Biological maturation throws a monkey wrench into our concepts of sex differences

The most outstanding sex differences,  vaginas and penises for example,  are unequivocally sex-specific from before birth right on until death.  However,  more subtle sex differences may invert through development.  A few examples of these phenomena are the following.   The body size (height, weight) of the human male is greater, on the average, than that of the female.  However,  there is a brief period,  at puberty,  during which it is the average girl who is taller and heavier than the average boy.  We are accustomed to recognizing that girls reach puberty before boys do.  By extension,  we tend to generalize this obvious biological precocity of girls to the ensemble of psychological function and to think it applies to the whole of development up until puberty.  In other words, we tend to think that girls mature faster,  psychologically and biologically, than boys.  However, there are many exceptions to this rule.  Boys progress as fast as girls on many items of infant development scales, and there are even a few examples of tissues that develop faster in boys.   Even in terms of the development of reproductive functions,  in some respects,  it is the boy who matures faster.  An interesting such sex difference prevails,  in a sense,  in the early development of endocrine functions in the ovary and testis. The testis actively produces androgens already in utero whereas the physiologically important steroid hormone production of the ovary does not start until puberty. Likewise, several components of the hypothalamic-pituitary-gonadal axis seem to mature earlier in the male. The hormonal regulation of the fetal testes differs in many respects from that of the adult, and these differences make it possible for the fetal testes to function in the intrauterine endocrine milieu.

There are also twists and turns during development (probably not entirely biologically determined)  having to do with sexual identity and sexual orientation.  Girls manifest sexual orientation and identity earlier than boys.   But then boys catch up.  From adolescence to young adulthood,  females become slightly more psychologically androgynous,  while males become less so.  Then in mature adulthood and senescence, there is an inversion of this sex difference.  Men become slightly more psychologically androgynous, and women slightly less so !    One investigation was based on observation of a group of between 84 and 91 rhesus monkeys (macaques) in captivity  for 18 months. Submission was most frequent in juveniles (aged 1.5-3.5 yrs), but aggression increased steadily with age. As infants (aged 0.5-1.5 yrs), males were more often involved in agonistic (friendly) behavior than were females, but this sex difference reversed with age.   By adolescence,  the males manifested less «friendliness» and more aggressiveness.  In humans,  male infants have most often been found to be fussier,  more irritable than female infants.   This difference is believed by some to be wholly explainable by the greater incidence of inborn perinatal complications affecting the male sex.

Male and female monkeys do not recover from brain lesions in the same way.  A researcher named Patricia Goldman-Rakic lesioned the anterior area of the brain,  the frontal lobe, of fetal monkeys.   She found that the males manifested the cognitive deficits earlier than the females. One study found that the ability to perform on a concurrent visual discrimination task with 24 hour intertrial intervals develops a few weeks earlier in female than in male infant monkeys. To test whether this sex difference was related to the presence of perinatal androgens, plasma testosterone levels were reduced in male infant monkeys by neonatal orchiectomy (removal of testes) and increased in neonatally ovariectomized (removal of ovaries) female infant monkeys by treatment with either testosterone propionate or its reduced metabolite, dihydrotestosterone.   At 3 months of age, the animals were tested on the task and their performance compared with that of age-matched intact male and female monkeys. Orchiectomy which was followed by a slight but visible atrophy of the external genitalia, hastened performance of male infant monkeys to the level of intact infant females. Conversely, androgenization of ovariectomized female infant monkeys given dihydrotestosterone, which had only a slight virilizing effect on the external genitalia, slowed the learning of these female infants to the rate of intact male infant monkeys.  Other experimenters have found that adult rats from both sexes with frontal lesions were impaired on many tasks, but the males were much less impaired than the females on tasks which require animals to use multiple visual-spatial cues for a successful solution (maze navigation).  Another research group found that relative rates of development of the prefrontal cortices in either hemisphere inverse over time in rats,  and in some areas, these developmental inversions are opposite in males and females.  One team of researchers looked at dendritic spining (this would correspond, say,  approximately to the number of neuronal synapses per cubic millimeter of brain tissue) of the hippocampal dentate gyrus after environmental enrichment (lots of toys and play mates) or impoverishment (no toys or play mates) of equally fed juvenile rats of either sex.  They found that «cultural» enrichment in rats favored the development of more dendritic spines in the females than males.  In the next section,  we will see that there are numerous sex differences in the size of various brain nuclei,  and most of these sex differences remain rather constant throughout life.  However,  the development of any particular brain tissue depends on another type of cell,  namely glial cells.  It has been observed that at certain phases of prenatal brain development there are transient sex differences in glial cell counts in certain of these brain nuclei before they become sexually dimorphic,  but not after.   In fact,  these glial cell count differences probably reflect sex differences in neuronal maturation. 

All of these findings show that sex differences can change with development.  Changes in sex differences in intellectual ability over the life span have also been reported in humans.   For example,  the male advantage in spatial ability undergoes some gain at puberty,  not because the pubertal boy improves but because the adolescent girl actually undergoes a slight regression.  The interpretation of this particular phenomenon remains very controversial.   Finally, we will see in detail later that risk factors for certain neuropsychiatric disorders cross over from male preponderance to female preponderance from childhood to the post menopausal years.   These phenomena (the ones I am aware of anyway) are all hormonally mediated,  and our challenge will be to try to disentangle the various factors, biological and cultural, which cause these interesting cross-overs. 

Now it must not be forgotten that cross-over of sex differences during development remains the exception rather than the rule.  For example, metabolism is higher in human males throughout life.   Boys and men expend more energy per hour per square meter of body surface than girls and women do, having consumed an equal amount of calories. Men have more absolute muscle mass than women, and they have a higher proportion of muscle mass to fat.  The higher male metabolism is associated with this greater muscle mass and even precedes it in development.   There even exist parameters routinely observed in blood samples of normal people which are significantly different for the two sexes throughout life.  Such blood parameters are related to muscle mass and metabolic rate.  One of the most commonly used machines  for biochemical analysis of blood for medical diagnostics is built by the Coulter company. The company provides crude norms which clearly show a substantial sex difference in blood biochemistry.   Normal men have higher concentrations of hemoglobins, hematocrites and erythrocytes,  and greater average globular size   -all indicative of higher blood oxygen metabolism in the male sex.

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This sex difference seems to be mediated directly by sex hormones.  Indeed, the blood of 18 untreated transsexuals and 20 castrated or non-castrated transsexuals was investigated in one study.  The erythrocyte (red blood cell) counts were significantly higher in untreated males and treated female-to-male transsexuals than in untreated females and treated male-to-female transsexuals,  a finding perfectly compatible with that of St Marseille described above.  This apparently innocuous sex difference seems to have implications for health issues.  Indeed,  it has been found that these blood paramneters are related to blood pressure,  and hypertension in particular,  and it is well known that men are more at risk for hypertension than women -with the ensuing greater risk of men for more dangerous and deadly vascular diseases.  The study of blood parameters could be surprisingly relevant to the neuropsychology of cognitive function.  One recent study analyzed six distinct protein markers in blood serum of normal men and women who completed an episodic memory task.  Episodic memory is the recall of an episode (event) not destined to be memorized (such as what one ate for breakfast two days ago).   The serum markers and episodic memory performance strongly interacted with gender.