Book - Brain and behavioural development 7
|Embryology - 10 Jul 2020 Expand to Translate|
|Google Translate - select your language from the list shown below (this will open a new external page)|
العربية | català | 中文 | 中國傳統的 | français | Deutsche | עִברִית | हिंदी | bahasa Indonesia | italiano | 日本語 | 한국어 | မြန်မာ | Pilipino | Polskie | português | ਪੰਜਾਬੀ ਦੇ | Română | русский | Español | Swahili | Svensk | ไทย | Türkçe | اردو | ייִדיש | Tiếng Việt These external translations are automated and may not be accurate. (More? About Translations)
|A personal message from Dr Mark Hill (May 2020)|
|contributors to the site. The good news is Embryology will remain online and I will continue my association with UNSW Australia. I look forward to updating and including the many exciting new discoveries in Embryology!|
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
|Historic Disclaimer - information about historic embryology pages|
|Embryology History | Historic Embryology Papers)|
- 1 Chapter Seven - Determinate and Plastic Principles in Neuropsychological Development
- 1.1 Introduction
- 1.2 The context within which damage occurs during development
- 1.3 Electrophysiological and neuroanatomical maturation
- 1.4 Neuropsychological evidence concerning functional maturation
- 1.5 Interactive effects and their interpretation
- 1.6 The consequences of early brain damage
- 1.7 Aphasia in children
- 1.8 The plasticity of the developing brain
- 1.9 Conclusions
- 1.10 References
Chapter Seven - Determinate and Plastic Principles in Neuropsychological Development
Denis M. Parker
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.
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.
I am grateful to H. D. Ellis and E. A. Salzen for advice and discussion during preparation of this manuscript.
Ackerly, S. S. (1964) ‘A case of paranatal bilateral frontal lobe defect observed for thirty years’, in The Frontal Granular Cortex and Behavior (eds. J. M. Warren and K. Akert), McGraw-Hill, London, 192-218.
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.
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.
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.
Boll, T. J. and Reitan, R. M. (1972) Comparative ability interrelationships in normal and brain injured children. J. Clin. Psychol, 28, 152-156.
Broca, P. (1861) Remarques sur le siege de la faculte du langage articule suivies d’une observation d’aphemie (pert de la parole). Bull. Soc. Anat. Paris, 3, 330-357.
Bronson, G. (1974) The postnatal growth of visual capacity. Child Devel, 45, 873-890.
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.
Byers, R. K. and McLean, W. T. (1962) Etiology and course of certain hemiplegias with aphasia in childhood. Pediatrics, 29, 376-383.
Cairns, H. and Davidson, M. A. (1951) Hemispherectomy in the treatment of infantile hemiplegia. Lancet, ii, 411-415.
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.
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.
Dejerine, J. (1892) Contribution a l’etude anatomopathologique et clinique des differentes varieties de cecite verbale. C. R. Soc. Biol, 4, 61-90.
Dejerine, J. and Andre-Thomas, J. (1912) Contribution a l’etude de l’aphasie chez les gauchers. Rev. Neurol, 24, 213-226.
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.
Dennis, M. and Kohn, B. (1975) Comprehension of syntax in infantile hemiplegics after cerebral hemidecortication: left hemisphere superiority. Brain and Lang., 2 , 472-482.
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.
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.
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.
Fedio, F. R. and Mirsky, A. F. (1969) Selective intellectual deficits in children with temporal lobe or centrencephalic epilepsy. Neuropsychologia, 1 , 287-300.
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.
Flourens, P. (1824) Recherches Experiment ales sur les Proprietes et les Fonctions du Systeme Nerveux dans les Animaux Vertebres. Crevot, Paris.
Galaburda, A. M., Le May, M., Kemper, T. L. and Geschwind, N. (1978) Right-left asymmetries in the brain. Science, 199, 852-856.
Gascon, G., Victor, D., Lombrosso, C. T. and Goodglass, H. (1973) Language disorder, convulsive disorder and electroencephalographic abnormalities. Arch. Neurol, 28, 156-162.
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.
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.
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.
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.
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.
Goldstein, K. (1939) The Organism. American Book Publishers, New York.
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.
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.
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.
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.
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.
Ingram, T. T. S. (1964) Pediatric Aspects of Cerebral Palsy. E. and S. Livingstone, Edinburgh.
Ingram, T. T. S. (1965) Specific retardation of speech development. Speech Pathol Ther., 8, 3-11.
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.
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.
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.
Landau, W. M., Goldstein, R. and Kleffner, F. R. (1960) Congenital aphasia: a clinicopathologic study. Neurol, 10, 905-921.
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.
Lashley, K. S. (1929) Brain Mechanisms and Intelligence: A Quantitative Study. Univ. Chicago Press, Chicago.
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.
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.
Marshall, W. A. (1968) Development of the Brain. Oliver and Boyd, Edinburgh.
McFie, J. (1961a) Intellectual impairment in children with localized post-infantile cerebral lesions. J. Neurol. Neurosurg. Psychiat., 24, 361-365.
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.
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.
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.
Paine, R. (1960) Disturbances of sensation in cerebral palsy. Little Club Clin. Dev. Med., 2, 105- 109.
Piaget, J. (1979) ‘Correspondences and transformations’, in The Impact of Piagetian Theory (ed. F. B. Murray), University Park Press, Baltimore, 17-27.
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.
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.
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.
Teuber, H.-L. (1975) ‘Recovery of function after brain injury in man’, in Outcome of Severe Damage to the Central Nervous System (Ciba Foundation Symposium No. 34), Elsevier, Amsterdam, 159-186.
Teuber, H.-L. and Rudel, R. G. (1962) Behavior after cerebral lesions in children and adults. Dev. Med. Child Neurol ., 4, 3-20.
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.
Tsang, Y.-C. (1937) Maze learning in rats hemidecorticated in infancy. J. Comp. Psychol., 24, 221-254.
Turner, O. A. (1948) Growth and development of cerebral cortical pattern in man. Arch. Neurol. Psychiat., 59, 1-12.
Turner, O. A. (1950) Postnatal growth of the cortical surface area. Arch. Neurol. Psychiat., 64, 378-384.
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.
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.
Walsh, K. W. (1978) Neuropsychology: A Clinical Approach. Churchill Livingstone, Edinburgh.
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.
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.
Yamadori, A., Osumi, Y., Masuhara, S. and Okubo, M. (1977) Preservation of singing in Broca’s aphasia. J. Neurol. Neurosurg. Psychiat., 40, 221-224.
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.
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. (2020, July 10) Embryology Book - Brain and behavioural development 7. Retrieved from https://embryology.med.unsw.edu.au/embryology/index.php/Book_-_Brain_and_behavioural_development_7
- © Dr Mark Hill 2020, UNSW Embryology ISBN: 978 0 7334 2609 4 - UNSW CRICOS Provider Code No. 00098G