salzen for advice and discussion during preparation of this
 
manuscript.
 
 
 
 
 
 
 
DETERMINATE AND PLASTIC PRINCIPLES
 
 
 
 
 
229
 
 
 
 
 
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Annet, M., Lee, D. and Oimsted, C. (1961) Intellectual disabilities in relation to lateralised features of
 
the EEG. Little Club Clin. Devel. Med., 4, 86-112.
 
 
 
Basser, L. S. (1962) Hemiplegia of early onset and the faculty of speech with special references to the
 
effects of hemispherectomy. Brain, 85, 427-459.
 
 
 
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==Chapter Eight - Sex Differences in Brain Development: Process and Effects==
 
 
 
Miranda Hughes
 
 
 
 
 
Introduction
 
 
 
Identifying the neural mechanisms which underlie particular behavioural and
 
cognitive functions has become a fundamental aspect of psychological research,
 
and in recent years considerable progress has been made in understanding the
 
way in which both pre- and postnatal hormones can affect brain differentiation.
 
The notion that prenatal hormones which are differentially produced by males
 
and females may have irrevocable effects on the brain as well as on physical
 
morphology is politically provocative; nonetheless, improving our knowledge of
 
the neural substrates of behaviour ought also to facilitate our understanding of
 
how postnatal environment exerts its influence. Thus, to find sex differences in
 
brain differentiation, and to link these to sex differences in cognitive ability and
 
behaviour, does not necessarily imply biological determinism; rather, it
 
enhances our understanding of the raw materials which educational and cultural
 
pressures may mould in a variety of ways.
 
 
 
This chapter discusses the way in which pre- and postnatal hormones affect
 
brain differentiation, and it is argued that the long-term effects of the early
 
hormone environment may predispose any individual to certain ‘masculine’ or
 
‘feminine’ type behaviours. However, different aspects of our behavioural
 
repertoire are certainly under different degrees of hormonal influence and
 
human behaviour is not clearly sexually differentiated. As Money (1977a) put it
 
so cogently ‘... the only irreducible sex differences are that women menstruate,
 
gestate and lactate, and men impregnate ... most sexually dimorphic behaviour
 
 
 
 
 
233
 
 
 
 
 
 
 
234
 
 
 
 
 
 
 
 
 
 
 
as we know it is the product of cultural history and not of some eternal verity
 
programmed by non-cultural biology. 5 (pp. 32, 33).
 
 
 
Following Pfeiffer’s (1936) innovative and now classic work, the precise role of
 
prenatal hormones in the development of the hypothalamic mechanisms which
 
control hormone release at puberty, and which are responsible for the development of sexually differentiated physical characteristics, is well established
 
(Harris, 1964, 1970). The well documented cases of children exposed to
 
abnormal levels of particular steroids in utero (Money and Ehrhardt, 1972), and
 
the work of Dorner (1979) on human homosexuality, have subsequently raised a
 
number of questions concerning the effect of hormones on a wide range of
 
behaviour. The line of reasoning seems to be that if (a) some neural mechanisms
 
(e.g. for gonadotropin release at puberty) are determined by the role of prenatal
 
hormones, and (b) foetuses exposed to abnormal levels of types of particular
 
hormones behave in specific and atypical ways, then it follows that (c) just as the
 
prenatal hormonal environment has ‘wired-up 5 the brain in such a way as to
 
determine the expression of certain endocrine functions, so too can it predispose
 
an organism to specific behaviour patterns. A closer examination of the three
 
stages of this argument should facilitate the development of a conceptual
 
framework within which to extend our understanding of the variety of
 
expression in human abilities and behaviour.
 
 
 
 
 
Prenatal sex differences in development
 
 
 
Distinctively male or female development begins at around the seventh week
 
after conception when the initially bi-potential embryonic gonad differentiates
 
to form either a testis (in the case of a male) or an ovary (in the case of a female).
 
This differentiation of the gonads is determined by the genetic sex of the zygote
 
(46XY in the male; 46XX in the female); where there is no second sex
 
chromosome as in Turner’s syndrome (45X) the gonads are undifferentiated at
 
birth, although germinal follicles may have been present in the early foetal stages
 
(Scott, 1978). Jost (1979) tentatively suggests that there may be a specific
 
membrane protein controlled by a locus on the Y chromosome (the H-Y
 
histocompatibility antigen) which is responsible for the differentiation of testes,
 
and whose individuals who do not produce this antigen will form an ovary. Once
 
a testis has been formed the release of a substance (probably a foetal protein)
 
known as Mullerian inhibiting substance (MIS) induces the regression of the
 
Mullerian ducts, and secretion of androgenic hormones enables the development of the male reproductive tracts and genitalia. In the absence of testicular
 
hormones female development occurs; ‘...in mammals and birds body sex
 
shows a basic developmental trend corresponding to that of the homozygous
 
sex. Characteristics of the heterozygous sex have to be actively imposed by the
 
secretions of the corresponding gonads 5 (Jost, 1979, p. 8). Thus, the appearance
 
 
 
 
 
 
 
SEX DIFFERENCES IN BRAIN DEVELOPMENT 235
 
 
 
of Turner’s syndrome infants is unequivocally female, and that of Klinefelter’s
 
syndrome infants (47XXY and 48XXXY) is unequivocally male.
 
 
 
Sexual differentiation does not, however, always proceed entirely smoothly,
 
and Scott (1978) has provided a useful classification of some ‘intersex’ conditions. He suggests that there are four basic processes which may distort normal
 
sexual differentiation: (i) chromosomal intersex, in which extra or missing sex
 
chromosomes affect development; (ii) gonadal intersex, in which the gonadal
 
tissue is at variance with the chromosomal constitution of the individual; (iii)
 
partial masculinization of chromosomal and gonadal females, due either to a
 
disorder of adrenal functioning or the exogenous administration of steroid
 
hormones to the mother; and (iv) incomplete masculinization of chromosomal
 
and gonadal males which may occur either because an individual is insensitive to
 
the androgen being produced by the testes or because there is some failure in
 
androgen production. These medical conditions have often been described as
 
‘nature’s experiments’ because they shed light on the various ways in which
 
hormones affect development.
 
 
 
In Turner’s syndrome, the missing chromosome may be either an X or a Y:
 
evidence for this comes from a report by Leujeune (1964) of monozygotic twins,
 
one of whom was a normal male of 46XY karyotype, the other of whom was
 
born with 45X karyotype (and therefore a female phenotype). Turner’s
 
syndrome females are typically short in stature, and require oestrogen therapy at
 
puberty to effect normal breast development. There may be a range of other
 
physical stigmata present (e.g. shield chest, neck webbing, low-set ears), but
 
general intelligence is not significantly affected (Money and Ehrhardt, 1972).
 
The streak gonads are often entirely non-functional, but they may contain some
 
ova in which case pregnancy is possible.
 
 
 
There are approximately two cases per thousand of males with a 47XXY
 
karyotype, and a similar number with 47XYY karyotype. The former often have
 
small testes and prostates and diminished body and facial hair; they may also
 
show some breast development at puberty, and are frequently infertile. Males
 
with 47XYY karyotype have a tendency to be taller than average, but otherwise
 
display no specific physical abnormalities. It has been estimated that both
 
47XXY and 47XYY males are over-represented in mental or penal institutions
 
during late adolescence or adulthood. Differences between these groups in
 
deviant behaviour are not significant; however, their crimes are more likely to be
 
sex or property offences than those of their delinquent peers (Meyer-Bahlburg,
 
1974).
 
 
 
Cases of gonadal intersex (hermaphroditism) show widely varying arrangements of gonadal tissue and genitalia. Scott (1978) suggests that there may be an
 
interchange of genetic material between the X and Y chromosome before the first
 
meiotic division in the primary spermatocyte, which could lead to widely
 
varying sexual differentiation according to the cells in which the Y chromosomal
 
 
 
 
 
 
 
236
 
 
 
 
 
 
 
 
 
 
 
material is active. Such cases clearly do not provide a homogeneous subject
 
sample, but are nonetheless interesting individually.
 
 
 
The partial masculinization of females and the incomplete masculinization of
 
males illustrate clearly the role of steroids in the development of sex-related
 
physical characteristics. The former of these conditions is usually due to
 
congenital adrenal hyperplasia (CAH) which occurs as a result of an enzymatic
 
deficiency in the adrenal steroid metabolic pathways. The most common form of
 
CAH is 21-hydroxylase deficiency which results in a build-up of 17-hydroxypro-
 
gesterone, the metabolic derivatives of which have a virilizing influence on the
 
female foetus. Male infants appear normal at birth (although puberty may be
 
accelerated by as much as ten years if the condition is not diagnosed and
 
treated), but female infants have masculinized external genitals. The female
 
internal organs are normal, and with appropriate medical treatment (including
 
surgery to feminize the genitals) these girls may menstruate at puberty and
 
eventually bear children.
 
 
 
Masculinization of females may also arise from the influence of steroid
 
hormones administered to the mother during pregnancy to prevent miscarriage.
 
Ehrhardt and Money (1967) report ten such cases, and Scott (1978) describes an
 
individual case following the administration of norethisterone to the mother. As
 
in the CAH cases, masculinization is apparently restricted to the external
 
genitalia, and can be corrected surgically.
 
 
 
There are three possible defects of the androgenization process which can give
 
rise to the incomplete masculinization of the male: defective androgen production, defective Mullerian regression, and androgen insensitivity. The last of
 
these is the best documented and is often known as ‘testicular feminization’. In
 
this condition infants with a normal male 46XY chromosome complement are
 
born with a female phenotype. Since Mullerian regression has occurred
 
normally, there is a short blind vagina, but the external genitalia are unequivocally female. At puberty, there is spontaneous breast development, although
 
pubic hair tends to be scant. The condition occurs despite normal steroid output
 
from the testes, when the receptor cells fail to respond to the androgens which
 
are present.
 
 
 
Individuals with complete androgen insensitivity may be quite oblivious to
 
their condition until puberty, when they seek medical advice for amenorrhea.
 
However, there are incomplete forms of androgen insensitivity: for example,
 
where there is a failure to convert testosterone to the more potent 5a-
 
dihydrotestosterone there may be incomplete masculinization of the external
 
genitalia. Imperato-McGinley et al (1974) described some such cases in which
 
the affected infants are given a female assignment at birth, but at puberty have to
 
undergo a gender re-assignment because ‘anabolic events at puberty, in
 
particular the increase in muscle mass, the growth of the phallus and scrotum,
 
and the voice change, appear to be mediated by testosterone’ (p. 1214).
 
 
 
 
 
 
 
SEX DIFFERENCES IN BRAIN DEVELOPMENT
 
 
 
 
 
237
 
 
 
 
 
All of these ‘intersex’ conditions have considerable interest for psychology, in
 
that they provide an opportunity to examine the possible behavioural effects of
 
the prenatal hormones. It is certainly true that the prenatal hormonal environment affects cell differentiation in the brain; the speculations which require
 
critical examination are those concerning the behavioural implications of such
 
hormonal effects.
 
 
 
 
 
Hormonal action
 
 
 
The role of prenatal hormones in the development of the internal sex organs and
 
genitalia is clearly established. If these hormones exert equally critical influences
 
on brain differentiation, one would expect to find different patterns of neural
 
networks in male and female brains. It is instructive therefore to examine the
 
mechanism whereby hormones exert their influence so that sex differential
 
developmental processes can be appropriately evaluated, and any anomalies of
 
normal development can be interpreted.
 
 
 
The steroid hormones include the male sex hormones (androgens), the female
 
sex hormones (oestrogens and progestins), and the hormones secreted by the
 
adrenal glands (corticosteroids). Structurally, they resemble one another quite
 
closely but differ radically in function. Their common core structure consists of
 
four interconnected carbon rings. The pattern of bonding and the different side
 
groups affect the overall shape of each molecule, and it is these subtle differences
 
in shape which enable the hormones to attach themselves to specific target cells.
 
 
 
Hormones act directly on genetic mechanisms, so that when gene action is
 
blocked (for example, by the action of certain antibiotics) hormones become
 
powerless to exert their characteristic effect. A single hormone can activate an
 
entire set of functionally related but otherwise quite separate genes, and
 
hormonal specificity is dependent on the functional integrity of the target cells as
 
much as on the hormone itself. The cytoplasm of target cells contains specific
 
intracellular receptor proteins which accumulate and retain the hormone (this in
 
contrast to the receptor mechanism of say, amines, for which the receptor site lies
 
in the cell membrane). The steroid hormones then give rise to an increase in
 
RNA synthesis, and can also effect the synthesis of a new variety of messenger
 
RNA; these RNA molecules direct the formation of new protein molecules in the
 
cytoplasm of the cell which enable the target cell to make its functional responses
 
to the hormone.
 
 
 
During development the presence of male hormones will (in general) have a
 
masculinizing effect on a genetic female. However, in experiments on rats it was
 
found that whilst testosterone increased the amount of RNA produced in the
 
liver cells of both males and females, in the female not only was there an
 
increased amount of RNA, but a new type of RNA was being produced; this
 
finding does suggest that even when male and female developing embryos are
 
 
 
 
 
 
 
238
 
 
 
 
 
 
 
 
 
 
 
exposed to similar hormonal environments, the consequences need not
 
necessarily be identical (Davidson, 1965). There has been some attempt to
 
discover whether sex differences in brain differentiation are mediated by sex
 
differences in cytoplasmic receptors. Data from Maurer (1973) and from Whalen
 
(1974) show that there was selective cytoplasmic binding of oestrogen in the
 
anterior hypothalamic-preoptic area (of rats), in the median eminence, but not in
 
the cortex; however, the sex differences were not striking \ .. it seems unlikely
 
that the small difference in nuclear retention that we found can account for the
 
large differences existing between males and females in their behavioural
 
responses to oestrogen’ (Whalen, 1974, p. 278).
 
 
 
 
 
Sex differences in brain differentiation
 
 
 
Pfeiffer (1936) was the first to establish that sex differences in the reproductive
 
endocrinology of rats were determined by the hormone environment at a specific
 
stage of development. He demonstrated that if a male rat is castrated within 3
 
days after birth and is subsequently (in adulthood) given ovarian grafts, he will
 
respond to endogenous hormones with a surge of luteinizing hormone (LH)
 
which is sufficient to produce corpora lutea in the ovarian graft. When the
 
ovaries of newborn females were replaced with testes, many of these females
 
failed to show any sign of oestrous cycles when they became adult, but entered a
 
state of constant vaginal oestrus. However, female rats, which were ovari-
 
ectomized at birth and subsequently had received ovarian implants, showed
 
normal oestrous cycles and formation of corpora lutea. Male rats in which the
 
testes were transplanted into the neck region at birth, and which received
 
ovarian implants as adults, showed no capacity to form corpora lutea in the
 
ovarian grafts. Pfeiffer concluded (erroneously) that the pituitary gland becomes
 
sexually differentiated; subsequent experiments (see Harris, 1964, 1970) made it
 
clear that in fact permanent control by the hypothalamus over the pituitary was
 
established by the presence or absence of testosterone in a critical neonatal
 
period. In the absence of testosterone a pattern of cyclic release of follicle
 
stimulating hormone (FSH) and LH by the pituitary was established; when
 
testosterone was present, release of hormones was tonic. Reznikov (1978) states
 
that the critical periods for the sexual differentiation of the brain centres which
 
regulate gonadotropin release \ .. occur in rabbits during the period of 19-23
 
days, and in guinea pigs at 36-38 days of pre-natal life, in rats, mice and
 
hamsters, in the course of the first five days after birth. In the case of humans, the
 
most probable period of sexual differentiation is considered to be the second
 
trimester of pregnancy. It should be emphasised that experimental influences
 
exerted outside the “critical” period are incapable of moderating the sex-
 
specifying parameters of differentiation of the brain’ (p. 127).
 
 
 
Barraclough and Gorski (1961) demonstrated that cyclic gonadotropin
 
 
 
 
 
 
 
SEX DIFFERENCES IN BRAIN DEVELOPMENT
 
 
 
 
 
239
 
 
 
 
 
release in female rats is regulated from a specific centre in the pre-optic
 
hypothalamic region, whereas tonic gonadotropin response is regulated from
 
the hypothalamic ventromedial arcuate region. Bari Kolata (1979) reviews the
 
recent evidence that (in rats) it is the aromatization of testosterone to oestrogen
 
which is crucial in the sex differences which occur during brain differentiation:
 
when testosterone reaches the brain cells of newborn male rats it is converted to
 
oestrogen and dihydrotestosterone but newborn female rats’ brains are protected from the effects of endogenous oestrogen by a-fetoprotein (a protein made
 
by the fetal liver) which binds oestrogen and thus prevents it from reaching the
 
developing brain. However, animals whose critical period for brain differentiation ends before birth (such as humans) have a-fetoproteins which do not bind
 
oestrogens, and it is not yet clear what mechanisms might protect those animals’
 
brains from the effects of oestrogen.
 
 
 
 
 
Behavioural effects of sex differences in brain differentiation
 
(i) Sexual behaviour
 
 
 
The effects of pre- and perinatal hormones on the sexual behaviour of infrahuman species are reviewed carefully by Hoyenga and Hoyenga (1980), and the
 
interested reader is referred to their text for a detailed list of primary sources. The
 
evidence that early hormones are critical in determining sexual behaviour is
 
unequivocal: neonatal castration of male rats (i.e. deandrogenization) increases
 
all types of female sexual behaviours; and the prenatal androgenization of
 
female rats increases the incidence of mounting and decreases the incidence of
 
lordosis (the female sexual response consisting of concave arching of the back
 
with simultaneous raising of the head and hind-quarters). Comparable evidence
 
is available from primate studies. However, the perinatal administration of
 
androgen to a female rat does not entirely masculinize her complete repertoire of
 
sexual behaviour, any more than the castration of a male entirely suppresses all
 
male-type responses.
 
 
 
Whalen (1974) proposed an orthogonal model of sexual differentiation in
 
which he suggested that ‘during development hormones can defeminize without
 
masculinizing and masculinize without defeminizing, and that hormones can
 
defeminize one behavioural system (e.g. mating) while masculinizing another
 
system’ (p. 469). This conception is not really satisfactory, for if one considers
 
any specific aspect of sexual behaviour (such as lordosis) it is difficult to see how
 
‘masculinization’ does not also imply ‘defeminization’; however, it does try to
 
deal with the data which indicates that lordosis in the female is not necessarily
 
inhibited by perinatal administration of testosterone, even though she also
 
exhibits increased incidence of mounting. In the same article Whalen raises some
 
important criticisms of the naivety of the behavioural analysis which has often
 
been employed in studies of sexual behaviour, and similar criticism is reiterated
 
 
 
 
 
 
 
240
 
 
 
 
 
 
 
 
 
 
 
by Beach (1979). Responses such as lordosis can be only partially completed,
 
and neonatally androgenized females do exhibit weak or partial lordosis
 
responses with moderate frequency. Similarly, mounting is not always accompanied by intromission and ejaculation. A fmer-grained categorization of the
 
behavioural units which comprise ‘sexual behaviour’, and due attention to
 
controlling for the stimulus conditions in which it occurs, might facilitate our
 
understanding of its general structure, and thus enhance our knowledge
 
concerning the differential effects of various hormones. Beach suggests that both
 
male and female brains have the appropriate neural substrates for homotypical
 
and heterotypical sexual behaviour, and that sexual differentiation of the brain
 
serves to alter the probability of a particular response being elicited in a given set
 
of stimulus conditions. Thus, demasculinization does not eradicate the possibility of a male type response, it simply reduces its probability of occurrence.
 
Figure 8.1 shows the critical period during which sexual differentiation of the
 
brain occurs in rats. The degree to which the behaviour of the female rat is
 
masculinized is dependent both on dosage and on timing of testosterone
 
administration.
 
 
 
 
 
 
 
Figure 8.1 The effects of perinatal testosterone or castration on neonatal rats.
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
 
SEX DIFFERENCES IN BRAIN DEVELOPMENT
 
 
 
 
 
241
 
 
 
 
 
There is some interesting evidence from Dorner’s laboratories (Dorner, 1977,
 
1979) that human sexual behaviour may be affected by the prenatal hormonal
 
environment. ‘An androgen deficiency in genetic males during a critical period of
 
brain organization gives rise to predominantly female differentiation of the
 
brain. This androgen deficiency in early life can be largely compensated by
 
increased hypophyseal gonadotropin secretion in later life. Thus, the predominantly female-differentiated brain is post-pubertally activated by an approximately normal androgen level, leading to homosexual behaviour’ (Dorner, 1979,
 
p. 87). The evidence from which this conclusion is derived comes partly from an
 
experiment in which adult males were given an intravenous oestrogen injection:
 
in homosexual males there was a subsequent rise in LH values above initial
 
levels (a response which would be normal in females), whereas in bisexual and
 
heterosexual males no such rise was detected. Goy and McEwen (1980) express
 
some discomfiture with these data, and in particular point to evidence of time-
 
dependent partial dissociation between the differentiation periods of central
 
nervous centres regulating gonadotropin secretion and those responsible for
 
sexual behaviour. However, Dorner (1977, 1979) clearly believes that the
 
evidence of a relationship between prenatal hormones and adult sexual
 
behaviour is now sufficiently strong to contra-indicate the prescribing of any
 
androgenic or anti-androgenic substances to pregnant women, and recent data
 
on females with CAH may tentatively support this view. In contrast to earlier
 
findings which suggested that CAH females were no different from normal
 
controls in their heterosexual interests and behaviour (Ehrhardt et al ., 1968a;
 
Ehrhardt et a/., 19686) a more recent investigation by Money and Schwartz
 
(1977) has suggested that early treated CAH females may be delayed in
 
establishing dating and romantic interests. In addition, they found that in their
 
sexual fantasies CAH females showed an increased rate of awareness of
 
bisexuality relative to controls (although this did not necessarily reflect actual
 
experience). It is plausible that these more recent data reflect a less prescriptive
 
social climate than that which prevailed during the early 1960s when the original
 
data were presumably collected, and one can only conclude that the nature of the
 
biological, cognitive and social factors which regulate human sexual behaviour
 
are by no means well established. This area remains wide open to debate.
 
 
 
(ii) Non-sexual behaviour
 
 
 
The effects of pre- and perinatal hormones on animals are not restricted to
 
endocrinology and sexual behaviour. Levine (1966) cites evidence which
 
demonstrates that female rats who have been injected as neonates with
 
testosterone show male-type behavioural responses in an open field; and that
 
female rhesus monkeys injected with testosterone in utero show levels of rough
 
and tumble play which are approximately equivalent to those of normal male
 
monkeys. Goy (1968, 1970) reports that initiation of play and pursuit play are
 
 
 
 
 
 
 
242
 
 
 
 
 
 
 
 
 
 
 
greater in neonatally androgenized female monkeys than in normal females, and
 
a number of workers have reported effects of neonatal hormones on activity
 
(Gray et al ., 1975; Stewart et al ., 1975), exploration (Quadagno et al ., 1972;
 
Gummow, 1975), and learning (Beatty and Beatty, 1970; Dawson, 1972;
 
Dawson et al ., 1973). Quadagno et al. (1977) have reviewed the extensive
 
literature on the effects of perinatal hormones on non-sexual behaviours with
 
particular reference to energy expenditure, maternalism and learning, and they
 
are able to conclude that the effects of early hormones on the behaviour of infrahuman species are well established.
 
 
 
McEwen (1976) and Goy and McEwen (1980) describe the experimental data
 
which have led to the identification of specific neural pathways that are
 
established by the influence of sex hormones and are sexually differentiated, and
 
which underlie sex differences in behaviour. The work of Raisman and Field
 
(1973) represented an important breakthrough in this field: they found that
 
adult female rats have more dendritic spine connections in the preoptic area than
 
males, but that males castrated within 12 hours of birth have spine connections
 
equivalent *o those of the female. They demonstrated that those animals which
 
show frequerd lordosis have different patterns of synaptic connectivity than
 
animals with a limited capacity for lordosis. Various other studies have also
 
shown that the brain of a male rat deprived of androgen and the female exposed
 
to androgen will take on heterotypical characteristics: for example, the size of
 
the cell nuclei in the preoptic area is positively correlated with the degree of
 
lemaleness’ in the rat’s sexual behaviour (Dorner and Staudt, 1968, 1969); both
 
serotonin levels (Ladosky and Gaziri, 1971) and RNA metabolism (Clayton et
 
al ., 1970) are also affected. Litteria and Thorner (1974) and Phillips and Deol
 
(1973) report sex differences in the cerebellum and septum which can be reversed
 
by the presence or absence of androgens. However, even if these differences do
 
indeed underlie the observed differences in behaviour (as seems plausible) and
 
we assume that similar mechanisms of differentiation occur in humans, it is
 
nonetheless unlikely that human behaviour would be so strongly determined by
 
neural networks (particularly in the face of conflicting socialization).
 
 
 
 
 
Hormonal anomalies in human development
 
 
 
The data from the above animal studies provide sufficient evidence for the
 
assertion that hormones are critical in determining patterns of brain differentiation, and suggest that pre- and perinatal hormones may also exert long-term
 
effects on behaviour patterns. It is instructive then, to consider the effects of early
 
hormones on human behaviour insofar as this can be achieved within the
 
limitations of ethical considerations (see Reinisch and Gandelman (1978) for an
 
interesting discussion of these issues). It has already been noted that prenatal
 
hormones affect the development of sex-typical physical characteristics, and
 
 
 
 
 
 
 
SEX DIFFERENCES IN BRAIN DEVELOPMENT
 
 
 
 
 
243
 
 
 
 
 
individuals with anomalous genital development at birth, or who present with
 
related problems at puberty (e.g. amenorrhea in patients with testicular
 
feminization), have been studied by psychologists interested in the possible
 
effects on hormones on behaviour.
 
 
 
Two clinical syndromes can be regarded as close counterparts of experimental
 
anti-androgenization (or demasculinization) in animals: Turner’s syndrome and
 
testicular feminization due to androgen insensitivity. In Turner’s syndrome the
 
missing chromosome may be either an X or a Y, and if a few androgen-secreting
 
cells remain in the gonadal streak tissue there may be a mild degree of labial
 
fusion and an enlarged clitoris. Some individuals have a 45X/45XY mosaic
 
karyotype: they have testes, but these are not properly formed and are at high
 
risk for cancer (Money, 1911b). Thus, deandrogenization in Turner’s syndrome
 
is due to a failure of the gonads to manufacture androgens; in contrast, other
 
testicular feminization syndromes are a result of the failure of the target organ
 
cells to take up and utilize the androgens which are secreted from testes in
 
foetuses with the normal 46XY karyotype.
 
 
 
The behaviour of girls and women with either Turner’s syndrome or testicular
 
feminization is unequivocally feminine. In the case of Turner’s syndrome there
 
seems even to be a tendency of extreme conformity to female sex stereotypes:
 
they are known to fight less, to be less athletic and to be more interested in
 
personal adornment than control comparisons (Money and Ehrhardt, 1972);
 
and Theilgaard (1972) reported that women with Turner’s syndrome preferred
 
to wear very feminine-style clothing and jewellery. All but one of the 15 girls in
 
the group studied by Money and Ehrhardt (1972) had played exclusively with
 
dolls, and most of them expressed a very strong interest in maternalistic activities
 
associated with child care. In their anticipation and imagery of romance and
 
motherhood, Turner’s syndrome females were found to be no different from their
 
control comparisons. From these data, one may infer that differentiation of a
 
feminine gender role is not dependent on the presence of prenatal gonadal
 
hormones, nor does it require the presence of a second X chromosome. Indeed,
 
Money and Ehrhardt are prepared to assert that ‘a feminine gender identity can
 
differentiate very effectively without any help from prenatal gonadal hormones
 
that might influence the brain and perhaps, in fact, all the more effectively in
 
their absence’ (p. 108).
 
 
 
Babies born with the testicular feminization syndrome look like absolutely
 
normal females, although these females tend to be of above average height
 
(Money, Ehrhardt and Masica (1968) quote a mean height of 5 feet 1\ inches for
 
their sample of ten patients). Diagnosis of their condition normally follows
 
referral for primary amenorrhea so data regarding behaviour in early childhood
 
are necessarily based on retrospective report (which may be influenced by
 
knowledge of their condition). Even with this caveat in mind the data reported
 
by Money et al (1968) and Money and Ehrhardt (1972) do seem to provide
 
 
 
 
 
 
 
244
 
 
 
 
 
 
 
 
 
 
 
strong evidence for the unequivocal differentiation of female gender role in these
 
patients. They reported playing primarily with dolls in early childhood and
 
having dreams and fantasies which reflected the normal sex-role stereotypes of
 
marriage and motherhood. With one exception these women rated themselves as
 
fully content with the female role, and at adolescence they conformed with the
 
normal patterns of heterosexual behaviour. Most of them expressed positive
 
enjoyment in adopting ‘feminine’ styles of dress and personal adornment. ‘Babies
 
with the androgen insensitivity syndrome who are consistently reared as girls
 
have no uncertainties about themselves as girls, women, wives, sexual partners,
 
and mothers by adoption ... they grow to be womanly in their behaviour, in
 
their erotic mental imagery, and in their self-perception, even when they know
 
the medical terminology of their diagnosis’ (Money, 1977a, p. 262).
 
 
 
Reifenstein’s syndrome resembles that of complete androgen insensitivity
 
except that there is partial masculinization of the genitalia during foetal life and
 
the neonate is thus sometimes classified as a male. At puberty the development of
 
secondary sex characteristics nevertheless proceeds as described above.
 
According to Money and Ogunro (1974) those infants assigned as males did not
 
show any preference in childhood for female-type activities (doll play etc.) and
 
made concerted efforts to compensate for their relative inferiority in athletic
 
pursuits. At puberty, their breasts had to be surgically removed; in adulthood
 
their physiognomy is beardless and unvirilized, and because of their extremely
 
small, surgically repaired genitalia they may encounter some difficulty establishing a sex life (none reported homosexual preference). On the whole, gender
 
identity conforms with socialization and there seems to be no evidence from
 
these cases of any biologically based behavioural imperative for feminization.
 
These cases may reflect the experimentally induced ‘demasculinization’ without
 
accompanying ‘feminization’; and as far as we can tell from these few cases the
 
social environment is a paramount factor in influencing preferred activity and
 
gender identity.
 
 
 
The form of male pseudohermaphroditism described by Imperato-McGinley
 
et al (1974) results from a 5a-reductase deficiency which leads to incomplete
 
differentiation of the external genitalia at birth, and thus a female sex assignment
 
is often made. At puberty, however, differentiation of male characteristics occurs
 
and sex re-assignment is necessary. A recent report by Savage et al (1980)
 
confirms the rather surprising finding that this gender-role transition is made
 
relatively easily and they conclude ‘... that exposure of the brain to androgens
 
during foetal life and thereafter appears to have had more effect on determining
 
gender identity than the pre-pubertal sex of rearing’ (p. 404).
 
 
 
In the light of this conclusion it is interesting to consider the effects of the
 
masculinization of a female foetus. These have been documented in two clinical
 
syndromes: progestin-induced hermaphroditism (PIH) and the adrenogenital
 
syndrome (CAH). PIH occurred following the administration of synthetic
 
 
 
 
 
 
 
SEX DIFFERENCES IN BRAIN DEVELOPMENT
 
 
 
 
 
245
 
 
 
 
 
progestins to pregnant mothers with histories of miscarriage; these steroids were
 
devised as substitutes for the pregnancy hormone, progesterone, but because
 
their chemical structure was similar to androgen, they exerted an unexpected
 
masculinizing effect on a female foetus (Walker and Money, 1972). Once this
 
effect was discovered (in the early 1950s) the use of these hormones was
 
discontinued; however, the subsequent development of girls born with PIH has
 
been studied (Ehrhardt and Money, 1967; Money and Ehrhardt, 1972). If the
 
external genitalia were surgically feminized shortly after birth, no further
 
surgical or hormonal treatment was required; this is in contrast to girls born
 
with CAH who require constant maintenance on cortisone to prevent continuing postnatal masculinization and accelerated pubertal development. Table
 
8.1 summarizes some of the data obtained on the reported behaviour of these
 
cases. Basically, there is little difference between that of the PIH and CAH girls,
 
but both these groups differ significantly from control comparisons on measures
 
of tomboyism, athletic skills and preference for boys’ toys (e.g. cars, guns etc.).
 
Perhaps, as a result of these interests, it is not surprising that these girls also
 
prefer male playmates.
 
 
 
The accuracy of assessment of behaviour in these cases is difficult to evaluate
 
and Ehrhardt and Baker (1974) are clearly aware of this when they discuss, in
 
some detail, exactly how the interviews with patients and their parents were
 
conducted. It is important to be aware'that no observations were made of the
 
 
 
 
 
Table 8.1 Behavioural effects of prenatal exposure to androgens*
 
 
 
 
 
Childhood behaviour
 
 
 
PIH
 
 
 
CAH
 
 
 
Tomboyism
 
 
 
above average
 
 
 
above average
 
 
 
Athletic interests and skills
 
 
 
above average
 
 
 
above average
 
 
 
Preference for male playmates
 
 
 
above average
 
 
 
above average
 
 
 
Preference for ‘functional’ clothing
 
 
 
above average
 
 
 
above average
 
 
 
Preference for toy cars, guns etc. over dolls
 
 
 
above average
 
 
 
above average
 
 
 
Anticipation of future
 
 
 
Priority of career over marriage
 
 
 
above average
 
 
 
above average
 
 
 
Heterosexual romanticism
 
 
 
normal
 
 
 
normal
 
 
 
Anticipation of pregnancy
 
 
 
normal
 
 
 
Less frequently reported
 
than controls
 
 
 
Dissatisfaction with female role
 
 
 
no
 
 
 
no
 
 
 
Sexual behaviour
 
 
 
Childhood-shared genital play/copulation
 
play
 
 
 
normal
 
 
 
normal
 
 
 
Adolescent boyfriend and dating
 
 
 
normal
 
 
 
normal
 
 
 
Bisexual/homosexual fantasy
 
 
 
(data not available)
 
 
 
above average
 
 
 
Bisexual/homosexual behaviour
 
 
 
no
 
 
 
within normal range
 
 
 
 
 
*Data adapted from Ehrhardt (1977); Ehrhardt and Baker (1974); Epstein and Money (1968);
 
Ehrhardt and Money (1967); Money and Ehrhardt (1972); Money and Schwartz (1977).
 
 
 
 
 
 
 
246
 
 
 
 
 
 
 
 
 
 
 
children and that reliability was assessed purely in terms of the concordance
 
between the mother’s and child’s reports. Even so, these data do seem to reflect a
 
tendency for increased activity in females who have been exposed to abnormally
 
high levels of androgen in utero ; and compatible with these tomboyish interests,
 
these girls also seem less interested than control comparisons in personal
 
adornment and maternal behaviours. Their gender identity is nonetheless
 
entirely female (although 35% of them said they would not mind being a
 
boy).
 
 
 
It appears then, that the effect of prenatal androgens on gender identity
 
cannot be as imperative as Imperato-McGinley et al. (1974) and Savage et al
 
(1980) suggest; it is more likely that the activational effects of circulating male
 
hormones at adolescence are crucial to the satisfactory transition to the male
 
gender role for these male pseudo-hermaphrodites. However, the surmise that
 
the behavioural development of CAH and PIH females is in some way
 
analogous to that of prenatally androgenized monkeys (Goy, 1968) is certainly
 
supported by the available data. Furthermore, it is interesting to note that whilst
 
the excess of androgens may be contributing to a masculinizing effect on some
 
behaviours it does not have a global ‘defeminizing’ effect. Indeed, a sample of
 
late-treated CAH patients described by Ehrhardt, Evers and Money (1968)
 
conform strongly to female sex stereotypes in their careers and/or marriages. In
 
fact, the influence of prenatal androgen exposure is probably limited to a specific
 
effect which in some way creates a predilection for physical energy expenditure;
 
associated preferences for functional clothing and male playmates may be no
 
more than a reflection of this basic trait. This conclusion is confirmed to some
 
extent by the finding that males with CAH are no different from a comparison
 
group of unaffected male siblings except that they are more frequently (80 % of
 
CAH males: 20% sibs) reported to engage in intense energy expenditure
 
(Ehrhardt and Baker, 1975).
 
 
 
In two studies (Zussman et al. (1975) cited in Goy and McEwen, 1980;
 
Ehrhardt et al, 1975) which considered the effects of prenatal progesterone on
 
childhood behaviour (not the androgenic progestins which caused PIH),
 
subjects were found to exhibit lower energy levels and a tendency to prefer
 
‘female type’ clothing styles. They suggest that non-androgenic progestins may
 
actively counteract androgen effects in utero in both males and females.
 
 
 
During childhood, then, the major behavioural effect of prenatal androgenic
 
hormones is on activity level: when the foetus has been exposed to androgen,
 
he/she will subsequently display a predilection for high levels of physical energy
 
expenditure (and these effects appear to be dose-related). These results are
 
consonant with the findings on the effects of androgens in rodents and primates
 
(Quadagno et al , 1977), and they do suggest that these hormones have an
 
organizing effect on brain differentiation which will usually be sexually
 
dimorphic.
 
 
 
 
 
 
 
SEX DIFFERENCES IN BRAIN DEVELOPMENT
 
 
 
 
 
247
 
 
 
 
 
Personality
 
 
 
Reinisch (1977) argues that prenatal exposure to (non-androgenic) progestin
 
also has long-term effects on personality, and her data confirm the earlier
 
suggestions of Ehrhardt and Money (1967) that progestin-exposed subjects
 
show high levels of self-assertive independence and self-reliance. Twenty-six
 
subjects, whose mothers had been administered a minimum dosage of 40 mg
 
progestin for at least four weeks during the first trimester of pregnancy, were
 
tested on age-appropriate Cattell Personality Questionnaires. They exhibited
 
high scores on individualistic, self-assured and self-sufficient factors relative to
 
sibling controls. In contrast, subjects exposed to high oestrogen levels in utero
 
were found to be more group-dependent and group-oriented than a sibling
 
control group.
 
 
 
An investigation by Yalom, Green and Fisk (1973) also attempted to evaluate
 
the long-term effects of prenatal oestrogens on personality. Because diabetic
 
women produce lowered levels of oestrogen and progesterone during pregnancy
 
they are sometimes prescribed supplemental doses of these hormones; Yalom et
 
al. studied the male children of diabetic mothers who had received high
 
oestrogen doses, and compared them to a control group of children with normal
 
mothers and a group of children of untreated diabetic mothers. At the age of 6
 
the boys who had been exposed to the highest levels of oestrogen were rated by
 
their teachers as being less assertive and less athletic than their male peers. By
 
the age of 16 a whole range of behaviours seemed to be related (albeit weakly)
 
to the level of oestrogen exposure: athletic coordination, competitiveness,
 
assertiveness, aggression, and global measures of ‘masculinity’. The children of
 
diabetic mothers who had not received oestrogen supplements were consistently
 
more masculinized than the control group of sons of normal mothers, and the
 
children of mothers who had received supplemental oestrogen were the least
 
masculine. It is possible that some of these effects may be due to differing levels of
 
activational hormones in these boys since the development of the testes and
 
output of testicular hormones are likely to have been affected (Zondek and
 
Zondek, 1974).
 
 
 
 
 
Cognitive ability
 
 
 
In an exhaustive review of psychological sex differences, Maccoby and Jacklin
 
(1974) concluded that males show superior visuo-spatial and mathematical
 
abilities relative to females. Females though, are better at some verbal skills: they
 
are more fluent, they are better readers and spellers, and their speech is more
 
comprehensible than that of males (Harris, 1977). The extent to which these
 
differences reflect underlying differences in neural organization has been a
 
matter of considerable debate (Archer, 1976) since the influence of differential
 
 
 
 
 
 
 
248
 
 
 
 
 
 
 
 
 
 
 
socialization in the development of sex-typed abilities is difficult to evaluate.
 
Males and females show similar rates of early babbling (Moss, 1967; Lewis,
 
1972), but by six months of age girls receive more physical, visual and vocal
 
contact with their mothers (Goldberg and Lewis, 1969; Messer and Lewis, 1972).
 
Infant boys are encouraged more than girls to explore and to be independent of
 
their mothers (Baumrind and Black, 1967; Hoffman, 1972). McGuinness (1976)
 
argues convincingly that sex differences in cognitive abilities may develop from
 
fundamental differences in auditory and visual acuity—from an early age
 
females show lower auditory thresholds and superior pitch discrimination
 
compared to males, and the sex difference increases with higher frequencies and
 
with age (McGuinness, 1972); males have superior foveal vision, greater sensitivity to light and longer photopic persistence.
 
 
 
The aspect of spatial ability in which males most consistently excel is the
 
capacity to rotate mentally three-dimensional images, or to redefine visual
 
images into new planes; males thus perform better on mathematical problems
 
which require spatial visualization (Fennema and Sherman, 1977; Petersen,
 
1979) and which involve the ability to ‘break set’ and restructure (Garai and
 
Scheinfeld, 1968; Hutt, 1972a, b). Until adolescence, the majority of studies show
 
no sex differences in quantitative skills, but males move ahead after this point
 
and show consistently superior performance (Maccoby and Jacklin, 1974).
 
 
 
If these sex differences in cognitive abilities are subserved by the neural
 
organizing effects of androgens in utero, a sample of females exposed prenatally
 
to androgen would be expected to show a male pattern of abilities. Similarly, if
 
enhanced oestrogen levels affect the neural substrates of verbal behaviour then
 
males exposed to supplemental oestrogen in utero would show a female pattern
 
of abilities. In fact, neither of these hypotheses is substantiated by the available
 
data.
 
 
 
Ehrhardt and Money (1967) report identical mean verbal and performance IQ
 
scores for a PIH sample of ten females (mean verbal IQ = 125, s.d. = 11.4; mean
 
performance IQ = 125, s.d. = 12.5). Although Perlman (1971) (cited in Reinisch
 
et al., 1979, and in Baker and Ehrhardt, 1974) found that CAH girls performed
 
significantly lower than their matched controls on Verbal and Comprehension
 
sub-tests of the Wechsler IQ scale, they also scored lower on Block Design.
 
However, the scores of CAH girls on the Healy Pictorial Completion Test were
 
comparable to those of CAH and normal boys; Perlman suggests that this result
 
may reflect the higher activity levels of the CAH girls which would have made
 
them more familiar with the kinds of situations depicted on the test. Baker and
 
Ehrhardt (1974) report no statistically significant difference on perceptual or
 
verbal factors between AGS patients and sibling control comparisons, although
 
the trends were in the expected direction (i.e. CAH females performed slightly
 
less well on the verbal sub-tests of the WISC than their unaffected female
 
siblings, but slightly better on the perceptual sub-tests).
 
 
 
 
 
 
 
SEX DIFFERENCES IN BRAIN DEVELOPMENT
 
 
 
 
 
249
 
 
 
 
 
Curiously, patients exposed to prenatal androgen do seem to have above
 
average IQ scores, but close examination of the relevant data reveal this finding
 
to be due to factors other than the androgenic influence. Baker and Ehrhardt
 
(1974) tentatively suggest that the recessive genetic trait for CAH may somehow
 
be linked to another trait which favours postnatal intellectual development, and
 
this notion is supported by the finding that the IQ levels of CAH patients do not
 
differ significantly from those of their parents and siblings which are also higher
 
than normal. The elevated IQ of the PIH group (Ehrhardt and Money, 1967)
 
can be ascribed to social class factors among the parents: six of the nine families
 
involved in this study had at least one parent who was a college graduate. Thus,
 
there is no substantial evidence to link prenatal androgens with enhanced IQ
 
scores.
 
 
 
Dalton (1968, 1976) suggested that prenatal progesterone (not of the
 
androgenic type) increased intellectual achievement, but these data were not
 
replicated in a study reported by Reinisch and Karow (1977) and have been
 
discredited on statistical and theoretical grounds (Lynch et al ., 1978; Lynch and
 
Mychalkiw, 1978).
 
 
 
The only study to consider the effects of prenatal oestrogen on cognitive
 
ability is that of Yalom et al. (1973). These (male) subjects were administered the
 
Embedded Figures Test to evaluate their spatial ability: those boys who had
 
been exposed to supplemental oestrogen in utero showed slightly inferior
 
performance relative to the two comparison groups, but this result did not reach
 
statistical significance.
 
 
 
Other hormonally anomalous clinical conditions in no way implicate the role
 
of prenatal hormones in determining the future patterns of intellectual abilities.
 
Patients with testicular feminization show the typical female pattern of lower
 
spatial than verbal ability: in the study reported by Masica et al. (1969) a sample
 
of fifteen cases had a mean Wechsler verbal score of 111.8 and a mean
 
performance score of 102.3. Since their exposure both to hormones and
 
socialization is equivalent to that of genetic females, one can conclude from these
 
data simply that superior male visuo-spatial abilities are not genetically
 
determined from a locus on the Y chromosomes. For some time it was thought
 
that spatial ability was partly determined by a locus on an X-linked gene
 
(O’Connor, 1943; Stafford, 1961), but recent data indicate that the pattern of
 
spatial abilities within familial groups is better explained by a model of an
 
autosomal dominant gene which has reduced penetrance in females (Fain, 1976,
 
cited in Vandenberg and Kuse, 1979). Whether this mechanism might influence
 
brain differentiation must be purely speculative, and there is, as yet, no evidence
 
to this effect.
 
 
 
Turner’s syndrome females have IQ scores within the normal range (Money,
 
1964; Shaffer, 1962), but also tend to show specific deficiencies in spatial ability.
 
Shaffer (1962) quotes a mean verbal IQ of 106, but a mean performance IQ of 88.
 
 
 
 
 
 
 
250
 
 
 
 
 
 
 
 
 
 
 
Alexander, Ehrhardt and Money (1966) showed that Turner’s syndrome females
 
experienced great difficulty on a visual memory test which requires the
 
reproduction of angulated shapes, and Theilgaard (1972) reported that they
 
performed badly on an embedded figures task.
 
 
 
It is reasonable to speculate from these data that androgens play some role in
 
facilitating spatial ability. Since Turner’s syndrome females produce no
 
androgens, and testicular feminized patients are insensitive to their effects,
 
spatial ability is thus slightly impaired. In the oestrogen-exposed patients, the
 
testes may have been producing less androgen than normal (Zondek and
 
Zondek, 1974). The data from the CAH patients indicate that it is not the
 
prenatal hormonal environment which is crucial, so the effect of androgens on
 
spatial ability appears to be activational rather than organizing. This conclusion
 
is supported by data from Petersen (1979) which indicate that females with
 
androgynous somatic characteristics have better spatial ability than their more
 
‘feminine’ peers.
 
 
 
Similarly, the effect of oestrogens on verbal ability may also be an activational
 
one. Dawson (1972) reports a study of West African males feminized by
 
kwashiorkor-induced endocrine dysfunction. In severe cases of kwashiorkor the
 
liver becomes unable to inactivate the normal amount of oestrogen which the
 
male produces, and Dawson found that males with this condition had
 
‘significantly lower spatial ability and a more feminine field-dependent cognitive
 
style than controls. In addition these subjects had significantly lower numerical
 
and higher verbal ability compared to normal males’ (p. 24). Presumably
 
though, these males had had equivalent gestational experiences to their
 
controls and so the prenatal hormonal environment is not implicated in these
 
results.
 
 
 
 
 
Sex differences in postnatal brain development
 
 
 
The human brain is not fully mature until around sixteen years of age. The main
 
‘growth spurt’ of the human brain begins during the last trimester of pregnancy
 
and continues into the second year of life. During this period there is an increase
 
in the number of glial cells (from which myelin is derived) and hypertrophy of all
 
cells, specifically in the form of increased axonal terminal and dendritic
 
branching (i.e. interneuronal connections). Most cortical areas are fully
 
myelinated by the child’s third year but myelination of the reticular formation
 
the cerebral commissure, and the intracortical association areas may continue
 
into the second and third decades of life (Marshall, 1968).
 
 
 
Recent evidence suggests that sex differences in brain development are partly
 
reflected in sex differences in hemispheric specialization (Hutt, 1979a; McGlone,
 
1980). For example, Witelson and Pallie (1973) in a study of infants up to 3
 
months old, reported that the increased size of the left (relative to the right)
 
 
 
 
 
 
 
SEX DIFFERENCES IN BRAIN DEVELOPMENT
 
 
 
 
 
251
 
 
 
 
 
temporal planum (the posterior surface of the temporal lobe, including part of
 
Wernicke’s area which subserves language) was significant in neonate females
 
but not in males (although a significant difference was found for slightly older
 
(20-90 days) males). Buffery and Gray (1972) cite evidence that in four-year-old
 
girls the degree of myelination in the temporal planum is greater than that for
 
four-year-old boys and they suggest that this may account for the female
 
precocity in language development.
 
 
 
Witelson (1976) describes an experiment which suggests that in boys, the right
 
hemisphere is specialized for spatial processing from as early as six years of age,
 
whereas females show evidence of bilateral representation. She suggested that
 
this specialization might subserve superior spatial skills in males. Levy (1969)
 
postulated that bilateral representation of language in females could interfere
 
with the development of spatial processing abilities in the right hemisphere—
 
thus the cerebral organization which is presumed to give females an advantage
 
in language development and verbal abilities may serve also to impede their
 
development of spatial skills.
 
 
 
Waber (1976) has argued that lateralization is a function of maturation rate
 
rather than sex. On the whole, girls mature faster than boys and generally
 
display a greater tendency towards bilateral representation of skills. However,
 
late-maturing adolescents of either sex are more likely to be strongly lateralized
 
than their early-maturing peers, and are also more likely to show evidence of
 
superior spatial skills.
 
 
 
The evidence for the existence of anatomical substrates which would underlie
 
lateralization processes is both limited and confusing. For example, Wada et al
 
(1975) did not replicate Witelson and Pallie’s (1973) findings on sex differences
 
in cerebral asymmetry in infants: they report that both male and female infants
 
tend to have a larger temporal planum in the left hemisphere than in the right,
 
yet adult females are more likely than males to show the reverse pattern of
 
asymmetry. It is possible that the anatomical asymmetry reported for adult
 
females is a reflection of the greater plasticity of localization of function in
 
females than in males. In a recent report (Hughes et al , 1980), females performed
 
faster on a task which had both a verbal and a visuo-spatial component, whereas
 
both sexes performed at the same speed on the verbal task alone. The authors
 
interpret this finding as reflecting the ability of females to process both aspects of
 
the task in one hemisphere; in males additional time is needed to complete the
 
combined task because information has to be transferred between hemispheres.
 
However, this sort of speculation awaits support or rebuttal from further
 
anatomical evidence.
 
 
 
The ontogeny of hemispheric specialization and lateralization is simply not
 
yet adequately charted. It is not known whether (or how) the environment might
 
modify lateralization and thus we cannot know whether the data of Wada et al.
 
(1975) from adult females are the result of endogenous, hormonally-mediated,
 
 
 
 
 
 
 
 
 
252
 
 
 
 
 
 
 
 
 
 
 
changes or a reflection of educational experience. Tomlinson-Keasey and Kelly
 
(1979) report that lack of early hemispheric specialization is predictive of better
 
reading skills, and that right hemisphere specialization is positively associated
 
with mathematical skills —data which confirm stereotypic achievements (i.e.
 
females tend to be less lateralized and are better readers, males show a greater
 
tendency towards lateralization of spatial skills in the right hemisphere and are
 
better at mathematics). However, the nature of these relationships needs to be
 
carefully explored.
 
 
 
Witelson (1977) argues that the functional neural substrates for the lateralization of particular abilities may show a plasticity during development which is
 
lost in adulthood, and that this plasticity may reflect a susceptibility to
 
environmental influences. However, experimental support for such an idea is still
 
thin. It may be that lateralization predisposes cognitive strategies and atten-
 
tional biases rather than specific skills. The female precocity in language
 
development leads to a preferential use of language as a processing mode and
 
consequent inferior performance in visuo-spatial skills (McGlone and Kertesz,
 
1973). Bryden (1979) offers a review of experimental data which serve as a useful
 
reminder that sex differences in cerebral organization are not clearly defined: the
 
degree of overlap between the sexes is often substantial, and seems to vary as a
 
function of the experimental paradigm.
 
 
 
 
 
How different are sex differences?
 
 
 
It is easy to fall into the habit of discussing sex differences in ability and
 
behaviour as though these represented absolute differences between two quite
 
distinct populations. A sex difference in mean scores on a particular ability tends
 
to deflect our attention from the within-group variances which indicate how
 
much the groups overlap. Even when there is a statistically significant difference
 
between the mean scores of males and females on a test the majority of both
 
sexes may score within the same range.
 
 
 
The interpretation of a report of sex differences will depend on whether one is
 
concerned with socio-political/practical issues (in which case differences are
 
often trivial and meaningless) or with scientific/theoretic issues (in which case
 
small but consistent differences may yield important insights). Thus, consistent
 
reports of sex differences in verbal and visuo-spatial skills have raised interesting
 
hypotheses both about hemispheric specialization, and the role of prenatal
 
hormones; they do not, of course, provide any justification for boys to do badly
 
when studying modern languages or for girls to abandon mathematics education
 
at the earliest possible opportunity.
 
 
 
It may be that sex differences in certain skills are a result of long-term
 
evolutionary pressures. For example, Hutt (1972 b) argued that athletic and
 
visuo-spatial skills in males maximize hunting success and thus increase the
 
 
 
 
 
 
 
SEX DIFFERENCES IN BRAIN DEVELOPMENT
 
 
 
 
 
253
 
 
 
 
 
probability of survival, whereas the socially communicative abilities and
 
superior manual dexterity of the females have evolved as an adaptive consequence of her predominantly nurturant role in caring for dependent infants.
 
Yet characteristics with a presumed evolutionary adaptive basis are not fixed for
 
every individual: cultural pressures will influence the expression of abilities, and
 
‘typical’ sex differences are simply not found in some cultures. For example,
 
cross-cultural studies of field-independence (presumed to be related to visuo-
 
spatial skills) reveal no sex differences in Eskimo and Zambian cultures
 
(MacArthur, 1967; Siann, 1972). McGuinness (1976) argues that \ .. the fact that
 
boys do learn to read and write fluently, suggests that though initial processes
 
may be guided by certain sensory differences, there is no reason to assume that
 
these differences must remain. Parents insist that boys learn to speak, read and
 
write but no such insistence induces the females to learn about spatial-
 
mechanical relationships’ (p. 144).
 
 
 
In our own culture then, there is an attempt to educate males in heterotypical
 
skills whereas the converse is not true for females. Even in homes where parents
 
believe that they do not discriminate between male and female children
 
Rheingold and Cook (1975) found that \ .. the rooms of boys contained more
 
animal furnishings, more educational art materials, more spatio-temporal toys,
 
more sports equipment and more toy animals. The rooms of girls contained
 
more dolls, more floral furnishings, and more “ruffles’” (p. 461). The agents of
 
socialization are evidently insidious, and may tend to exaggerate sex differences
 
in proclivities for particular forms of behaviour. Even if we accept that
 
evolutionary pressures have resulted in sex differences in neural organization
 
which may differentially predispose males and females to specific abilities, we
 
must stand this against our knowledge that the plasticity of the human brain will
 
probably enable us to modify the expression of those abilities. This in turn
 
implies a responsibility of educators and caretakers to provide an appropriate
 
range of educational opportunities and role exemplars for their male and female
 
charges.
 
 
 
At present, not only are females less likely to be given the wide range of toys
 
that males have, their role is also under-represented by the literature and
 
television media: \ .. females were under-represented in the titles, central roles,
 
pictures, and stories of every sample of books we examined ... Even when
 
women can be found in books, they often play insignificant roles, remaining both
 
inconspicuous and nameless’ (Weitzman et al ., 1972). Sternglanz and Serbin
 
(1974) made a study of T.Y. programmes with high popularity ratings, and
 
found that half of these programmes did not portray any female roles: of those
 
that did, the authors comment ‘female children are taught that almost the only
 
way to be a successful human being if you are a female is through the use of
 
magic’ (p. 714). Exposed to these kinds of socialization pressures it comes as little
 
surprise that females tend to be diffident about their own ability and are
 
 
 
 
 
 
 
254
 
 
 
 
 
 
 
 
 
 
 
particularly unwilling to tackle those skills which they perceive as falling within
 
the male domain (Hutt, 1979b; Byrne, 1978).
 
 
 
Socialization experiences in our culture thus tend to exaggerate a dichotomy
 
of roles and abilities between males and females. Historically, this socialization
 
has acted to repress the female more than the male (her rights to be educated and
 
to vote have, after all, been won only comparatively recently), but there is little
 
doubt that a deliberate educational policy could serve to increase the range of
 
both male and female behaviour. Goy and McEwen (1980, pp. 60-61) present
 
some interesting evidence that female attachment to an infant may be innate (its
 
expression being in part activated by elevated hormonal levels during pregnancy
 
and birth), whereas male attachment is socially learned. This in no way implies
 
that males are unable adequately to perform parenting behaviours, but its
 
expression may be subserved by different neural mechanisms. There is no reason
 
to believe that the expression of sex typical intellectual abilities is any less
 
modifiable.
 
 
 
 
 
Towards a model of human sex differences
 
 
 
Waddington’s (1957) notion of‘canalization’ in an epigenetic landscape provides
 
a useful conceptualization for understanding differences in the degree of sexual
 
dimorphism in behaviour. Waddington suggested that, for all members of a
 
species, a set of target physical characteristics (eyes, arms, legs etc.) is defined by
 
the genotype and, despite underlying genetic variability, genetic processes
 
operate together to ensure that these targets are achieved. He depicts the
 
development pathways of the phenotype as a ball rolling through a set of valleys
 
(the epigenetic landscape); the valleys can vary in steepness and thus vary the
 
opportunity of the phenotype to deviate from a given course—-the steepness of
 
the valley reflects the degree of canalization. At certain critical points in
 
development, when the phenotype is undergoing rapid change, it is susceptible
 
to certain environmental or genetically induced stresses. For example, the
 
embryological development of the arms takes place around 38-48 days
 
(postmenstrual); this development is strongly canalized (i.e. all normal humans
 
have arms) but a teratogen, such as thalidomide, taken by the mother during this
 
critical period will inhibit this normal phenotypic development and the foetus
 
will eventually be born either with no arms at all or severe under-development
 
(see Fishbein, 1976, pp. 46-47). The development of some other physical
 
characteristics may also be affected by thalidomide during this period, but in
 
general each character has its own critical period.
 
 
 
As we noted earlier, the basic developmental trend of the body’s sexual
 
characteristics is in a direction corresponding to that of the homozygous sex (i.e.
 
the female). This trend is canalized to develop a female foetus from the zygote
 
which is formed at conception. However, if the embryonic gonad differentiates to
 
 
 
 
 
 
 
SEX DIFFERENCES IN BRAIN DEVELOPMENT
 
 
 
 
 
255
 
 
 
 
 
form a testis, then phenotypic development is deflected from the female pathway
 
when the testis begins to secrete MIS and androgens. Differentiation of neural
 
networks occurs in the same manner: there will be critical periods when the
 
presence or absence of biochemical agents (usually hormones) will affect the
 
development of RNA which is specific to particular structures. Behaviours which
 
depend on these specific neural anlagen for their expression will subsequently be
 
affected. The specificity of hormonal effects is well illustrated by some data
 
presented by Short (1979): certain aspects of male-type sexual behaviour were
 
exhibited by ewes which were androgenized late during gestation (days 50-100,
 
or 70-120) and had essentially female external genitalia; androgenization during
 
early gestation (days 30-80) resulted in complete masculinization of the external
 
genitalia which was not accompanied by male type sexual behaviour. Masculinization of urination behaviour could be effected by androgenization at a
 
relatively late period of gestation after it was no longer possible to masculinize
 
sexual behaviour. The positive feedback effect of oestrogen on LH, which is
 
normally exhibited only as a female characteristic, was sometimes abolished by
 
androgenization but ‘gave no clue whatsoever to the type of sexual behaviour to
 
expect from the animal’ (p. 258). This example illustrates clearly that the degree
 
of masculinization of behaviour cannot be inferred from physical characteristics.
 
The developmental pathways for specific behaviour patterns are also
 
independent of one another, so the masculinization of sexual behaviour does not
 
necessarily imply masculinization of activity levels.
 
 
 
If we return to the image of males and females rolling through their
 
(sometimes overlapping) epigenetic landscapes, it is possible to visualize the way
 
in which different levels of canalization will result in different degrees of sexual
 
dimorphism in the eventual expression of behaviour. If the pathway for a
 
particular neural substrate is very steep, it will be difficult to deflect the
 
phenotype from its developmental path—thus most genetic females will manifest
 
the appropriate ‘female’ behaviour pattern and most males will not. If the
 
pathways are gentle then the phenotypes may be spread more thinly, and a linear
 
male-female dimension may be evident in the subsequent behavioural pattern.
 
The neural mechanism which mediates gonadotropin release is clearly strongly
 
canalized, other neural substrates in humans are less strongly canalized and
 
therefore enable the expression of greater variability in behaviour and skills.
 
 
 
The critical periods for development of the neural networks which underlie
 
particular behaviours may vary in length; they may overlap in time, but they are
 
independent of one another. Thus, in the female rat, by the judicious administration of neonatal testosterone, it is possible to decrease the incidence of lordosis
 
but not to increase the incidence of mounting. Armstrong’s attempt (cited in
 
Jost, 1974) to relate sexual orientation to body type is therefore quite
 
misconceived: there is no reason to believe the homosexuals will have heterotypical body characteristics.
 
 
 
 
 
 
 
256
 
 
 
 
 
 
 
 
 
 
 
There are three ways in which hormones can act on the brain to produce sex-
 
differentiated effects. The prenatal hormones organize neural networks in
 
distinctively male and female patterns; they also have a critical role in the
 
development of physical characteristics. Postnatally, the output of gonadotropic
 
hormones can activate these neural networks (for example, in the control of the
 
menstrual cycle). Alternatively, sex-related hormones may have independent
 
effects: an example of this is the yawning behaviour of rhesus monkeys which is
 
normally displayed more frequently by males than by females, but which can be
 
increased in the female by the administration of exogenous testosterone (Goy
 
and McEwen, 1980).
 
 
 
In humans, evolution has operated to permit a high degree of behavioural
 
phenotypic plasticity, which would in turn imply weak canalization of the neural
 
mechanisms which subserve particular behaviours and abilities. (This may
 
account for the conflicting findings in anatomical studies of hemispheric
 
asymmetry, supra). This phenotypic plasticity enables individuals with very
 
different genotypes to exhibit similar or identical behaviour. In the expression of
 
human behaviour and ability then, phenotypic plasticity and not biological
 
canalization may produce conformity of behaviour within a same-sex group.
 
Evidence for sexually differentiated canalization of a particular behaviour
 
requires that its manifestation be virtually universal and not restricted to a single
 
cultural group: the only behaviours which fulfil this stringent requirement are
 
indeed ‘menstruation, gestation and lactation’ in females and ‘impregnation’ by
 
males. The weaker canalization of sex-related brain differentiation in humans
 
relative to infra-human species would also lead us to expect less sexual
 
dimorphism of behaviour in humans; this should always be borne in mind when
 
extrapolating from animal to human studies. Rodent studies have been crucial in
 
extending our knowledge of brain differentiation—they do not necessarily tell us
 
much about human behaviour.
 
 
 
The identification of the brain areas and mechanisms which subserve
 
particular behaviours or the articulation of specific cognitive skills in humans is
 
by no means straightforward. Whilst it has been possible in infra-human species
 
to identify the critical period of development for the expression of certain
 
behaviours (vide Short, 1979) this has not been possible in humans and probably
 
(for ethical reasons) never will be. Nor is it entirely clear how circulating
 
hormones affect human behaviour: studies of the menstrual cycle produce
 
conflicting evidence (Hutt et al ., 1980), and studies of sexual behaviour (e.g.
 
Bancroft and Stakkebaek, 1979) or cognitive ability (Peterson, 1979) have not
 
yielded definitive conclusions. We also lack evidence on the way in which
 
educational experience affects brain development. Thus, information which is
 
vital to a definitive model of the effects of brain differentiation on psychological
 
sex differences is not available. Nonetheless, the existing evidence leaves no
 
doubt that brains of males and females differ as a function both of the prenatal
 
 
 
 
 
 
 
SEX DIFFERENCES IN BRAIN DEVELOPMENT
 
 
 
 
 
257
 
 
 
 
 
environment and subsequent maturational effects. These differences may well
 
underlie the predilection for males and females to act in particular ways, but
 
they cannot be seen as constituting a biological imperative.
 
 
 
 
 
Summary
 
 
 
De facto sex differences in ability and behaviour are not as dimorphic as sex
 
differences in physical characteristics. The major influences on sex differential
 
brain development are the sex steroids (androgens, oestrogens and progestins),
 
but their effect on behaviour is attenuated by the weak canalization of the
 
human behavioural repertoire. Sexual differentiation of the brain may create
 
predilections for particular behaviour and specific cognitive strategies, but it
 
does not constitute a biological imperative for psychological sex differences.
 
 
 
 
 
Acknowledgements
 
 
 
I would like to thank Dr. J. E. Blundell and Professor J. Scott for their helpful comment and criticism
 
during the preparation of this manuscript. I am also grateful to Derrick Pritchatt who translated the
 
article by Reznikov (1978).
 
 
 
 
 
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Brain and Behavioural Development - 1982: 1 Neural Development | 2 Comparative Neural | 3 Malnutrition | 4 Hormones and Growth Factors | 5 Cortical Activity | 6 Functional Asymmetry | 7 Plasticity | 8 Sex Differences

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Chapter Seven - Determinate and Plastic Principles in Neuropsychological Development

Denis M. Parker


Introduction

To those interested in the relationship between brain mechanisms and behaviour, study of the outcome of damage to the central nervous system currently provides the most useful information concerning the structural basis of cognition and action. Observation of the pattern of behavioural loss and the extent to which recovery is possible following specific brain injury enables differing models of brain organization to be specifically tested. In fact, this question of the pattern of loss and the extent of recovery lies at the heart of a controversy, between the advocates of functional localization and those who proposed a diffuse physical basis for cognitive functions, which began during the nineteenth century. Some investigators stressed the return of almost complete function following a transient period of loss (Flourens, 1824), or stressed the re- emergence of functions at a reduced level while denying that behavioural effects contingent on the damage were specifically related to the region destroyed (Goltz, 1892). These views were amplified during the present century by the experimental work of Lashley (1929) who argued that, excluding the primary sensory and motor areas of the cortex, the association areas contributed in a unified way to the performance of any complex skill—the well-known principle of Mass Action. The degree of functional loss that could be detected following brain damage was assumed to be determined by the extent, rather than the location, of damaged tissue. The results of Lashley’s experiments, together with his theoretical exposition of them, supported the views of Goldstein (1939) who regarded cognitive skills as a function of the entire organism. He saw the symptoms following brain damage as manifestations of a complex adaptive syndrome in which higher intellectual abilities, in particular the ability to abstract, were likely to be depressed. This general intellectual loss was likely to be seen in the patients’ failure on a variety of cognitive tasks, but particularly in linguistic skills since these demanded, more than other capabilities, the integrity of the entire brain. Holding views such as these, there was no problem in accounting for the return of functions after cerebral injury since the intact areas of the brain would continue to function in their usual way following an initial period of shock, although there would of course be a loss of efficiency. Factors such as the age of the subject at the time of injury were seen to play a part, and indeed one of Lashley’s students (Tsang, 1937) had provided evidence that proportionately equivalent lesions in adult and juvenile rats produced less impairment in the younger animals.

In contrast to models of the brain based on assumptions of global processing and diffuse representation, from the middle nineteenth century onwards evidence began to accumulate rapidly that restricted brain lesions often produced highly specific disorders in which the patients’ remaining spectrum of skills were relatively unaffected. Broca (1861) produced two cases in which the patients’ verbal expression was drastically impaired but whose comprehension of language appeared to be relatively good. Wernicke (1874) produced evidence that patients’ ability to comprehend and utter meaningful linguistic statements could be grossly impaired yet their pronunciation and rate of verbal output could remain unimpaired. Other descriptions followed of patients with restricted and often bizarre symptom complexes. Dejerine’s description (1892) of Mr. C is perhaps one of the classic cases. This patient, who had right visual field blindness, could nevertheless recognize objects and continue his everyday life. Despite apparently normal vision in his left visual field and the ability to speak and write normally, he was unable to read by sight even the sentences he had written himself a short while before. He was however able to ‘read’ by feeling the shapes of cut out letters. Other syndromes described included those of disordered motor planning (Leipmann, 1908), the inability to recognize objects (Lissauer, 1890), and the inability to recognize melody (Henschen, 1926). The list could be continued, but the importance of these cases was that they convinced a substantial number of investigators that the brain could not be organized in a diffuse equipotential manner but, on the contrary, must contain relatively specialized processors even for such uniquely human processes as the comprehension and generation of language.

Modern neuropsychology has moved away from the exclusive study of such rare and extraordinary cases to the systematic examination of groups of patients in which the behavioural effects of differences in known cerebral pathology can be investigated. The more extreme forms of cerebral localization have been rejected, but the acceptance of specialized processing within and between the two hemispheres of the brain has gained wide acceptance (see Walsh, 1978, and Hecaen and Albert, 1978). This current position regarding the distribution of functional systems within and between the cerebral hemispheres in the adult’s central nervous system is of considerable importance to those interested in neuropsychological development. The relative paucity of information concerning the specific effects of brain damage during development necessitates the use of the effects of adult brain damage as a yardstick against which the outcome of early brain damage may be set. By contrasting the effects of early brain injury with those which occur following damage to the mature brain, it may be possible to ascertain whether the organizational pattern typical of the adult brain is present also in early development or whether it emerges gradually.

It may seem odd that this question should be asked at all, given the fact that, superficially at least, the anatomical structure of the brain is broadly similar in the neonate and the adult, even to the extent of the presence of the adult pattern of anatomical asymmetry (Wada et al, 1975). However, evidence has been presented from time to time which argues that certain crucial functional differences are present. Animal studies have indicated that effects of motor cortex damage in infancy are less deleterious than equivalent damage at maturity since the younger animals escape the flaccid paralysis and spasticity of their elders and retain their postural and locomotor capabilities (Kennard, 1940). Even in humans the claim has been made that children may escape some of the effects of cerebellar injury suffered by adults (Geschwind, 1972). In the area of language it has been known for some time that children who become aphasic following massive left hemisphere injury usually recover speech rapidly (Guttman, 1942), a phenomenon which is not unknown but is certainly rare in the adult (Dejerine and Andre-Thomas, 1912). In such cases it is possible to resort to concepts like plasticity in order to explain the greater resilience of the immature brain, but in some cases the reorganization following injury appears to be so expeditious that it is difficult to believe that other areas of the brain not previously involved have acquired behavioural functions so rapidly (Kennard, 1940; Geschwind, 1972). Even if the idea of greater neural plasticity is accepted, the question may still be asked as to how great this capacity for compensation is? When children become aphasic following unilateral brain damage and language eventually resides in the contralateral hemisphere, does it cope as adequately as the damaged hemisphere would have done? The existence of greater plasticity in the developing brain does not necessarily mean that disparate structures are functionally equivalent. This inference would be valid only if different structures were shown to attain the same degree of functional sophistication.

These two issues concerning the establishment of the adult pattern of neural organization and the extent to which it can be modified following early brain damage will be explored in the following pages.


The context within which damage occurs during development

It is clear, that, as a child grows from birth, the various indices of maturation (behavioural, neurophysiological and morphological) tend to move together towards levels accepted as indicating greater maturity. The range and complexity of spatial, linguistic and social skills increases. In association with them electrophysiological measures of brain activity move from showing a slow and irregular pattern at birth to faster rhythms and widening of the bandwidth characteristics with increasing age. Neuroanatomical changes are also evident both at a gross level, where changes in surface area and the fissural pattern of the brain are seen (Turner, 1948, 1950), and at the microscopic level, where the size of neurones and the complexity of the dendritic pattern increases (Marshall, 1968). When investigators are concerned exclusively with behavioural development, electrophysiological and anatomical factors may provide an interesting but non-essential background. However, where one is concerned with the outcome of brain injury, which occurs early rather than late in the developmental sequence, then the broad neurobiological context in which the injury occurs assumes increasing prominence. A child who suffers brain injury has not just lived for a shorter time, and consequently experienced less, than an adult. The injury has occurred within a system which has a complex and uncompleted developmental plan which is rapidly unfolding, rather than as in the adult where injury occurs within a system where the developmental sequence may have reached a plateau of several decades’ duration. With this in mind some relevant data which outline the changing status of cerebral structures during development will be examined.


Electrophysiological and neuroanatomical maturation

Electrophysiological measures of cerebral development in man indicate a progressive increase in mean frequency content of the EEG from birth to maturity. Whilst in the neonate this is characterized by a labile pattern with periods of almost total electrical silence and an unclearly differentiated sleep pattern, the adult shows a pattern of continuous activity with a frequency spectrum that is at least superficially related to the subject’s state of alertness and with a well-differentiated pattern during the various stages of sleep (see Marshall, 1968, and Milner, 1976, for reviews, and Thompson, this volume). The adult pattern, with the occipital alpha frequency centred in the region of 10 Hz, and the presence of clear beta activity (14-30 Hz) during arousal, is attained only gradually (Henry, 1944). The most typical frequency band shifts from the delta region (1-3 Hz) at age 1 year and below, through the theta band (4-7 Hz) between 2 and 5 years, to the alpha band (8-13 Hz) between 6 years and adulthood. Beta frequencies become increasingly common in late childhood, and are an increasingly common feature of the adult EEG. Measurement of evoked potentials reveals that peak latencies are long in infancy and decrease as maturation proceeds, whilst in general, amplitude tends to decline after an initial rise. This amplitude trend is also characteristic of the development of the gross EEG (Shagass, 1972). Whilst the behavioural significance of the EEG in man is currently an extremely active research area, the status of the research findings is not always unequivocal. The existence during infancy and childhood of a differential density of waveforms in the left and right hemispheres (Walter, 1950) and the presence of lateral differences in auditory evoked potentials (Molfese, 1977) cannot be taken as evidence of functional asymmetry within the cortex at these ages, since they may indicate changes in the thalamus and corpus striatum, which are simply mirrored in an as yet incompletely differentiated and immature cerebral mantle. The EEG data do, however, allow us to see the gradual emergence of intracerebral rhythms whose mean cycle time becomes shorter with age, and whose responsiveness to external stimulation becomes crisper. Furthermore, this developmental trend continues throughout the period from birth to sexual maturity and may actually show reversal in old age (Shagass, 1972).

The impression of a long-term developmental cycle which emerges from examination of human electrophysiological development perhaps finds even stronger support when neuroanatomical development is examined. It is apparent that although the full complement of neurones is probably present in the central nervous system at birth, the brain continues to grow in overall size and the characteristic sulcal and gyral pattern of the adult emerges gradually over the first 6 years, and perhaps even later in the case of the frontal lobe (Turner, 1948, 1950). When the internal differentiation of the brain is considered a complex and protracted pattern of development unfolds (Yakovlev and Lecours, 1967; Lecours, 1975). Using the density of myelin, the lipid sheath surrounding the axons of neurones, as a criterion of maturation these workers have mapped the development of CNS pathways and structures and used the termination of the myelogenetic cycle as an index of when the system reaches final functional maturity.

It is apparent from this research that brain development does not proceed uniformly in all central nervous subsystems. Sensory fibre tracts and associated nuclei myelinate before the cortical intra- and interhemispheric communication systems. Different sensory systems however may show a diversity of time courses. The optic radiations subserving the visual cortex show a short cycle of myelination closely following the myelination of the optic tract, and is virtually complete by 4 months of age. The acoustic radiation subserving the auditory cortex does not show complete development until the 4th year, in marked contrast to the prethalamic auditory system, which is mature by the 4th postnatal month. The intracortical and interhemispheric association fibres, which allow communication between different regions and whose disruption leads to many of the bizarre neuropsychological disconnection syndromes (Geschwind, 1965), have prolonged maturational cycles extending into the second decade of life. Examination of the cortex itself indicates that some regions implicated in linguistic competence (inferior parietal lobule) show a slow onset of myelination and that this process may also continue beyond the second decade of life. It should be emphasized that although the study of the myelogenetic cycles of maturation shows a complex extended pattern of development from birth to maturity, a caveat is necessary. Neural conduction can occur in fibres before they become myelinated (Ulett et al , 1944) and indeed myelination may be aided by neural activity (Langworthy, 1933). However, myelin contributes greatly to the efficiency and speed of neural conduction, which underlies the complex analysis and planning characteristics of human cognition and action. The importance of myelin may be appreciated by considering the devastating behavioural effects of demyelination disease in man such as occurs in multiple sclerosis. The myelogenetic analysis emphasizes the manner in which the brain becomes structurally mature. Phylogenetically older structures, in general, mature earlier than those of recent phyletic origin. There are exceptions to this, for example the reticular formation, whose developmental cycle again extends into the second decade of life, partly no doubt because its final operational capability is not required until cortical systems are completely mature.

Both the electrophysiological and neuroanatomical data indicate that the human central nervous system develops over an extended period. Particularly fascinating are the observations that the higher auditory systems (geniculo- temporal pathways) exhibit a developmental cycle that is more than ten times longer than visual structures at the same level of the CNS. It is probable that this reflects the necessity of incorporating into the growing brain the species specific demand of learning the complexities of language via the acoustic mode and allows for the building of the culture-specific phoneme system which is eventually used. However, it is apparent that a considerable part of the developing child’s life is characterized by the presence of cortical structures which are functionally (by electrophysiological and anatomical criteria) immature. The status that these immature structures have in subserving the growing child’s cognitive repertoire is not straightforward. It is possible to envisage the mapping of cognitive growth within the cerebral structures which subserve cognition in the adult in at least two ways. The first view would regard all those structures which are involved in a given functional system in the adult as also being involved in infancy, although the immaturity of the system considered as a whole would limit its capabilities. The limitations seen for instance in perceptual and motor systems in the neonate would be ascribed to the immaturity of the cortical system, which was nevertheless functional, rather than to the fact that lower but morphologically more mature structures are controlling the behaviour. The alternative view would regard neurobehavioural development as a process beginning with relatively primitive analysis and response control systems residing in phylogenetically older structures which mature earlier in the developmental sequence. As development proceeds, phylogenetically newer structures, which attain maturity later in the developmental sequence, will capture and modulate the activity of the older systems as well as adding more complex control processes. This process will not have a uniform time course across all systems. In the case of the visual system this transition may occur relatively early in development at two to three months of age since the cortical network in this case has a short developmental cycle. In the case of audition the whole process may be more protracted with cortical control becoming ascendant in the period of 2-4 years, whilst in the complex action systems controlled by the frontal lobe, the processes may take even longer, given the differential growth of the region beyond 6 years of age (Turner, 1948, 1950). Evidence that it is this latter view which is the more reasonable description of neurobehavioural development comes from a number of observations that will be subsequently outlined, but it must be said in advance that the case is by no means proven.


Neuropsychological evidence concerning functional maturation

When damage occurs in the mature brain the effects are usually immediate; the degree of functional loss, whether it be sensory, motor or cognitive, is greatest immediately after the lesion and usually shows some remission over time. In the immature brain in a number of instances the pattern is almost the reverse of this. In the case of hemiplegia, sustained as a consequence of prenatal or perinatal injury, the symptoms of the disorder frequently emerge gradually over a prolonged period. Abnormalities in the use of the hand and arm may emerge at between 4 and 6 months, whilst differences in the behaviour of the legs may not become apparent until 10 months of age or more. Deficits in the use of the lower limbs may only become apparent when the child begins to walk, a milestone that is frequently attained in the normal age range (Lyon, 1961). Finally, athetoid movements do not make their appearance until much later, typically between three and four years of age (Lenneberg, 1968). Thus the developmental pattern is seen to move through a series of stages: for example, the grasp reflex is present initially in both the affected and the normal hand, but it persists on the affected side and usually the hand becomes clenched into a tight fist. Individual finger movements do not appear on the hemiplegic side, although movement of the thumbs may be possible. As the child grows, then, the deficit becomes more severe. However, it is noticeable that these children escape some of the more drastic consequences of hemiplegia resulting from cerebral injury at maturity.

The severity of paralysis in the upper limb is less and the lower limb is capable of greater use than after comparable damage in adults. That the residual function on the affected side is not attributable to surviving undamaged tissue in the diseased hemisphere is shown by the fact that removing the diseased hemisphere later in development does not cause further impairment and may frequently result in improvement (Cairns and Davidson, 1951).

Two features then are apparent in these cases. The first is the greater capacity of the young brain to compensate and escape some of the consequences of equivalent injury in adulthood—its plastic propensity. The second feature is cogently described by Lenneberg (1968): ‘one may say that the child with a perinatal cerebral injury only gradually grows into his symptoms’. This emergence of deficit with age is compatible with the view that certain systems are pre-programmed to appear at certain stages in development and injury to them will only become apparent when they fail to appear. Similar affects in the motor sphere were observed by Kennard (1940) in macaque monkeys where ablation of the motor cortex in infancy resulted in surprisingly little immediate effect, but precluded the development of fine manipulatory skills, and this, together with signs of dyskenesia, became more apparent as the animals grew older. It appears that the motor cortex only begins to exert its influence gradually and its loss or malfunction may not become apparent until a later stage of development.

Further support for the notion that behaviour early in development may be mediated exclusively by subcortical structures, with cortical processors becoming involved later, has been provided by Goldman (1976). It has been apparent for some time that tasks which require a monkey to remember the location of a stimulus over a brief interval of time are drastically affected by damage to the dorsolateral prefrontal cortex (Chow and Hutt, 1953). These are known as the delayed-response and delayed-alternation tasks. When the dorsolateral frontal cortex is removed within the first 2 months of life however, the operated animals perform as well on this task as unoperated controls as long as testing is carried out within the first year of life (Harlow et al , 1970). If these monkeys are followed into the second year of life they show evidence of increasing impairment of delayed response tasks. Lesions in subcortical structures which are functionally connected with the dorsolateral prefrontal cortex (dorsomedial nucleus of the thalamus and the head of the caudate nucleus), indicate that the monkeys operated on as juveniles show the same pattern of deficit as adults, i.e. failure on delayed alternation tasks (Goldman, 1974). These results emphasize that not only may the effects of brain damage fail to appear early in development and only reveal themselves as the animal grows, they also show that structures which are required for the adequate performance of a task in adulthood (the dorsolateral prefrontal cortex), are not necessary for the performance of the same task when the animal is an infant or a juvenile.

These experiments contribute a salutary warning to those who would assume that, because a cortical structure is implicated in a functional system in adulthood it must of necessity be involved in performance of those same functions at an earlier developmental stage. In infant and juvenile macaques subcortical systems are capable of mediating responses which in adults require the participation of the cortex. Furthermore, evidence is available which indicates that the time course over which the effects of cortical lesions become apparent during development differs for different regions. While monkeys aged 2\ months with orbital frontal cortex lesions are equivalent to unoperated controls in the performance of object reversal learning, deficits in performance became apparent by the time the animals are one year old (Goldman, 1974). Thus, while the effects of dorsolateral frontal cortex damage sustained in infancy on delayed alternation tasks do not become apparent until after one year of age, the effects of orbitofrontal damage in infancy on object reversal learning become apparent before one year of age. In the case of both delayed alternation and object reversal learning early in development subcortical structures are capable of mediating the behaviour successfully. With respect to these studies it should be pointed out that macaque monkeys attain sexual maturity between 24 and 30 months of age, so the effects of early brain damage may take a considerable proportion of the developmental cycle before they become apparent.

The evidence cited so far has argued for a model of development in which the complete maturational cycle is prolonged, but within which different systems may attain functional maturity at widely divergent times. Initially, behaviour may be controlled by subcortical systems, and depending on the time-course of the maturational cycle in the higher reaches (cortical) of each system so control will pass to the phylogenetically newer and more adaptive system. Bronson (1974) has argued, on the basis of changes in the pattern of visual behaviour in infants, that in the case of the visual system a transfer of control passes from the superior colliculus to the striate cortex, from the ‘ambient’ to the ‘focal’ system (Trevarthen, 1968), during the 2nd and 3rd postnatal month. Such a view is certainly compatible with the rapid postnatal development of the geniculo- striate system (Yakovlev and Lecours, 1967). In the case of motor function the longer maturational cycle of the medullary pyramids (up to 12 months), which carry the axons of the Betz cells of the motor cortex to the spinal cord and are required for control of individual fingers and skilled sequences (Lawrence and Hopkins, 1972), leads one to expect that transition of control in this case may take place over a more protracted period. The emergence of comparative motor deficit between affected and normal side, in cases in infantile hemiplegia, between 4 and 12 months of age (Lyon, 1961) appears to reflect this longer cycle of development. In man, however, the long-term emergence of a deficit in previously established skills after early brain injury akin to that reported by Goldman (1974, 1976) for the macaque monkey, has not as yet been reported.

Nevertheless, evidence is available which indicates that, on some perceptual tasks, brain-damaged children may show either a consistent difference from controls over a wide age range (Cobrinik, 1959), or a progressive change, which either diverges from or converges to control values between the ages of 5 and 15 years depending on the particular measure being considered (Teuber and Rudel, 1962). Thus, slowly emerging effects of early brain damage in man are not unknown, but long-term effects, with an intervening ‘silent’ interval, have not, to the present author’s knowledge, been described.


Interactive effects and their interpretation

Generalized effects on intelligence that result from presumed structural incapacity (Hebb, 1942) or following localized injury (Thompson, 1978) have indicated that while early injury may produce generalized depression of full- scale IQ, late injury produces a more specific pattern of deficit, with less depression of full-scale IQ. Research findings of this nature can be seen as support either for a model of brain development in which neural structures only gradually attain their mature state, or alternatively, as support for the view that reorganizational capacities are at work during development which allow savings on specific skills but at the cost of overall depression in intellectual attainment. However, there is no doubt that both views are valid and have independent evidence to support them. The developing brain is more vulnerable than the mature brain and this can be seen in the long term generalized deleterious consequences of nutritional deprivation during the brain-growth spurt, as measured by both neurochemical and anatomical criteria (Dobbing, 1968), and by behavioural criteria (Chase, 1973). However, it is also clear that substantial left hemisphere damage, which usually leads to long-term severe dysphasia in adulthood, results in only transitory dysphasic symptoms when the damage occurs early in childhood (Hecaen, 1976), and there is evidence of savings in visuo-spatial skills following early right hemisphere dysfunction, which is not apparent with equivalent damage at maturity (Kohn and Dennis, 1974).

These findings provide unequivocal evidence of the reorganizational and plastic capacities of the developing brain. However, it is also evident that the usual predetermined pattern of left hemisphere specialization for language and right hemisphere specialization for visuo-spatial skills set limits to this plastic capacity. Where one hemisphere has sustained early injury, the language skills exhibited by a remaining and intact right hemisphere are less proficient than those exhibited by a remaining intact left hemisphere (Dennis and Kohn, 1975). It also appears that visuospatial abilities are better developed in an intact right hemisphere than when the left hemisphere alone remains fully functional (Kohn and Dennis, 1974). Thus, while reorganization is possible following early brain injury, this may be more limited than has been previously thought. Indeed, given the anatomical asymmetry present in the neonatal brain (Wada et al, 1975) it would be surprising if this structural specialization were not detectable at some stage in the behavioural effects of unilateral brain injury. The results of unilateral brain injury in early development nicely juxtapose two major tendencies which emerge from neurobehavioural research: on the one hand, the trend towards carrying through the construction of a preprogrammed system over a protracted time period and, on the other, an adaptive plastic capacity which allows the partial redirection of functional systems should damage occur.

The complexity of the processes involved in the analysis of sensory information (Hubei and Wiesel, 1963; Werner and Whitsell, 1973) that has emerged from single neurone recording makes it clear why a great deal of preprogramming must be involved in the construction of complex adaptive neural systems. It is less easy to describe the mechanisms which allow complex brain systems to exhibit the degree of plasticity that they evidently do in early development. The explanation may reside in the fact that younger individuals are less susceptible to transneural degeneration effects and also show higher levels of biosynthetic activity in brain tissue, which may allow damaged networks greater restitutional capacity (see Goldman and Lewis, 1978, for review). It is also evident that behavioural recovery, seen after early injury in some cases, depends on the ability of young animals to profit from experience in a way not available to the adult. Monkeys sustaining brain injury in infancy show greater recovery the earlier training experience is given in development, although the ability to profit from this experience depends on the nature of the task and the site of the lesion in the brain (Goldman and Lewis, 1978). The results of this study gave some indication that it was the nonspecific stimulation effects of the training which were important in recovery, rather than specific carry-over from common features of the task.

The fact that experience per se may be an important factor in promoting recovery is of considerable importance, since there has been suspicion about the value of training programmes in the recovery from brain damage (Byers and McLean, 1962). Given the intricacy of the neurobiological factors involved in early brain injury it may be too easy to forget about the cognitive dimension. During development a child moves from a relatively primitive analysis and interaction with the external world to a stage where his conceptual structures are complex and enable sophisticated analysis and prediction of the environment. The cognitive capacities evident at maturity have been built on simpler ones gathered progressively during childhood. Thus, impairment of systems which gather and utilize information as a consequence of cerebral damage could result in diminished intellectual achievement, not through injury to critical higher-level systems, but because essential ‘feeder’ mechanisms have malfunctioned. An adult with a subcortical lesion which destroys the left auditory radiation and the callosal input from the contralateral hemisphere may show a normal audiogram but be incapable of interpreting spoken language (Gloning et al ., 1963). Nevertheless, speech, reading and writing may be normal since their associated cortical circuitry is undamaged and language has been previously established. In a child, bilateral disruption of the auditory radiations by a lesion damaging the lips of the sylvian fissures and the insulae can preclude the normal development of language, despite evidence of hearing in the normal range (Landau et al , 1960). Even children who become peripherally deaf after acquiring speech may not only show arrested language development but lose previously acquired linguistic skills (Bay, 1975). This ‘cognitive starvation’ effect, which is easy to comprehend in the instances cited, may also operate within association areas of the cortex and may underlie the tendency of early brain pathology to produce more global intellectual depression effects than are seen with lesions in adolescence and adulthood.

The data briefly reviewed in this section emphasize that the effects of brain injury in the developing nervous system are particularly complex. When injury occurs, it is within a system whose functional capacities are still unfolding, and the effects of injury are sometimes not immediately apparent. The plastic capacity of the system may also mask the extent of any physical injury and lead to a false assumption that effects have been transitory. There is also the added complication that, whilst injury may not have damaged structures critical for the attainment of certain cognitive skills, because critical ‘feeder’ systems have been impaired, these cognitive mechanisms may not have the experiental basis upon which to build.

The consequences of early brain damage

Global and specific processing

In 1942 Hebb drew attention to the different patterns seen following brain damage in both mature and immature nervous systems. Adults, he found, could be considered to be either aphasic or non-aphasic types (Hebb, 1942). The aphasic type showed obvious evidence of deterioration on verbal tasks and some also showed evidence of impairment on such non-verbal tasks as detecting absurd errors in pictures and block manipulation performance. However, some of the aphasic patients showed evidence of almost normal performance on nonverbal tasks, and Hebb remarked on the wide disparity of abilities seen on particular tests in individual aphasic patients. This conclusion of Hebb’s (that non-verbal skills may be retained to a remarkable extent in some cases of aphasia) is reinforced by more recent research on this topic (Zangwill, 1964; Kertesz and McCabe, 1975). In the non-aphasic type of brain injury on the other hand many verbal tasks could be adequately completed, but there was usually severe impairment on maze learning, block manipulation and picture absurdity tasks, as well as impairment on some verbal tasks, e.g. the defining of abstract words, or naming opposites. The two types were, however, sufficiently different for Hebb to state that following adult brain injury a reasonably specific pattern of deficit often emerges—some skills showing deterioration and others being relatively intact. In contrast, a group of children with what he termed ‘exogenous’ brain injury showed no evidence of a dual pattern, that is the ‘aphasic’ and ‘non-aphasic’ types did not occur as a consequence of early brain injury. The group as a whole showed depression of verbal IQ, but since he thought it unlikely that every case of brain injury in infancy involved damage to the language areas it must be that ‘low verbal test scores are produced by early lesions outside the speech areas’ (Hebb, 1942, p. 286). He went on to argue that the more global pattern of intellectual depression seen after early brain injury occurs as a result of the differing demands being made on the adult and the child after cerebral damage. The adult has merely to make use of skills which have already been acquired, whereas the child has still to assimilate a range of skills. Since a greater cognitive demand is made during the acquisition of a skill than by the performance of one already acquired, the growing child is at a greater loss than the adult when an equivalent amount of brain tissue has been lost in both. Hebb went further and argued—following Lashley (1929)—that some degree of equipotentiality must exist in the cortex and that areas outside the classical language areas must be involved in the development, but not the maintenance, of linguistic skills once they have been mastered.

Two major hypotheses then emerge from Hebb’s work (1942). The first is that early, rather than late, brain damage has a more global depressive effect upon intellectual development. The second hypothesis is that the developing nervous system is characterized by a greater degree of equipotentiality than that of the adult, since the attainment of normal adult performance on a range of specific skills seems to depend on the integrity of whole cerebrum. The first hypothesis has, in general, received support from subsequent research. Bryan and Brown (1957) found that there is a strong relation between the age of injury and mean IQ, so that those with an injury present at birth averaged a score of 62, those injured in infancy averaged 66 while those with injuries occurring between 3 and 10 years and between 10 and 20 years averaged 71 and 85 respectively. Thompson (1978) reported that in 282 subjects who sustained localized cerebral injury in childhood, there was a linear relationship between age of injury and full-scale IQ with those injured before 5 scoring 97 and those injured above 15 years scoring 106.5. It should be noted, however, that whilst McFie (1961a) found a rise in mean IQ between those injured in the age bands 1-4 and 5-9 years from 88.8 to 106.0, he found a fall in IQ with those sustaining injury between 10 and 15 years (82.7). However, on balance the findings would seem to support Hebb’s initial contention.

The second hypothesis emerging from Hebb’s (1942) study, that the developing nervous system is characterized by a greater degree of equipotentiality than that of the adult, is rather more contentious since it is more difficult to test than it might appear at first sight. It has already been pointed out that general depression of IQ cannot be used as evidence for a type of mass action operating during development, since it may also argue for an interdependence of separate capabilities being required for the construction of more complex schemata. It is also apparent that brain-damaged children show widely differing patterns of impairment, which would be difficult to comprehend if there were a tendency for the brain to act uniformly in the acquisition of cognitive skills (Strauss and Lehtinen, 1968). There is also the added difficulty that IQ tests may be rather insensitive to specific patterns of disability produced by brain injury, both in children (Boll and Reitan, 1972) and adults (Walsh, 1978), a factor which has resulted in the construction of specialized test batteries.

However, instead of asking whether the general depressive effect of early brain damage on IQ is due to a greater degree of global processing in the immature CNS, it might be more fruitful to consider whether a similar pattern of impairment emerges on specific skills after similar damage in the child and the adult. McFie (1961a), in an investigation of the effects of localized post-infantile cerebral lesions in children, found that there was a tendency for Wechsler verbal scores to be lower following left hemisphere injury and performance scores to be lower following damage to the right hemisphere. He also noted a similarity in the pattern of impairment shown on the Memory for Designs component of the Terman-Merrill scale (1937) between children and adults when comparing the effects of frontal, temporal and parietal injury. He reported that the greatest deficit is to be found in both groups following right parietal damage. Fedio and Mirsky (1969) examined the pattern of impairment exhibited by children with either unilateral temporal lobe or with centrencephalic epilepsy on a test battery designed to measure performance on both verbal and non-verbal tasks, and a task of sustained attention. The children, who had a history of illness dating from early school years, showed similar impairment profiles to those of adults with similar pathology. Those with left temporal epileptiform foci required a greater number of trials to learn lists of ten words and showed greater loss after a 5- minute interval than those with right temporal or centrencephalic pathology. Those with right temporal pathology showed greatest impairment on the recall of the order of random shapes and on production of the Rey-Osterrieth figure. The centrencephalic group showed the greatest deficit on a task requiring sustained attention. Annet et al (1961) also found a similar pattern of verbal and spatial difficulties in children classified on the basis of lateralized EEG abnormalities. These results would suggest that children show impairments of the same type as those found in adults with similar pathology. It may be objected however, that in these cases the damage is characteristic of juvenile rather than infant brain damage, and, if adult cortical specialization appears gradually, then patterns of specific loss will also begin to appear, producing the observed similarity to the adult type by middle childhood. However, evidence does exist which would suggest that there is hemisphere specialization, even when damage occurs perinatally or in infancy.

Damage to the left, but not the right, hemisphere before the end of the first year of life results in impairment in the rate at which combinations of words (elementary syntax), but not single words, are learned (Bishop, 1967). Furthermore, children who have had either a left or right hemisphere removed as a consequence of damage sustained during the first year of life show differential effects depending on which hemisphere is involved. Those with left hemisphere removal show greater difficulty in the comprehension of syntax than right hemi- decorticates (Dennis and Kohn, 1975). In particular, difficulties as shown by a greater number of errors are apparent in comprehension of the passive negative, e.g. ‘the girl is not pushed by the boy’, as opposed to the active affirmative, ‘the boy pushes the girl’. In these experiments comprehension was assessed by having the child choose a picture which depicted the sentence. The greater difficulty in the comprehension of passive sentences was also apparent in longer response latencies. Children with early right hemisphere damage followed by hemi- spherectomy show difficulties on spatial tasks (Kohn and Dennis, 1974). The types of spatial task on which they show relative deficit are those which continue to show improvements in normal subjects through the teens, e.g. the WISC and Porteus mazes, and map reading tasks, which require a subject either to state the direction to be taken or to follow a route through markers placed on the floor. Early maturing skills, such as tactile form matching and visual closure, were unaffected in contrast to right hemisphere injury at maturity which severely depresses these abilities. Further analyses of three cases where hemispherectomy antedated the beginnings of speech were presented by Dennis and Whitaker (1976) and two cases where hemispherectomy for unilateral pathology was carried out at ages 3 and 4 years respectively were reported by Day and Ulatowska (1979). In these cases the pattern of deficit is similar to those previously reported and supports the view that the hemispheres are differentially involved in different aspects of cognition. Specialization would appear to be an early-established characteristic of the child’s brain although its potential for reorganization complicates the issue (see p. 225).

Given that differences in the patterning of intelligence subtest scores only really become obvious during adolescence and beyond (Thompson, 1978), whereas specific deficits are detectable by specially devised tests in younger children, IQ tests appear to be insensitive instruments on which to base theories concerning brain development. One obvious factor which will lessen the sensitivity of IQ tests to brain damage early in development is the capacity to transfer the development of linguistic and spatial skills to the contralateral hemisphere should damage occur. This plastic capacity should not however be confused with ideas about mass action or equipotentiality. These latter ideas imply the existence of a type of diffuse processing network to which the association cortex within each hemisphere contributes uniformly (Lashley, 1929). The transfer of functional capability from one hemisphere to the other, however, is to be understood in a rather different context. Each cerebral hemisphere contains anatomical structures which are essentially duplicates of those found in the other, with the difference that certain cytoarchitectonic areas may be relatively larger or smaller. In some instances, particularly in the language area, these cytoarchitectonic differences in size may be as great as 700% in favour of the left hemisphere (Galaburda et al ., 1978). However, each specialized cortical area has a pattern of connections to the rest of the brain which, in essence, is a lateral reversal of those found in the other hemisphere. The ability of these ‘duplicates’ to assume some of the functional capacities previously assumed by their cytoarchitectonic counterparts is perhaps not too surprising. Indeed, the puzzling feature is that in a substantial majority of the adult population this ability is lost. The assumption that somehow the areas within each hemisphere act as a kind of equipotential unit, is not supported by the available evidence. If such a diffusely organized system were operative in the left hemisphere during development, then it would be reasonable to assume that unilateral damage, resulting in suboptimal processing capacity, would be sufficient reason to transfer linguistic processing to the remaining intact hemisphere. Milner (1973) has provided evidence, based on language lateralization, tested by the Wada (intracarotid injection of sodium amytal) technique, that only when early injury invades those areas shown to be important for linguistic processing in the adult, will language transfer to the right hemisphere. These results suggest that certain key regions, not the global processing capacity or total operational mode of one hemisphere, promote the establishment of language within that hemisphere.

In considering the question of global or specific processing in development, the evidence on balance suggests a specific processing configuration not dissimilar to that found in the adult brain. It has also been argued that one of the reasons why early brain damage often has a markedly depressive effect on intellectual growth may be that the substrate of complex cognitive processes may require the integrity of fundamental systems in order to attain their full potential. One line of evidence which supports this is the finding that right hemisphere damage, which occurs before one year of age, may have more depressive effects on cognitive growth than damage to the left hemisphere at an equivalent age, or damage to either hemisphere after one year of age (McFie, 1961 b; Woods, 1980). This greater deleterious effect of early right hemisphere pathology on both verbal and performance IQ scores argues for the participation of the right hemisphere in certain fundamental processes that may underlie both linguistic and spatial competence. Given the specialization of the right hemisphere for the acquisition of spatial skills it appears possible that a certain elementary sensori-motor coordinate system may normally be established by the right hemisphere, and in some way aid the differentiation of more complex skills which do not, at first sight, appear directly connected to it. The importance of elementary sensori-motor expedience in evolving more complex cognitive operations has been stressed by many theorists, and by Piaget (1979) in particular. However, regardless of whether or not the presence of this correspondence between theories of cognitive development and neuropsychological research finding is accepted, the results obtained by McFie (1971a, b) and Woods (1980) emphasize the importance of the presence of a particular structure at a particular stage during development rather than supporting the view that different structures are functionally equivalent.


Aphasia in children

The study of language disorders in children is important to a number of problems in developmental neuropsychology. It has provided evidence concerning the extent of functional specialization in the cerebral hemispheres during maturation; data concerning the reorganizational or plastic capacity of the developing brain; and a third, equally important, question, evidence as to the manner in which language becomes established in cortical structures. This question is, in fact, separate from those of hemispheric specialization and plasticity. Here we are concerned with the similarity between the aphasic symptoms of the child and the adult. The greater the similarity of the syndromes the more likely it is that the adult structural pattern has become established, even if subsequently the recovery of the child is more complete because duplication of function in the contralateral hemisphere is still possible. In the present section each of these three topics will be examined, but the characteristics of childhood aphasia will be examined first.

The clinical picture found in childhood aphasia was described by Guttman (1942), who noted that despite claims that the syndrome was rare, he had found it not an unusual accompaniment of head injury or intracranial pathology. In contrast to the adult, where complaints with speech difficulties, failures to name objects and paraphrasia are common, the aphasic child is usually apathetic and morose with such extreme poverty of speech that it approaches mutism. Absence of spontaneous speech, lack of willingness to speak, and a hesitant dysarthric telegrammatic-style speech are frequently noted, these symptoms being more common in the younger child. In contrast to the extreme poverty of speech production, comprehension of simple instructions is evident so that parts of the body or objects can be appropriately indicated when a request is made. When prompted to speak difficulties in the manipulation of lips and tongue may be apparent together with failure to produce sound. As recovery progresses, initially the child will speak single words when prompted. It will then move to sparse spontaneous utterances before speech moves into a stage when impoverished but spontaneous conversation occurs with persistent dysarthria. This pattern, which bears the imprint of an almost exclusively motor disorder, occurred in all cases below 10 years of age and occurred regardless of the location of the lesion within a hemisphere. Where damage occurred after the tenth year in some cases speech showed a lack of spontaneity but symptoms more characteristic of the adult pattern with impaired auditory comprehension, syntactical and paraphrasic errors, together with difficulties of naming were found. Dysarthria may or may not accompany these symptoms.

This picture of aphasia in childhood has been supported by subsequent research in which the onset of the language loss is sudden following external injury or internal pathology. In Guttman’s cases the five instances of injury which produced aphasia in which the symptom was exclusively one of speech production difficulty were aged 8 years or below, and the two instances in which speech output was not affected but other aphasic symptoms were present were over 10 years of age. The series of cases reported by Hecaen (1976) show that in two instances where the disorder was exclusively one of speech production the children were aged 6, and in the remaining case 3j years. In children aged 7 years and more, comprehension, naming and paraphrasic disorders were more likely to occur. Both Guttman (1942) and Hecaen (1976) stress the fact that recovery may be extremely rapid, marked improvement sometimes being noted in as little as 6 weeks. In children aged over 10 years however, the time course of the disability may sometimes be prolonged. In middle to late childhood the aphasic symptoms begin to mimic the adult pattern, whereas in early childhood the disorder appears to be purely expressive. In adults expressive aphasia is often produced by lesions located in the anterior region of the hemisphere and difficulties in comprehension occur more frequently with temporal and inferior parietal damage (Geschwind, 1970). However, in children below 10 years, disorders of expression appear to occur regardless of the location of the lesion (Guttman, 1942). A second distinctive feature of the aphasic syndrome in young children is the absence of cases of jargon aphasia, where the speech output is rapid with relatively normal articulation but contains many circumlocutions and paraphrasias (Geschwind, 1972). Woods and Teuber (1978) claim to have one documented case of jargon aphasia in a 5-year-old child, but the clinical description is unlike the adult form. The child produced a stream of meaningless sounds, but when recognizable words were uttered they were most often the names of objects. The child also showed evidence of a purely apraxic disturbance, e.g. sticking out his tongue when asked to blow out a light. To the present author, the picture is too dissimilar to the adult form to be classed as an instance of jargon aphasia, the only feature in common being the high rate of vocal, as opposed to verbal, output.

The cases of language loss in childhood so far described were instances where loss was abrupt, following external or internal injury, and where injury was usually confined to one cerebral hemisphere. A rather different type of childhood aphasia occurs when the language loss is associated with either the onset or development of bilateral epileptiform abnormalities (Landau and Kleffner, 1957; Worster-Drought, 1971; Gascon et al , 1973). In these cases, the loss of language is associated with difficulties in understanding speech, which, in some cases, may evolve over a matter of days or weeks. The child shows lack of response to speech, which may be mistaken for peripheral deafness. Audiometric testing reveals either mild or moderate hearing loss, but this loss is insufficient to account for the comprehension disorder and, in any case, hearing usually shows progressive improvement after an initial depression. In some cases auditory evoked potentials to pure tones may be normal, but evoked potentials to speech show abnormalities (Gascon et al ., 1973). Loss of language is gradual and persistent, and while in some cases recovery may occur over a period of years (Landau and Kleffner, 1957), in other cases it appears to be permanent (Worster- Drought, 1971). In some cases loss of speech may be almost total and auditory comprehension limited to less than a dozen words. Despite gross impairment in the development of language, frequently these children do not show impairment on non-verbal tasks in intelligence tests. Of the 14 cases described by Worster- Drought (1971), performance IQ ranged from 96 to 140, with only one case falling below 100. This remains true despite the fact that, in many cases, the onset of pathology is at less than 5 years of age. These cases of bilateral abnormality are in contrast to cases where a unilateral lesion produces aphasia, from which the child subsequently recovers yet shows a low overall IQ (Hecaen, 1976).

When damage to a single hemisphere produces aphasia the child usually recovers language, and in the young child this recovery is usually better than when damage occurs above 10 years (Lenneberg, 1967). This has often been seen as evidence that the two cerebral hemispheres are initially equipotential as far as the development of language is concerned. Further, it has sometimes been claimed that both cerebral hemispheres are involved initially in language development with lateralization increasing with age (see Dennis and Whitaker, 1977 for a review). It has already been noted that as far as attainment on certain language tests is concerned the two hemispheres are not equivalent. The view that the right hemisphere is involved in language acquisition in the infant and young child comes from reports of the high incidence of speech disturbances following right hemisphere damage. The incidence of language disorders with lesions of the left and right hemispheres described by different researchers varies widely. In the case of the left hemisphere, damage has been estimated to produce language disorder with an incidence varying from 25% (Ingram, 1964) to over 90% (Dunsdon, 1952). In the case of the right hemisphere the estimated incidence has varied from less than 1 % (Ingram, 1964) to nearly 38 % (Dunsdon, 1952). Only one investigator has claimed an equal frequency of language disorder following either left or right cerebral damage (Basser, 1962). The discrepancies seem too large to attribute to statistical sampling fluctuations. One of the problems encountered in this area is the definition of what constitutes an aphasic language disturbance. Language difficulties are associated with depressed general intelligence (Mein, 1960) so that severe brain damage which produces severe retardation may produce language disturbance indirectly. There is also the problem of whether speech disturbance should be considered an aphasic disturbance (Ingram, 1965). It is already apparent that the syndrome of aphasia • in children may vary from almost total mutism to a clinical picture similar to that of the adult with comprehension disturbance and naming impairment. That the type of impairment can vary not just with age of the child but also be related to the damaged hemisphere can be seen by examining the series of Hecaen (1976). Of 6 cases of right hemisphere damage, only the two youngest (6 and 3^ years) showed any disturbance and this was articulatory. Bishop (1967) has reported that in cases of infantile hemiplegia, articulatory disturbances are equally likely following damage to either hemisphere, but that left hemisphere damage additionally delays the acquisition of word combinations rather than single words.

The possibility of a different pattern of impairment following left and right hemisphere injury is not the only factor which complicates the issue. Woods and Teuber (1978) have pointed out that there is a tendency for investigators since 1940 to report a lower incidence of aphasia following right hemisphere injury than earlier workers. They attribute this to the fact that in older investigations aphasias and hemiplegias were frequently complications of systemic infectious illnesses such as scarlet fever, bacterial pneumonia and diphtheria, which can produce not only focal lesions but also diffuse bilateral encephalopathy. Undoubtedly the frequent reliance on hemiplegia alone as the sign indicating exclusive damage to one hemisphere is likely to result in the inclusion of cases where a less extensive pathology is also present in the hemisphere that is assumed to be intact. Bearing these facts in mind, it would obviously be hazardous to speculate concerning the true incidence of language disturbance following right hemisphere pathology. For the moment it is sufficient to say that the incidence of aphasia following right hemisphere damage may be considerably less than previously thought, perhaps as little as 5 % in those who were previously right-handed (Woods and Teuber, 1978).

A finding that has already been mentioned several times is that concerning the capacity of the right hemisphere to acquire language following early left hemisphere injury. There is little doubt that the capacity to transfer language to the right hemisphere is a real factor in the recovery from aphasia in children. However, it cannot be assumed that in every case of childhood aphasia recovery of language is due to transfer to the contralateral hemisphere. Milner (1974) noted, on the basis of the Wada test, that in adults who were left-handed but had sustained early left hemisphere damage, language was present in the left hemisphere in 30 % and bilaterally present in 16 % of cases. Thus, in 46 % of cases who had left hemisphere injury, the left hemisphere was still involved in language to some degree. Whether or not language transferred depended on whether certain critical areas were damaged. In cases where left hemispherectomy is performed, following widespread unilateral damage, it is clear that the presence of linguistic competence is dependent on the remaining hemisphere (Dennis and Whitaker, 1977). When such language transfer does occur, while verbal IQ may not be significantly depressed relative to performance IQ, it should be remembered that such tests do not directly sample knowledge of language structure. Where tests are designed to evaluate grammatical comprehension then deficits appear (Dennis and Kohn, 1975; Teuber, 1975; Dennis and Whitaker, 1976; Day and Ulatowska, 1979). However, with these reservations in mind, children exposed to left hemispherectomy do show an adequate degree of language competence in relation to their overall IQ and it has frequently been remarked that it would be an incredible improvement if each adult aphasic could recover the same level of language competence (Geschwind, 1972).

The duration of such plasticity in the developing brain has been the subject of disagreement. Lenneberg (1967) believed that the period of plasticity in regard to language mechanisms lasted until puberty. Krashen (1973) has challenged this view mainly on the basis that right hemisphere damage above the age of 5 does not often produce aphasia whereas below this age it frequently does. However it should be understood that the issue of the degree to which both hemispheres are involved in language acquisition early in life (and evidence has already been cited that right hemisphere aphasia may be quite different in form from left hemisphere aphasia in young children) is quite a different one from the question of whether interhemispheric transfer is possible. Children between 5 and 10 years do show good recovery from aphasia and it would be surprising indeed if language could have survived in the left hemisphere given the extent and severity of the damage in some instances, e.g. right hemiplegia and hemianopsia (Hecaen, 1976). On the balance the evidence would appear to favour a period of plasticity extending to at least 10 years of age. There is even some indication that a period of reduced plasticity may extend far beyond this age although whether it involves inter-hemispheric transfer or improved within-hemisphere recovery is another question. Teuber (1975) noted that an analysis of 167 cases of brain injury sustained during the Korean campaign showed that the population who were under 22 at the time of injury showed better recovery of language than those who were 23 years and over. It may be premature then to try to set rigid cut-off points for recovery.

The evidence presented here suggests that aphasia in children is not one syndrome but several. In children of 6 years and below mutism and dysarthria appear as the main symptoms with comprehension being relatively well preserved. Furthermore this pattern appears to occur regardless of whether the lesion is in the left or right hemisphere and also appears to be insensitive to the precise location of the lesion within a hemisphere (whether it is frontal, temporal or parietal). Above 6 years, symptoms which are regarded by many as truly aphasic (comprehension and naming disorders) appear. The symptoms appear to occur largely following left rather than right hemisphere lesions. Between the ages of 6 and 14, jargon aphasia in its adult form is infrequent although the extended circumlocutions that are one of the characteristics of aphasia do occur (Guttman, 1942). The rapidity of the recovery process in some cases and, in very young children, the preservation of comprehension, makes it extremely unlikely that language has been totally relearned by the right hemisphere (Geschwind, 1972). This factor has suggested to some investigators that the right hemisphere must be involved in linguistic processing at an early developmental stage and in fact retains some capacity for comprehension even in the adult after cerebral differentiation (Kinsbourne, 1975).

It is possible then that during the early stages of language learning both hemispheres acquire comprehension and share control of the speech mechanism. This may be necessary in the initial stages, because fine bilateral control of the speech mechanism is required since suitable motor synergisms for a culture- specific phoneme system are not yet well established in subcortical structures. The consequence of this arrangement is that a lesion to either hemisphere can disrupt speech production but comprehension is relatively unaffected because the structural basis of language as opposed to speech does not require a bilateral component. However, the establishment of subcortical synergisms for the execution of the basic components of speech production together with the presence of structurally more specialized language mechanisms in the temporoparietal region of the left hemisphere normally leads to left hemisphere capture of the speech output mechanism. This process is probably a gradual one, but as it proceeds there is less functional demand for right hemisphere processing of language and there may even be active inhibition of its linguistic processing by the left hemisphere. Eventually this isolation of the right hemisphere may lead to structural changes at the synaptic level so that the re-establishment of control is no longer possible. To the extent that this isolation process is incomplete transfer of control is still possible. Thus in young children (under 5 years) the loss of the left hemisphere will show itself in only transitory speech output disturbances since this process of capture is just beginning and both hemispheres are still involved. Even at this age however the linguistic superiority of the left hemisphere is already apparent (see Young, Chapter 6, this volume, for a review of the psychophysical literature), and it is in fact this superiority that will allow the eventual suppression of the right hemisphere. In children between the ages of six and ten years the speech mechanism is probably under the control of the left hemisphere but right hemisphere control mechanisms have not yet functionally atrophied. Left hemisphere damage at this age can produce speech disturbances solely and/or truly aphasic disturbances which are transitory, while damage to the right hemisphere only rarely affects these mechanisms. With the passage of time however, the capability of the right hemisphere wanes through disuse and in the majority of cases only a token linguistic capacity remains. Even if in later life the possibility of direct inhibition by the left hemisphere is removed, by severing the corpus callosum, the right hemisphere has residual linguistic comprehension but remains mute (Gazzaniga and Sperry, 1967). This is probably because the process of gaining control of the speech mechanisms involves the regulation of neuromuscular synergisms at subcortical levels, and these remain under left hemisphere control. It should be noted that the control of the vocal apparatus by the left hemisphere may be specific to its use in the context of spoken language. Where lesions of the left hemisphere produce expressive (Broca’s type) aphasia the ability to use the voice in the context of singing including the fluent production of words may be well preserved (Yamadori et al ., 1977). Evidence for a motor capture account of left hemisphere language dominance can also be found in studies of adult aphasics (cf. Kinsbourne, 1975).


The plasticity of the developing brain

It is usually accepted that the younger the individual when the brain sustains injury, the greater the resilience and the greater the capacity for functional restitution. Against this one must set the view that the developing brain is particularly vulnerable and long-term effects emerge if normal development is impaired. These two views may be partially reconciled by proposing that following early brain damage, specific skills may be spared but at a cost that will be seen in the overall lowered cognitive capacity of the brain (Teuber, 1975). Thus language or visuo-spatial skills may be spared following left or right hemisphere injury respectively, but intellectual achievement as measured by IQ tests or by school performance will show depression. Evidence already cited concerning the specific effects of early brain damage makes it clear that the consequences are not just seen in a uniformly lowered total processing capacity but depend on the site of injury. Language achievement is specifically lowered following left hemisphere injury and spatial skills depressed specifically following right hemisphere injury.

The evidence in favour of a greater degree of plasticity comes from a number of sources. Some animal species show spared sensory capacity following cortical lesions in infancy (Schneider, 1969) while in other species age at time of injury does not appear to affect the magnitude of the deficit (Doty, 1973). Even where pattern vision is spared following early lesions of the striate cortex, the animals may still take longer to pretrain before formal testing can commence (Schneider, 1970). In man there is evidence of age-related sparing of sensory function. Rudel et al (1974) noted minimal impairment in brain damaged children on somaesthetic thresholds but these children were still impaired on tactile object recognition. Elementary motor function in children may also show greater savings following early massive unilateral injury (Cairns and Davidson, 1951), but such abilities as are preserved, are rudimentary. In man following early unilateral damage that is extensive enough to destroy large areas of the striate cortex, the visual field defects are similar to those produced in adults with similar pathology (Paine, 1960). In this case it might be expected that savings would be possible given the existence of a second, phylogenetically older, visual structure in the midbrain. Where lesions are more restricted, however, savings on visual (in terms of shrinkage of the size of scotoma), somatosensory and motor functions are age-related and show relatively better recovery even when damage occurs early in the third decade of life as compared to later (Teuber, 1975). Without doubt however, the most outstanding examples of functional recovery are those which occur in the areas of language and spatial skills in man following early injury.

The explanation of the functional recovery that does occur following early brain damage is not straightforward. As discussed above, part of the restitu- tional capacity may lie in mechanisms that enable individual neurones to withstand injury so the functional extent of a lesion may be less than in the mature system. It may also lie in neural regeneration per se, although Schneider (1979) has provided evidence that such anomalous regeneration, when it occurs, may actually result in greater behavioural deficit. In the case of the somatosensory and motor systems, while the greater volume of neural circuitry is concerned with analysis and control of the contralateral side of the body, ipsilateral pathways do exist. In the case of the motor system there is even evidence that hypertrophy of ipsilateral pathways occurs after early hemi- spherectomy (Hicks and D’Amato, 1970). These ipsilateral pathways may assume greater functional importance in the case of unilateral brain damage and sustain the limited behavioural savings that occur. The continued development of linguistic and spatial skills after early brain damage are however of a different order. It has been suggested that the survival of these skills in one hemisphere is due to the fact that the necessary processors exist initially in each hemisphere but that during development one hemisphere suppresses the influence of the other. This suppression of the influence of the contralateral hemisphere may be a necessary prerequisite for the development of higher cognitive skills, since processing space may be at a premium. When both language and spatial skills are acquired by only one hemisphere (following early hemispherectomy) neither skill reaches its full potential (Teuber, 1975). Where the corpus callosum is absent during development, and normal interhemispheric communication is consequently impossible, a rather bizarre pattern of cognitive development is seen. In such cases of callosal agenesis it appears that either performance IQ or verbal IQ becomes pre-eminent despite the existence of functional capacity in two hemispheres (Dennis, 1977). Extreme discrepancies do not in these cases appear to be predictable from age of the subject at the time of testing, sex, type of agenesis, handedness or specific neurological signs. It appears rather that a mechanism which enables a normal balance of cognitive skills to occur is absent. In the normal individual then the existence of two intact hemispheres may not be sufficient for normal cognitive growth. Some additional mechanism which ensures that unnecessary duplication does not occur and enables an efficient use of available processing capacity seems to be necessary. The consequence of the presence of such a mechanism during development is that usually specific skills become established predominantly in one hemisphere or the other and once they are so established there is little opportunity to recapitulate the process. The failure of the adult brain to fully re-establish linguistic or spatial skills following damage is a consequence of the presence of a mechanism (whose effector path is the corpus callosum) that enables a balanced and complete cognitive growth to occur.


Conclusions

Consideration of the evidence concerning the outcome of brain injury in the developing nervous system leads to the inescapable conclusion that age at the time of injury is a critical factor in determining both the initial syndrome and the pattern of adaptation that follows. Certain abilities such as early maturing spatial skills, language and various elementary sensory and motor functions may show relative recovery, the extent being determined by the location and size of the lesion. Other abilities, particularly those involving fine motor coordination, late maturing spatial skills as well as the overall level of intellectual attainment, may show more profound defects. These latter effects may be partly ascribed to a lower overall processing capacity, but in the case of general intellectual attainment, more profound effects are seen following damage to the right hemisphere before (compared with after) one year of age, a factor which argues that volume of tissue damaged is not the sole consideration. Differing patterns of language disturbances are also seen in children depending on the child’s age at the time pathology develops. These considerations, which emphasize that damage is occurring within a system whose state is continually changing, present particular difficulties for those with interests in the outcome of early brain damage. As Teuber and Rudel (1962) point out: ‘Whether we are working with infrahuman forms or with children, we must define (1) those aspects of behaviour in which the effects of early injury appear only with a delay, as development progresses; (2) those other aspects of performance in which there will be impairment at all ages; and finally, (3) those aspects of performance where there is an immediate effect which, however, disappears as development proceeds’. The interpretation of research which finds age-dependent differences is often far from clear. Reports that the patterning of IQ subtests is insensitive to the location of injury in young children may be a genuine indication of an age- dependent difference, despite the fact that such tests were not specifically designed to assess brain damage. However, since it is found that in adults that IQ tests are only indicative of lesion laterality in the acute but not the chronic phase (Fitzhugh et al ., 1962), the failure to find specific indication of lesion location in children with infantile injury may be attributable to the interval between injury and testing rather than an age-related difference in functional organization.

The emergence of specific functional deficit following early brain injury stresses the importance of critical structures for cognitive achievement. Just how extensively the predesignated structures of the nervous system determine the detailed characteristics of cognitive development remains to be seen. It is only relatively recently that explorations of the specific patterns of loss, as measured by specially developed tests, have begun. It is also apparent that much of the research has been concerned with hemispheric asymmetry where the structural similarity of the hemispheres means that the capacity for interhemispheric reorganization may lead to an over-valuation of the plastic capacities of the developing brain. Cases where bilateral loss of a structure is involved give one much less confidence in the restitutional capacity of the young brain. Bilateral frontal lobe damage in childhood appears to have effects at least as serious as equivalent damage in adults (Russell, 1959; Ackerly, 1964) although the paucity of research in this area and the anecdotal nature of some of the findings make conclusions tentative. There is a scarcity of unequivocal evidence that areas of the brain not normally involved in the development or performance of specific functions may assume those functions when other areas are damaged. Goldman and Lewis’s (1978) demonstration that the dorsolateral prefrontal cortex in the macaque may assume some of the functional capability of the orbitofrontal cortex, provided damage occurs early in development, remains one of the few clear demonstrations of such effects in the CNS of primates following bilateral lesions. However, the fact that the normal limits of plasticity and the extent to which they may be influenced by specific experience remain undetermined, gives developmental neuropsychologists particular problems in understanding the precise nature of brain-behaviour interrelations. Nevertheless, the fact that plasticity is a real phenomenon and may be influenced by specific experience (Goldman and Lewis, 1978) gives some hope that understanding of its nature may lead to more effective remediation regimes designed to capitalize on its characteristics.

Acknowledgements

I am grateful to H. D. Ellis and E. A. Salzen for advice and discussion during preparation of this manuscript.


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Dickerson JWT. and McGurk H. Brain And Behavioural Development. (1982) Blackie & Son Ltd., Glasgow.

Brain and Behavioural Development - 1982: 1 Neural Development | 2 Comparative Neural | 3 Malnutrition | 4 Hormones and Growth Factors | 5 Cortical Activity | 6 Functional Asymmetry | 7 Plasticity | 8 Sex Differences


Cite this page: Hill, M.A. (2019, August 26) Embryology Book - Brain and behavioural development 7. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Book_-_Brain_and_behavioural_development_7

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