Book - Brain and behavioural development 8

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

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

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Chapter Eight - Sex Differences in Brain Development: Process and Effects

Miranda Hughes

Introduction

Identifying the neural mechanisms which underlie particular behavioural and cognitive functions has become a fundamental aspect of psychological research, and in recent years considerable progress has been made in understanding the way in which both pre- and postnatal hormones can affect brain differentiation. The notion that prenatal hormones which are differentially produced by males and females may have irrevocable effects on the brain as well as on physical morphology is politically provocative; nonetheless, improving our knowledge of the neural substrates of behaviour ought also to facilitate our understanding of how postnatal environment exerts its influence. Thus, to find sex differences in brain differentiation, and to link these to sex differences in cognitive ability and behaviour, does not necessarily imply biological determinism; rather, it enhances our understanding of the raw materials which educational and cultural pressures may mould in a variety of ways.

This chapter discusses the way in which pre- and postnatal hormones affect brain differentiation, and it is argued that the long-term effects of the early hormone environment may predispose any individual to certain ‘masculine’ or ‘feminine’ type behaviours. However, different aspects of our behavioural repertoire are certainly under different degrees of hormonal influence and human behaviour is not clearly sexually differentiated. As Money (1977a) put it so cogently ‘... the only irreducible sex differences are that women menstruate, gestate and lactate, and men impregnate ... most sexually dimorphic behaviour as we know it is the product of cultural history and not of some eternal verity programmed by non-cultural biology. 5 (pp. 32, 33).

Following Pfeiffer’s (1936) innovative and now classic work, the precise role of prenatal hormones in the development of the hypothalamic mechanisms which control hormone release at puberty, and which are responsible for the development of sexually differentiated physical characteristics, is well established (Harris, 1964, 1970). The well documented cases of children exposed to abnormal levels of particular steroids in utero (Money and Ehrhardt, 1972), and the work of Dorner (1979) on human homosexuality, have subsequently raised a number of questions concerning the effect of hormones on a wide range of behaviour. The line of reasoning seems to be that if (a) some neural mechanisms (e.g. for gonadotropin release at puberty) are determined by the role of prenatal hormones, and (b) foetuses exposed to abnormal levels of types of particular hormones behave in specific and atypical ways, then it follows that (c) just as the prenatal hormonal environment has ‘wired-up 5 the brain in such a way as to determine the expression of certain endocrine functions, so too can it predispose an organism to specific behaviour patterns. A closer examination of the three stages of this argument should facilitate the development of a conceptual framework within which to extend our understanding of the variety of expression in human abilities and behaviour.

Prenatal sex differences in development

Distinctively male or female development begins at around the seventh week after conception when the initially bi-potential embryonic gonad differentiates to form either a testis (in the case of a male) or an ovary (in the case of a female). This differentiation of the gonads is determined by the genetic sex of the zygote (46XY in the male; 46XX in the female); where there is no second sex chromosome as in Turner’s syndrome (45X) the gonads are undifferentiated at birth, although germinal follicles may have been present in the early foetal stages (Scott, 1978). Jost (1979) tentatively suggests that there may be a specific membrane protein controlled by a locus on the Y chromosome (the H-Y histocompatibility antigen) which is responsible for the differentiation of testes, and whose individuals who do not produce this antigen will form an ovary. Once a testis has been formed the release of a substance (probably a foetal protein) known as Mullerian inhibiting substance (MIS) induces the regression of the Mullerian ducts, and secretion of androgenic hormones enables the development of the male reproductive tracts and genitalia. In the absence of testicular hormones female development occurs; ‘...in mammals and birds body sex shows a basic developmental trend corresponding to that of the homozygous sex. Characteristics of the heterozygous sex have to be actively imposed by the secretions of the corresponding gonads 5 (Jost, 1979, p. 8). Thus, the appearance of Turner’s syndrome infants is unequivocally female, and that of Klinefelter’s syndrome infants (47XXY and 48XXXY) is unequivocally male.

Sexual differentiation does not, however, always proceed entirely smoothly, and Scott (1978) has provided a useful classification of some ‘intersex’ conditions. He suggests that there are four basic processes which may distort normal sexual differentiation: (i) chromosomal intersex, in which extra or missing sex chromosomes affect development; (ii) gonadal intersex, in which the gonadal tissue is at variance with the chromosomal constitution of the individual; (iii) partial masculinization of chromosomal and gonadal females, due either to a disorder of adrenal functioning or the exogenous administration of steroid hormones to the mother; and (iv) incomplete masculinization of chromosomal and gonadal males which may occur either because an individual is insensitive to the androgen being produced by the testes or because there is some failure in androgen production. These medical conditions have often been described as ‘nature’s experiments’ because they shed light on the various ways in which hormones affect development.

In Turner’s syndrome, the missing chromosome may be either an X or a Y: evidence for this comes from a report by Leujeune (1964) of monozygotic twins, one of whom was a normal male of 46XY karyotype, the other of whom was born with 45X karyotype (and therefore a female phenotype). Turner’s syndrome females are typically short in stature, and require oestrogen therapy at puberty to effect normal breast development. There may be a range of other physical stigmata present (e.g. shield chest, neck webbing, low-set ears), but general intelligence is not significantly affected (Money and Ehrhardt, 1972). The streak gonads are often entirely non-functional, but they may contain some ova in which case pregnancy is possible.

There are approximately two cases per thousand of males with a 47XXY karyotype, and a similar number with 47XYY karyotype. The former often have small testes and prostates and diminished body and facial hair; they may also show some breast development at puberty, and are frequently infertile. Males with 47XYY karyotype have a tendency to be taller than average, but otherwise display no specific physical abnormalities. It has been estimated that both 47XXY and 47XYY males are over-represented in mental or penal institutions during late adolescence or adulthood. Differences between these groups in deviant behaviour are not significant; however, their crimes are more likely to be sex or property offences than those of their delinquent peers (Meyer-Bahlburg, 1974).

Cases of gonadal intersex (hermaphroditism) show widely varying arrangements of gonadal tissue and genitalia. Scott (1978) suggests that there may be an interchange of genetic material between the X and Y chromosome before the first meiotic division in the primary spermatocyte, which could lead to widely varying sexual differentiation according to the cells in which the Y chromosomal material is active. Such cases clearly do not provide a homogeneous subject sample, but are nonetheless interesting individually.

The partial masculinization of females and the incomplete masculinization of males illustrate clearly the role of steroids in the development of sex-related physical characteristics. The former of these conditions is usually due to congenital adrenal hyperplasia (CAH) which occurs as a result of an enzymatic deficiency in the adrenal steroid metabolic pathways. The most common form of CAH is 21-hydroxylase deficiency which results in a build-up of 17-hydroxypro- gesterone, the metabolic derivatives of which have a virilizing influence on the female foetus. Male infants appear normal at birth (although puberty may be accelerated by as much as ten years if the condition is not diagnosed and treated), but female infants have masculinized external genitals. The female internal organs are normal, and with appropriate medical treatment (including surgery to feminize the genitals) these girls may menstruate at puberty and eventually bear children.

Masculinization of females may also arise from the influence of steroid hormones administered to the mother during pregnancy to prevent miscarriage. Ehrhardt and Money (1967) report ten such cases, and Scott (1978) describes an individual case following the administration of norethisterone to the mother. As in the CAH cases, masculinization is apparently restricted to the external genitalia, and can be corrected surgically.

There are three possible defects of the androgenization process which can give rise to the incomplete masculinization of the male: defective androgen production, defective Mullerian regression, and androgen insensitivity. The last of these is the best documented and is often known as ‘testicular feminization’. In this condition infants with a normal male 46XY chromosome complement are born with a female phenotype. Since Mullerian regression has occurred normally, there is a short blind vagina, but the external genitalia are unequivocally female. At puberty, there is spontaneous breast development, although pubic hair tends to be scant. The condition occurs despite normal steroid output from the testes, when the receptor cells fail to respond to the androgens which are present.

Individuals with complete androgen insensitivity may be quite oblivious to their condition until puberty, when they seek medical advice for amenorrhea. However, there are incomplete forms of androgen insensitivity: for example, where there is a failure to convert testosterone to the more potent 5a- dihydrotestosterone there may be incomplete masculinization of the external genitalia. Imperato-McGinley et al (1974) described some such cases in which the affected infants are given a female assignment at birth, but at puberty have to undergo a gender re-assignment because ‘anabolic events at puberty, in particular the increase in muscle mass, the growth of the phallus and scrotum, and the voice change, appear to be mediated by testosterone’ (p. 1214).

All of these ‘intersex’ conditions have considerable interest for psychology, in that they provide an opportunity to examine the possible behavioural effects of the prenatal hormones. It is certainly true that the prenatal hormonal environment affects cell differentiation in the brain; the speculations which require critical examination are those concerning the behavioural implications of such hormonal effects.

Hormonal action

The role of prenatal hormones in the development of the internal sex organs and genitalia is clearly established. If these hormones exert equally critical influences on brain differentiation, one would expect to find different patterns of neural networks in male and female brains. It is instructive therefore to examine the mechanism whereby hormones exert their influence so that sex differential developmental processes can be appropriately evaluated, and any anomalies of normal development can be interpreted.

The steroid hormones include the male sex hormones (androgens), the female sex hormones (oestrogens and progestins), and the hormones secreted by the adrenal glands (corticosteroids). Structurally, they resemble one another quite closely but differ radically in function. Their common core structure consists of four interconnected carbon rings. The pattern of bonding and the different side groups affect the overall shape of each molecule, and it is these subtle differences in shape which enable the hormones to attach themselves to specific target cells.

Hormones act directly on genetic mechanisms, so that when gene action is blocked (for example, by the action of certain antibiotics) hormones become powerless to exert their characteristic effect. A single hormone can activate an entire set of functionally related but otherwise quite separate genes, and hormonal specificity is dependent on the functional integrity of the target cells as much as on the hormone itself. The cytoplasm of target cells contains specific intracellular receptor proteins which accumulate and retain the hormone (this in contrast to the receptor mechanism of say, amines, for which the receptor site lies in the cell membrane). The steroid hormones then give rise to an increase in RNA synthesis, and can also effect the synthesis of a new variety of messenger RNA; these RNA molecules direct the formation of new protein molecules in the cytoplasm of the cell which enable the target cell to make its functional responses to the hormone.

During development the presence of male hormones will (in general) have a masculinizing effect on a genetic female. However, in experiments on rats it was found that whilst testosterone increased the amount of RNA produced in the liver cells of both males and females, in the female not only was there an increased amount of RNA, but a new type of RNA was being produced; this finding does suggest that even when male and female developing embryos are exposed to similar hormonal environments, the consequences need not necessarily be identical (Davidson, 1965). There has been some attempt to discover whether sex differences in brain differentiation are mediated by sex differences in cytoplasmic receptors. Data from Maurer (1973) and from Whalen (1974) show that there was selective cytoplasmic binding of oestrogen in the anterior hypothalamic-preoptic area (of rats), in the median eminence, but not in the cortex; however, the sex differences were not striking \ .. it seems unlikely that the small difference in nuclear retention that we found can account for the large differences existing between males and females in their behavioural responses to oestrogen’ (Whalen, 1974, p. 278).

Sex differences in brain differentiation

Pfeiffer (1936) was the first to establish that sex differences in the reproductive endocrinology of rats were determined by the hormone environment at a specific stage of development. He demonstrated that if a male rat is castrated within 3 days after birth and is subsequently (in adulthood) given ovarian grafts, he will respond to endogenous hormones with a surge of luteinizing hormone (LH) which is sufficient to produce corpora lutea in the ovarian graft. When the ovaries of newborn females were replaced with testes, many of these females failed to show any sign of oestrous cycles when they became adult, but entered a state of constant vaginal oestrus. However, female rats, which were ovari- ectomized at birth and subsequently had received ovarian implants, showed normal oestrous cycles and formation of corpora lutea. Male rats in which the testes were transplanted into the neck region at birth, and which received ovarian implants as adults, showed no capacity to form corpora lutea in the ovarian grafts. Pfeiffer concluded (erroneously) that the pituitary gland becomes sexually differentiated; subsequent experiments (see Harris, 1964, 1970) made it clear that in fact permanent control by the hypothalamus over the pituitary was established by the presence or absence of testosterone in a critical neonatal period. In the absence of testosterone a pattern of cyclic release of follicle stimulating hormone (FSH) and LH by the pituitary was established; when testosterone was present, release of hormones was tonic. Reznikov (1978) states that the critical periods for the sexual differentiation of the brain centres which regulate gonadotropin release \ .. occur in rabbits during the period of 19-23 days, and in guinea pigs at 36-38 days of pre-natal life, in rats, mice and hamsters, in the course of the first five days after birth. In the case of humans, the most probable period of sexual differentiation is considered to be the second trimester of pregnancy. It should be emphasised that experimental influences exerted outside the “critical” period are incapable of moderating the sex- specifying parameters of differentiation of the brain’ (p. 127).

Barraclough and Gorski (1961) demonstrated that cyclic gonadotropin release in female rats is regulated from a specific centre in the pre-optic hypothalamic region, whereas tonic gonadotropin response is regulated from the hypothalamic ventromedial arcuate region. Bari Kolata (1979) reviews the recent evidence that (in rats) it is the aromatization of testosterone to oestrogen which is crucial in the sex differences which occur during brain differentiation: when testosterone reaches the brain cells of newborn male rats it is converted to oestrogen and dihydrotestosterone but newborn female rats’ brains are protected from the effects of endogenous oestrogen by a-fetoprotein (a protein made by the fetal liver) which binds oestrogen and thus prevents it from reaching the developing brain. However, animals whose critical period for brain differentiation ends before birth (such as humans) have a-fetoproteins which do not bind oestrogens, and it is not yet clear what mechanisms might protect those animals’ brains from the effects of oestrogen.

Behavioural effects of sex differences in brain differentiation

(i) Sexual behaviour

The effects of pre- and perinatal hormones on the sexual behaviour of infrahuman species are reviewed carefully by Hoyenga and Hoyenga (1980), and the interested reader is referred to their text for a detailed list of primary sources. The evidence that early hormones are critical in determining sexual behaviour is unequivocal: neonatal castration of male rats (i.e. deandrogenization) increases all types of female sexual behaviours; and the prenatal androgenization of female rats increases the incidence of mounting and decreases the incidence of lordosis (the female sexual response consisting of concave arching of the back with simultaneous raising of the head and hind-quarters). Comparable evidence is available from primate studies. However, the perinatal administration of androgen to a female rat does not entirely masculinize her complete repertoire of sexual behaviour, any more than the castration of a male entirely suppresses all male-type responses.

Whalen (1974) proposed an orthogonal model of sexual differentiation in which he suggested that ‘during development hormones can defeminize without masculinizing and masculinize without defeminizing, and that hormones can defeminize one behavioural system (e.g. mating) while masculinizing another system’ (p. 469). This conception is not really satisfactory, for if one considers any specific aspect of sexual behaviour (such as lordosis) it is difficult to see how ‘masculinization’ does not also imply ‘defeminization’; however, it does try to deal with the data which indicates that lordosis in the female is not necessarily inhibited by perinatal administration of testosterone, even though she also exhibits increased incidence of mounting. In the same article Whalen raises some important criticisms of the naivety of the behavioural analysis which has often been employed in studies of sexual behaviour, and similar criticism is reiterated by Beach (1979). Responses such as lordosis can be only partially completed, and neonatally androgenized females do exhibit weak or partial lordosis responses with moderate frequency. Similarly, mounting is not always accompanied by intromission and ejaculation. A fmer-grained categorization of the behavioural units which comprise ‘sexual behaviour’, and due attention to controlling for the stimulus conditions in which it occurs, might facilitate our understanding of its general structure, and thus enhance our knowledge concerning the differential effects of various hormones. Beach suggests that both male and female brains have the appropriate neural substrates for homotypical and heterotypical sexual behaviour, and that sexual differentiation of the brain serves to alter the probability of a particular response being elicited in a given set of stimulus conditions. Thus, demasculinization does not eradicate the possibility of a male type response, it simply reduces its probability of occurrence. Figure 8.1 shows the critical period during which sexual differentiation of the brain occurs in rats. The degree to which the behaviour of the female rat is masculinized is dependent both on dosage and on timing of testosterone administration.

Figure 8.1 The effects of perinatal testosterone or castration on neonatal rats.

There is some interesting evidence from Dorner’s laboratories (Dorner, 1977, 1979) that human sexual behaviour may be affected by the prenatal hormonal environment. ‘An androgen deficiency in genetic males during a critical period of brain organization gives rise to predominantly female differentiation of the brain. This androgen deficiency in early life can be largely compensated by increased hypophyseal gonadotropin secretion in later life. Thus, the predominantly female-differentiated brain is post-pubertally activated by an approximately normal androgen level, leading to homosexual behaviour’ (Dorner, 1979, p. 87). The evidence from which this conclusion is derived comes partly from an experiment in which adult males were given an intravenous oestrogen injection: in homosexual males there was a subsequent rise in LH values above initial levels (a response which would be normal in females), whereas in bisexual and heterosexual males no such rise was detected. Goy and McEwen (1980) express some discomfiture with these data, and in particular point to evidence of time- dependent partial dissociation between the differentiation periods of central nervous centres regulating gonadotropin secretion and those responsible for sexual behaviour. However, Dorner (1977, 1979) clearly believes that the evidence of a relationship between prenatal hormones and adult sexual behaviour is now sufficiently strong to contra-indicate the prescribing of any androgenic or anti-androgenic substances to pregnant women, and recent data on females with CAH may tentatively support this view. In contrast to earlier findings which suggested that CAH females were no different from normal controls in their heterosexual interests and behaviour (Ehrhardt et al ., 1968a; Ehrhardt et a/., 19686) a more recent investigation by Money and Schwartz (1977) has suggested that early treated CAH females may be delayed in establishing dating and romantic interests. In addition, they found that in their sexual fantasies CAH females showed an increased rate of awareness of bisexuality relative to controls (although this did not necessarily reflect actual experience). It is plausible that these more recent data reflect a less prescriptive social climate than that which prevailed during the early 1960s when the original data were presumably collected, and one can only conclude that the nature of the biological, cognitive and social factors which regulate human sexual behaviour are by no means well established. This area remains wide open to debate.

(ii) Non-sexual behaviour

The effects of pre- and perinatal hormones on animals are not restricted to endocrinology and sexual behaviour. Levine (1966) cites evidence which demonstrates that female rats who have been injected as neonates with testosterone show male-type behavioural responses in an open field; and that female rhesus monkeys injected with testosterone in utero show levels of rough and tumble play which are approximately equivalent to those of normal male monkeys. Goy (1968, 1970) reports that initiation of play and pursuit play are greater in neonatally androgenized female monkeys than in normal females, and a number of workers have reported effects of neonatal hormones on activity (Gray et al ., 1975; Stewart et al ., 1975), exploration (Quadagno et al ., 1972; Gummow, 1975), and learning (Beatty and Beatty, 1970; Dawson, 1972; Dawson et al ., 1973). Quadagno et al. (1977) have reviewed the extensive literature on the effects of perinatal hormones on non-sexual behaviours with particular reference to energy expenditure, maternalism and learning, and they are able to conclude that the effects of early hormones on the behaviour of infrahuman species are well established.

McEwen (1976) and Goy and McEwen (1980) describe the experimental data which have led to the identification of specific neural pathways that are established by the influence of sex hormones and are sexually differentiated, and which underlie sex differences in behaviour. The work of Raisman and Field (1973) represented an important breakthrough in this field: they found that adult female rats have more dendritic spine connections in the preoptic area than males, but that males castrated within 12 hours of birth have spine connections equivalent *o those of the female. They demonstrated that those animals which show frequerd lordosis have different patterns of synaptic connectivity than animals with a limited capacity for lordosis. Various other studies have also shown that the brain of a male rat deprived of androgen and the female exposed to androgen will take on heterotypical characteristics: for example, the size of the cell nuclei in the preoptic area is positively correlated with the degree of lemaleness’ in the rat’s sexual behaviour (Dorner and Staudt, 1968, 1969); both serotonin levels (Ladosky and Gaziri, 1971) and RNA metabolism (Clayton et al ., 1970) are also affected. Litteria and Thorner (1974) and Phillips and Deol (1973) report sex differences in the cerebellum and septum which can be reversed by the presence or absence of androgens. However, even if these differences do indeed underlie the observed differences in behaviour (as seems plausible) and we assume that similar mechanisms of differentiation occur in humans, it is nonetheless unlikely that human behaviour would be so strongly determined by neural networks (particularly in the face of conflicting socialization).

Hormonal anomalies in human development

The data from the above animal studies provide sufficient evidence for the assertion that hormones are critical in determining patterns of brain differentiation, and suggest that pre- and perinatal hormones may also exert long-term effects on behaviour patterns. It is instructive then, to consider the effects of early hormones on human behaviour insofar as this can be achieved within the limitations of ethical considerations (see Reinisch and Gandelman (1978) for an interesting discussion of these issues). It has already been noted that prenatal hormones affect the development of sex-typical physical characteristics, and individuals with anomalous genital development at birth, or who present with related problems at puberty (e.g. amenorrhea in patients with testicular feminization), have been studied by psychologists interested in the possible effects on hormones on behaviour.

Two clinical syndromes can be regarded as close counterparts of experimental anti-androgenization (or demasculinization) in animals: Turner’s syndrome and testicular feminization due to androgen insensitivity. In Turner’s syndrome the missing chromosome may be either an X or a Y, and if a few androgen-secreting cells remain in the gonadal streak tissue there may be a mild degree of labial fusion and an enlarged clitoris. Some individuals have a 45X/45XY mosaic karyotype: they have testes, but these are not properly formed and are at high risk for cancer (Money, 1911b). Thus, deandrogenization in Turner’s syndrome is due to a failure of the gonads to manufacture androgens; in contrast, other testicular feminization syndromes are a result of the failure of the target organ cells to take up and utilize the androgens which are secreted from testes in foetuses with the normal 46XY karyotype.

The behaviour of girls and women with either Turner’s syndrome or testicular feminization is unequivocally feminine. In the case of Turner’s syndrome there seems even to be a tendency of extreme conformity to female sex stereotypes: they are known to fight less, to be less athletic and to be more interested in personal adornment than control comparisons (Money and Ehrhardt, 1972); and Theilgaard (1972) reported that women with Turner’s syndrome preferred to wear very feminine-style clothing and jewellery. All but one of the 15 girls in the group studied by Money and Ehrhardt (1972) had played exclusively with dolls, and most of them expressed a very strong interest in maternalistic activities associated with child care. In their anticipation and imagery of romance and motherhood, Turner’s syndrome females were found to be no different from their control comparisons. From these data, one may infer that differentiation of a feminine gender role is not dependent on the presence of prenatal gonadal hormones, nor does it require the presence of a second X chromosome. Indeed, Money and Ehrhardt are prepared to assert that ‘a feminine gender identity can differentiate very effectively without any help from prenatal gonadal hormones that might influence the brain and perhaps, in fact, all the more effectively in their absence’ (p. 108).

Babies born with the testicular feminization syndrome look like absolutely normal females, although these females tend to be of above average height (Money, Ehrhardt and Masica (1968) quote a mean height of 5 feet 1\ inches for their sample of ten patients). Diagnosis of their condition normally follows referral for primary amenorrhea so data regarding behaviour in early childhood are necessarily based on retrospective report (which may be influenced by knowledge of their condition). Even with this caveat in mind the data reported by Money et al (1968) and Money and Ehrhardt (1972) do seem to provide strong evidence for the unequivocal differentiation of female gender role in these patients. They reported playing primarily with dolls in early childhood and having dreams and fantasies which reflected the normal sex-role stereotypes of marriage and motherhood. With one exception these women rated themselves as fully content with the female role, and at adolescence they conformed with the normal patterns of heterosexual behaviour. Most of them expressed positive enjoyment in adopting ‘feminine’ styles of dress and personal adornment. ‘Babies with the androgen insensitivity syndrome who are consistently reared as girls have no uncertainties about themselves as girls, women, wives, sexual partners, and mothers by adoption ... they grow to be womanly in their behaviour, in their erotic mental imagery, and in their self-perception, even when they know the medical terminology of their diagnosis’ (Money, 1977a, p. 262).

Reifenstein’s syndrome resembles that of complete androgen insensitivity except that there is partial masculinization of the genitalia during foetal life and the neonate is thus sometimes classified as a male. At puberty the development of secondary sex characteristics nevertheless proceeds as described above. According to Money and Ogunro (1974) those infants assigned as males did not show any preference in childhood for female-type activities (doll play etc.) and made concerted efforts to compensate for their relative inferiority in athletic pursuits. At puberty, their breasts had to be surgically removed; in adulthood their physiognomy is beardless and unvirilized, and because of their extremely small, surgically repaired genitalia they may encounter some difficulty establishing a sex life (none reported homosexual preference). On the whole, gender identity conforms with socialization and there seems to be no evidence from these cases of any biologically based behavioural imperative for feminization. These cases may reflect the experimentally induced ‘demasculinization’ without accompanying ‘feminization’; and as far as we can tell from these few cases the social environment is a paramount factor in influencing preferred activity and gender identity.

The form of male pseudohermaphroditism described by Imperato-McGinley et al (1974) results from a 5a-reductase deficiency which leads to incomplete differentiation of the external genitalia at birth, and thus a female sex assignment is often made. At puberty, however, differentiation of male characteristics occurs and sex re-assignment is necessary. A recent report by Savage et al (1980) confirms the rather surprising finding that this gender-role transition is made relatively easily and they conclude ‘... that exposure of the brain to androgens during foetal life and thereafter appears to have had more effect on determining gender identity than the pre-pubertal sex of rearing’ (p. 404).

In the light of this conclusion it is interesting to consider the effects of the masculinization of a female foetus. These have been documented in two clinical syndromes: progestin-induced hermaphroditism (PIH) and the adrenogenital syndrome (CAH). PIH occurred following the administration of synthetic progestins to pregnant mothers with histories of miscarriage; these steroids were devised as substitutes for the pregnancy hormone, progesterone, but because their chemical structure was similar to androgen, they exerted an unexpected masculinizing effect on a female foetus (Walker and Money, 1972). Once this effect was discovered (in the early 1950s) the use of these hormones was discontinued; however, the subsequent development of girls born with PIH has been studied (Ehrhardt and Money, 1967; Money and Ehrhardt, 1972). If the external genitalia were surgically feminized shortly after birth, no further surgical or hormonal treatment was required; this is in contrast to girls born with CAH who require constant maintenance on cortisone to prevent continuing postnatal masculinization and accelerated pubertal development. Table 8.1 summarizes some of the data obtained on the reported behaviour of these cases. Basically, there is little difference between that of the PIH and CAH girls, but both these groups differ significantly from control comparisons on measures of tomboyism, athletic skills and preference for boys’ toys (e.g. cars, guns etc.). Perhaps, as a result of these interests, it is not surprising that these girls also prefer male playmates.

Table 8.1 Behavioural effects of prenatal exposure to androgens*

Childhood behaviour

PIH

CAH

Tomboyism

above average

above average

Athletic interests and skills

above average

above average

Preference for male playmates

above average

above average

Preference for ‘functional’ clothing

above average

above average

Preference for toy cars, guns etc. over dolls

above average

above average

Anticipation of future

Priority of career over marriage

above average

above average

Heterosexual romanticism

normal

normal

Anticipation of pregnancy

normal

Less frequently reported than controls

Dissatisfaction with female role

no

no

Sexual behaviour

Childhood-shared genital play/copulation play

normal

normal

Adolescent boyfriend and dating

normal

normal

Bisexual/homosexual fantasy

(data not available)

above average

Bisexual/homosexual behaviour

no

within normal range

Data adapted from Ehrhardt (1977); Ehrhardt and Baker (1974); Epstein and Money (1968); Ehrhardt and Money (1967); Money and Ehrhardt (1972); Money and Schwartz (1977).

The accuracy of assessment of behaviour in these cases is difficult to evaluate and Ehrhardt and Baker (1974) are clearly aware of this when they discuss, in some detail, exactly how the interviews with patients and their parents were conducted. It is important to be aware'that no observations were made of the children and that reliability was assessed purely in terms of the concordance between the mother’s and child’s reports. Even so, these data do seem to reflect a tendency for increased activity in females who have been exposed to abnormally high levels of androgen in utero ; and compatible with these tomboyish interests, these girls also seem less interested than control comparisons in personal adornment and maternal behaviours. Their gender identity is nonetheless entirely female (although 35% of them said they would not mind being a boy).

It appears then, that the effect of prenatal androgens on gender identity cannot be as imperative as Imperato-McGinley et al. (1974) and Savage et al (1980) suggest; it is more likely that the activational effects of circulating male hormones at adolescence are crucial to the satisfactory transition to the male gender role for these male pseudo-hermaphrodites. However, the surmise that the behavioural development of CAH and PIH females is in some way analogous to that of prenatally androgenized monkeys (Goy, 1968) is certainly supported by the available data. Furthermore, it is interesting to note that whilst the excess of androgens may be contributing to a masculinizing effect on some behaviours it does not have a global ‘defeminizing’ effect. Indeed, a sample of late-treated CAH patients described by Ehrhardt, Evers and Money (1968) conform strongly to female sex stereotypes in their careers and/or marriages. In fact, the influence of prenatal androgen exposure is probably limited to a specific effect which in some way creates a predilection for physical energy expenditure; associated preferences for functional clothing and male playmates may be no more than a reflection of this basic trait. This conclusion is confirmed to some extent by the finding that males with CAH are no different from a comparison group of unaffected male siblings except that they are more frequently (80 % of CAH males: 20% sibs) reported to engage in intense energy expenditure (Ehrhardt and Baker, 1975).

In two studies (Zussman et al. (1975) cited in Goy and McEwen, 1980; Ehrhardt et al, 1975) which considered the effects of prenatal progesterone on childhood behaviour (not the androgenic progestins which caused PIH), subjects were found to exhibit lower energy levels and a tendency to prefer ‘female type’ clothing styles. They suggest that non-androgenic progestins may actively counteract androgen effects in utero in both males and females.

During childhood, then, the major behavioural effect of prenatal androgenic hormones is on activity level: when the foetus has been exposed to androgen, he/she will subsequently display a predilection for high levels of physical energy expenditure (and these effects appear to be dose-related). These results are consonant with the findings on the effects of androgens in rodents and primates (Quadagno et al , 1977), and they do suggest that these hormones have an organizing effect on brain differentiation which will usually be sexually dimorphic.

Personality

Reinisch (1977) argues that prenatal exposure to (non-androgenic) progestin also has long-term effects on personality, and her data confirm the earlier suggestions of Ehrhardt and Money (1967) that progestin-exposed subjects show high levels of self-assertive independence and self-reliance. Twenty-six subjects, whose mothers had been administered a minimum dosage of 40 mg progestin for at least four weeks during the first trimester of pregnancy, were tested on age-appropriate Cattell Personality Questionnaires. They exhibited high scores on individualistic, self-assured and self-sufficient factors relative to sibling controls. In contrast, subjects exposed to high oestrogen levels in utero were found to be more group-dependent and group-oriented than a sibling control group.

An investigation by Yalom, Green and Fisk (1973) also attempted to evaluate the long-term effects of prenatal oestrogens on personality. Because diabetic women produce lowered levels of oestrogen and progesterone during pregnancy they are sometimes prescribed supplemental doses of these hormones; Yalom et al. studied the male children of diabetic mothers who had received high oestrogen doses, and compared them to a control group of children with normal mothers and a group of children of untreated diabetic mothers. At the age of 6 the boys who had been exposed to the highest levels of oestrogen were rated by their teachers as being less assertive and less athletic than their male peers. By the age of 16 a whole range of behaviours seemed to be related (albeit weakly) to the level of oestrogen exposure: athletic coordination, competitiveness, assertiveness, aggression, and global measures of ‘masculinity’. The children of diabetic mothers who had not received oestrogen supplements were consistently more masculinized than the control group of sons of normal mothers, and the children of mothers who had received supplemental oestrogen were the least masculine. It is possible that some of these effects may be due to differing levels of activational hormones in these boys since the development of the testes and output of testicular hormones are likely to have been affected (Zondek and Zondek, 1974).

Cognitive ability

In an exhaustive review of psychological sex differences, Maccoby and Jacklin (1974) concluded that males show superior visuo-spatial and mathematical abilities relative to females. Females though, are better at some verbal skills: they are more fluent, they are better readers and spellers, and their speech is more comprehensible than that of males (Harris, 1977). The extent to which these differences reflect underlying differences in neural organization has been a matter of considerable debate (Archer, 1976) since the influence of differential socialization in the development of sex-typed abilities is difficult to evaluate. Males and females show similar rates of early babbling (Moss, 1967; Lewis, 1972), but by six months of age girls receive more physical, visual and vocal contact with their mothers (Goldberg and Lewis, 1969; Messer and Lewis, 1972). Infant boys are encouraged more than girls to explore and to be independent of their mothers (Baumrind and Black, 1967; Hoffman, 1972). McGuinness (1976) argues convincingly that sex differences in cognitive abilities may develop from fundamental differences in auditory and visual acuity—from an early age females show lower auditory thresholds and superior pitch discrimination compared to males, and the sex difference increases with higher frequencies and with age (McGuinness, 1972); males have superior foveal vision, greater sensitivity to light and longer photopic persistence.

The aspect of spatial ability in which males most consistently excel is the capacity to rotate mentally three-dimensional images, or to redefine visual images into new planes; males thus perform better on mathematical problems which require spatial visualization (Fennema and Sherman, 1977; Petersen, 1979) and which involve the ability to ‘break set’ and restructure (Garai and Scheinfeld, 1968; Hutt, 1972a, b). Until adolescence, the majority of studies show no sex differences in quantitative skills, but males move ahead after this point and show consistently superior performance (Maccoby and Jacklin, 1974).

If these sex differences in cognitive abilities are subserved by the neural organizing effects of androgens in utero, a sample of females exposed prenatally to androgen would be expected to show a male pattern of abilities. Similarly, if enhanced oestrogen levels affect the neural substrates of verbal behaviour then males exposed to supplemental oestrogen in utero would show a female pattern of abilities. In fact, neither of these hypotheses is substantiated by the available data.

Ehrhardt and Money (1967) report identical mean verbal and performance IQ scores for a PIH sample of ten females (mean verbal IQ = 125, s.d. = 11.4; mean performance IQ = 125, s.d. = 12.5). Although Perlman (1971) (cited in Reinisch et al., 1979, and in Baker and Ehrhardt, 1974) found that CAH girls performed significantly lower than their matched controls on Verbal and Comprehension sub-tests of the Wechsler IQ scale, they also scored lower on Block Design. However, the scores of CAH girls on the Healy Pictorial Completion Test were comparable to those of CAH and normal boys; Perlman suggests that this result may reflect the higher activity levels of the CAH girls which would have made them more familiar with the kinds of situations depicted on the test. Baker and Ehrhardt (1974) report no statistically significant difference on perceptual or verbal factors between AGS patients and sibling control comparisons, although the trends were in the expected direction (i.e. CAH females performed slightly less well on the verbal sub-tests of the WISC than their unaffected female siblings, but slightly better on the perceptual sub-tests).

Curiously, patients exposed to prenatal androgen do seem to have above average IQ scores, but close examination of the relevant data reveal this finding to be due to factors other than the androgenic influence. Baker and Ehrhardt (1974) tentatively suggest that the recessive genetic trait for CAH may somehow be linked to another trait which favours postnatal intellectual development, and this notion is supported by the finding that the IQ levels of CAH patients do not differ significantly from those of their parents and siblings which are also higher than normal. The elevated IQ of the PIH group (Ehrhardt and Money, 1967) can be ascribed to social class factors among the parents: six of the nine families involved in this study had at least one parent who was a college graduate. Thus, there is no substantial evidence to link prenatal androgens with enhanced IQ scores.

Dalton (1968, 1976) suggested that prenatal progesterone (not of the androgenic type) increased intellectual achievement, but these data were not replicated in a study reported by Reinisch and Karow (1977) and have been discredited on statistical and theoretical grounds (Lynch et al ., 1978; Lynch and Mychalkiw, 1978).

The only study to consider the effects of prenatal oestrogen on cognitive ability is that of Yalom et al. (1973). These (male) subjects were administered the Embedded Figures Test to evaluate their spatial ability: those boys who had been exposed to supplemental oestrogen in utero showed slightly inferior performance relative to the two comparison groups, but this result did not reach statistical significance.

Other hormonally anomalous clinical conditions in no way implicate the role of prenatal hormones in determining the future patterns of intellectual abilities. Patients with testicular feminization show the typical female pattern of lower spatial than verbal ability: in the study reported by Masica et al. (1969) a sample of fifteen cases had a mean Wechsler verbal score of 111.8 and a mean performance score of 102.3. Since their exposure both to hormones and socialization is equivalent to that of genetic females, one can conclude from these data simply that superior male visuo-spatial abilities are not genetically determined from a locus on the Y chromosomes. For some time it was thought that spatial ability was partly determined by a locus on an X-linked gene (O’Connor, 1943; Stafford, 1961), but recent data indicate that the pattern of spatial abilities within familial groups is better explained by a model of an autosomal dominant gene which has reduced penetrance in females (Fain, 1976, cited in Vandenberg and Kuse, 1979). Whether this mechanism might influence brain differentiation must be purely speculative, and there is, as yet, no evidence to this effect.

Turner’s syndrome females have IQ scores within the normal range (Money, 1964; Shaffer, 1962), but also tend to show specific deficiencies in spatial ability. Shaffer (1962) quotes a mean verbal IQ of 106, but a mean performance IQ of 88.

Alexander, Ehrhardt and Money (1966) showed that Turner’s syndrome females experienced great difficulty on a visual memory test which requires the reproduction of angulated shapes, and Theilgaard (1972) reported that they performed badly on an embedded figures task.

It is reasonable to speculate from these data that androgens play some role in facilitating spatial ability. Since Turner’s syndrome females produce no androgens, and testicular feminized patients are insensitive to their effects, spatial ability is thus slightly impaired. In the oestrogen-exposed patients, the testes may have been producing less androgen than normal (Zondek and Zondek, 1974). The data from the CAH patients indicate that it is not the prenatal hormonal environment which is crucial, so the effect of androgens on spatial ability appears to be activational rather than organizing. This conclusion is supported by data from Petersen (1979) which indicate that females with androgynous somatic characteristics have better spatial ability than their more ‘feminine’ peers.

Similarly, the effect of oestrogens on verbal ability may also be an activational one. Dawson (1972) reports a study of West African males feminized by kwashiorkor-induced endocrine dysfunction. In severe cases of kwashiorkor the liver becomes unable to inactivate the normal amount of oestrogen which the male produces, and Dawson found that males with this condition had ‘significantly lower spatial ability and a more feminine field-dependent cognitive style than controls. In addition these subjects had significantly lower numerical and higher verbal ability compared to normal males’ (p. 24). Presumably though, these males had had equivalent gestational experiences to their controls and so the prenatal hormonal environment is not implicated in these results.

Sex differences in postnatal brain development

The human brain is not fully mature until around sixteen years of age. The main ‘growth spurt’ of the human brain begins during the last trimester of pregnancy and continues into the second year of life. During this period there is an increase in the number of glial cells (from which myelin is derived) and hypertrophy of all cells, specifically in the form of increased axonal terminal and dendritic branching (i.e. interneuronal connections). Most cortical areas are fully myelinated by the child’s third year but myelination of the reticular formation the cerebral commissure, and the intracortical association areas may continue into the second and third decades of life (Marshall, 1968).

Recent evidence suggests that sex differences in brain development are partly reflected in sex differences in hemispheric specialization (Hutt, 1979a; McGlone, 1980). For example, Witelson and Pallie (1973) in a study of infants up to 3 months old, reported that the increased size of the left (relative to the right) temporal planum (the posterior surface of the temporal lobe, including part of Wernicke’s area which subserves language) was significant in neonate females but not in males (although a significant difference was found for slightly older (20-90 days) males). Buffery and Gray (1972) cite evidence that in four-year-old girls the degree of myelination in the temporal planum is greater than that for four-year-old boys and they suggest that this may account for the female precocity in language development.

Witelson (1976) describes an experiment which suggests that in boys, the right hemisphere is specialized for spatial processing from as early as six years of age, whereas females show evidence of bilateral representation. She suggested that this specialization might subserve superior spatial skills in males. Levy (1969) postulated that bilateral representation of language in females could interfere with the development of spatial processing abilities in the right hemisphere— thus the cerebral organization which is presumed to give females an advantage in language development and verbal abilities may serve also to impede their development of spatial skills.

Waber (1976) has argued that lateralization is a function of maturation rate rather than sex. On the whole, girls mature faster than boys and generally display a greater tendency towards bilateral representation of skills. However, late-maturing adolescents of either sex are more likely to be strongly lateralized than their early-maturing peers, and are also more likely to show evidence of superior spatial skills.

The evidence for the existence of anatomical substrates which would underlie lateralization processes is both limited and confusing. For example, Wada et al (1975) did not replicate Witelson and Pallie’s (1973) findings on sex differences in cerebral asymmetry in infants: they report that both male and female infants tend to have a larger temporal planum in the left hemisphere than in the right, yet adult females are more likely than males to show the reverse pattern of asymmetry. It is possible that the anatomical asymmetry reported for adult females is a reflection of the greater plasticity of localization of function in females than in males. In a recent report (Hughes et al , 1980), females performed faster on a task which had both a verbal and a visuo-spatial component, whereas both sexes performed at the same speed on the verbal task alone. The authors interpret this finding as reflecting the ability of females to process both aspects of the task in one hemisphere; in males additional time is needed to complete the combined task because information has to be transferred between hemispheres. However, this sort of speculation awaits support or rebuttal from further anatomical evidence.

The ontogeny of hemispheric specialization and lateralization is simply not yet adequately charted. It is not known whether (or how) the environment might modify lateralization and thus we cannot know whether the data of Wada et al. (1975) from adult females are the result of endogenous, hormonally-mediated, changes or a reflection of educational experience. Tomlinson-Keasey and Kelly (1979) report that lack of early hemispheric specialization is predictive of better reading skills, and that right hemisphere specialization is positively associated with mathematical skills —data which confirm stereotypic achievements (i.e. females tend to be less lateralized and are better readers, males show a greater tendency towards lateralization of spatial skills in the right hemisphere and are better at mathematics). However, the nature of these relationships needs to be carefully explored.

Witelson (1977) argues that the functional neural substrates for the lateralization of particular abilities may show a plasticity during development which is lost in adulthood, and that this plasticity may reflect a susceptibility to environmental influences. However, experimental support for such an idea is still thin. It may be that lateralization predisposes cognitive strategies and atten- tional biases rather than specific skills. The female precocity in language development leads to a preferential use of language as a processing mode and consequent inferior performance in visuo-spatial skills (McGlone and Kertesz, 1973). Bryden (1979) offers a review of experimental data which serve as a useful reminder that sex differences in cerebral organization are not clearly defined: the degree of overlap between the sexes is often substantial, and seems to vary as a function of the experimental paradigm.

How different are sex differences?

It is easy to fall into the habit of discussing sex differences in ability and behaviour as though these represented absolute differences between two quite distinct populations. A sex difference in mean scores on a particular ability tends to deflect our attention from the within-group variances which indicate how much the groups overlap. Even when there is a statistically significant difference between the mean scores of males and females on a test the majority of both sexes may score within the same range.

The interpretation of a report of sex differences will depend on whether one is concerned with socio-political/practical issues (in which case differences are often trivial and meaningless) or with scientific/theoretic issues (in which case small but consistent differences may yield important insights). Thus, consistent reports of sex differences in verbal and visuo-spatial skills have raised interesting hypotheses both about hemispheric specialization, and the role of prenatal hormones; they do not, of course, provide any justification for boys to do badly when studying modern languages or for girls to abandon mathematics education at the earliest possible opportunity.

It may be that sex differences in certain skills are a result of long-term evolutionary pressures. For example, Hutt (1972 b) argued that athletic and visuo-spatial skills in males maximize hunting success and thus increase the probability of survival, whereas the socially communicative abilities and superior manual dexterity of the females have evolved as an adaptive consequence of her predominantly nurturant role in caring for dependent infants. Yet characteristics with a presumed evolutionary adaptive basis are not fixed for every individual: cultural pressures will influence the expression of abilities, and ‘typical’ sex differences are simply not found in some cultures. For example, cross-cultural studies of field-independence (presumed to be related to visuo- spatial skills) reveal no sex differences in Eskimo and Zambian cultures (MacArthur, 1967; Siann, 1972). McGuinness (1976) argues that \ .. the fact that boys do learn to read and write fluently, suggests that though initial processes may be guided by certain sensory differences, there is no reason to assume that these differences must remain. Parents insist that boys learn to speak, read and write but no such insistence induces the females to learn about spatial- mechanical relationships’ (p. 144).

In our own culture then, there is an attempt to educate males in heterotypical skills whereas the converse is not true for females. Even in homes where parents believe that they do not discriminate between male and female children Rheingold and Cook (1975) found that \ .. the rooms of boys contained more animal furnishings, more educational art materials, more spatio-temporal toys, more sports equipment and more toy animals. The rooms of girls contained more dolls, more floral furnishings, and more “ruffles’” (p. 461). The agents of socialization are evidently insidious, and may tend to exaggerate sex differences in proclivities for particular forms of behaviour. Even if we accept that evolutionary pressures have resulted in sex differences in neural organization which may differentially predispose males and females to specific abilities, we must stand this against our knowledge that the plasticity of the human brain will probably enable us to modify the expression of those abilities. This in turn implies a responsibility of educators and caretakers to provide an appropriate range of educational opportunities and role exemplars for their male and female charges.

At present, not only are females less likely to be given the wide range of toys that males have, their role is also under-represented by the literature and television media: \ .. females were under-represented in the titles, central roles, pictures, and stories of every sample of books we examined ... Even when women can be found in books, they often play insignificant roles, remaining both inconspicuous and nameless’ (Weitzman et al ., 1972). Sternglanz and Serbin (1974) made a study of T.Y. programmes with high popularity ratings, and found that half of these programmes did not portray any female roles: of those that did, the authors comment ‘female children are taught that almost the only way to be a successful human being if you are a female is through the use of magic’ (p. 714). Exposed to these kinds of socialization pressures it comes as little surprise that females tend to be diffident about their own ability and are particularly unwilling to tackle those skills which they perceive as falling within the male domain (Hutt, 1979b; Byrne, 1978).

Socialization experiences in our culture thus tend to exaggerate a dichotomy of roles and abilities between males and females. Historically, this socialization has acted to repress the female more than the male (her rights to be educated and to vote have, after all, been won only comparatively recently), but there is little doubt that a deliberate educational policy could serve to increase the range of both male and female behaviour. Goy and McEwen (1980, pp. 60-61) present some interesting evidence that female attachment to an infant may be innate (its expression being in part activated by elevated hormonal levels during pregnancy and birth), whereas male attachment is socially learned. This in no way implies that males are unable adequately to perform parenting behaviours, but its expression may be subserved by different neural mechanisms. There is no reason to believe that the expression of sex typical intellectual abilities is any less modifiable.

Towards a model of human sex differences

Waddington’s (1957) notion of‘canalization’ in an epigenetic landscape provides a useful conceptualization for understanding differences in the degree of sexual dimorphism in behaviour. Waddington suggested that, for all members of a species, a set of target physical characteristics (eyes, arms, legs etc.) is defined by the genotype and, despite underlying genetic variability, genetic processes operate together to ensure that these targets are achieved. He depicts the development pathways of the phenotype as a ball rolling through a set of valleys (the epigenetic landscape); the valleys can vary in steepness and thus vary the opportunity of the phenotype to deviate from a given course—-the steepness of the valley reflects the degree of canalization. At certain critical points in development, when the phenotype is undergoing rapid change, it is susceptible to certain environmental or genetically induced stresses. For example, the embryological development of the arms takes place around 38-48 days (postmenstrual); this development is strongly canalized (i.e. all normal humans have arms) but a teratogen, such as thalidomide, taken by the mother during this critical period will inhibit this normal phenotypic development and the foetus will eventually be born either with no arms at all or severe under-development (see Fishbein, 1976, pp. 46-47). The development of some other physical characteristics may also be affected by thalidomide during this period, but in general each character has its own critical period.

As we noted earlier, the basic developmental trend of the body’s sexual characteristics is in a direction corresponding to that of the homozygous sex (i.e. the female). This trend is canalized to develop a female foetus from the zygote which is formed at conception. However, if the embryonic gonad differentiates to form a testis, then phenotypic development is deflected from the female pathway when the testis begins to secrete MIS and androgens. Differentiation of neural networks occurs in the same manner: there will be critical periods when the presence or absence of biochemical agents (usually hormones) will affect the development of RNA which is specific to particular structures. Behaviours which depend on these specific neural anlagen for their expression will subsequently be affected. The specificity of hormonal effects is well illustrated by some data presented by Short (1979): certain aspects of male-type sexual behaviour were exhibited by ewes which were androgenized late during gestation (days 50-100, or 70-120) and had essentially female external genitalia; androgenization during early gestation (days 30-80) resulted in complete masculinization of the external genitalia which was not accompanied by male type sexual behaviour. Masculinization of urination behaviour could be effected by androgenization at a relatively late period of gestation after it was no longer possible to masculinize sexual behaviour. The positive feedback effect of oestrogen on LH, which is normally exhibited only as a female characteristic, was sometimes abolished by androgenization but ‘gave no clue whatsoever to the type of sexual behaviour to expect from the animal’ (p. 258). This example illustrates clearly that the degree of masculinization of behaviour cannot be inferred from physical characteristics. The developmental pathways for specific behaviour patterns are also independent of one another, so the masculinization of sexual behaviour does not necessarily imply masculinization of activity levels.

If we return to the image of males and females rolling through their (sometimes overlapping) epigenetic landscapes, it is possible to visualize the way in which different levels of canalization will result in different degrees of sexual dimorphism in the eventual expression of behaviour. If the pathway for a particular neural substrate is very steep, it will be difficult to deflect the phenotype from its developmental path—thus most genetic females will manifest the appropriate ‘female’ behaviour pattern and most males will not. If the pathways are gentle then the phenotypes may be spread more thinly, and a linear male-female dimension may be evident in the subsequent behavioural pattern. The neural mechanism which mediates gonadotropin release is clearly strongly canalized, other neural substrates in humans are less strongly canalized and therefore enable the expression of greater variability in behaviour and skills.

The critical periods for development of the neural networks which underlie particular behaviours may vary in length; they may overlap in time, but they are independent of one another. Thus, in the female rat, by the judicious administration of neonatal testosterone, it is possible to decrease the incidence of lordosis but not to increase the incidence of mounting. Armstrong’s attempt (cited in Jost, 1974) to relate sexual orientation to body type is therefore quite misconceived: there is no reason to believe the homosexuals will have heterotypical body characteristics.

There are three ways in which hormones can act on the brain to produce sex- differentiated effects. The prenatal hormones organize neural networks in distinctively male and female patterns; they also have a critical role in the development of physical characteristics. Postnatally, the output of gonadotropic hormones can activate these neural networks (for example, in the control of the menstrual cycle). Alternatively, sex-related hormones may have independent effects: an example of this is the yawning behaviour of rhesus monkeys which is normally displayed more frequently by males than by females, but which can be increased in the female by the administration of exogenous testosterone (Goy and McEwen, 1980).

In humans, evolution has operated to permit a high degree of behavioural phenotypic plasticity, which would in turn imply weak canalization of the neural mechanisms which subserve particular behaviours and abilities. (This may account for the conflicting findings in anatomical studies of hemispheric asymmetry, supra). This phenotypic plasticity enables individuals with very different genotypes to exhibit similar or identical behaviour. In the expression of human behaviour and ability then, phenotypic plasticity and not biological canalization may produce conformity of behaviour within a same-sex group. Evidence for sexually differentiated canalization of a particular behaviour requires that its manifestation be virtually universal and not restricted to a single cultural group: the only behaviours which fulfil this stringent requirement are indeed ‘menstruation, gestation and lactation’ in females and ‘impregnation’ by males. The weaker canalization of sex-related brain differentiation in humans relative to infra-human species would also lead us to expect less sexual dimorphism of behaviour in humans; this should always be borne in mind when extrapolating from animal to human studies. Rodent studies have been crucial in extending our knowledge of brain differentiation—they do not necessarily tell us much about human behaviour.

The identification of the brain areas and mechanisms which subserve particular behaviours or the articulation of specific cognitive skills in humans is by no means straightforward. Whilst it has been possible in infra-human species to identify the critical period of development for the expression of certain behaviours (vide Short, 1979) this has not been possible in humans and probably (for ethical reasons) never will be. Nor is it entirely clear how circulating hormones affect human behaviour: studies of the menstrual cycle produce conflicting evidence (Hutt et al ., 1980), and studies of sexual behaviour (e.g. Bancroft and Stakkebaek, 1979) or cognitive ability (Peterson, 1979) have not yielded definitive conclusions. We also lack evidence on the way in which educational experience affects brain development. Thus, information which is vital to a definitive model of the effects of brain differentiation on psychological sex differences is not available. Nonetheless, the existing evidence leaves no doubt that brains of males and females differ as a function both of the prenatal environment and subsequent maturational effects. These differences may well underlie the predilection for males and females to act in particular ways, but they cannot be seen as constituting a biological imperative.

Summary

De facto sex differences in ability and behaviour are not as dimorphic as sex differences in physical characteristics. The major influences on sex differential brain development are the sex steroids (androgens, oestrogens and progestins), but their effect on behaviour is attenuated by the weak canalization of the human behavioural repertoire. Sexual differentiation of the brain may create predilections for particular behaviour and specific cognitive strategies, but it does not constitute a biological imperative for psychological sex differences.

Acknowledgements

I would like to thank Dr. J. E. Blundell and Professor J. Scott for their helpful comment and criticism during the preparation of this manuscript. I am also grateful to Derrick Pritchatt who translated the article by Reznikov (1978).

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

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