Endogenous testosterone levels

In the early seventies, determination of sex hormones using radioimmunoassays was established as a highly specific and reliable method. This enabled scientists to obtain quantitative data on circulating hormones in blood or saliva and to investigate the relationship of current sex steroids and cognitive abilities in normal, healthy subjects (Table 4.6). Komnenich et al. (1978) were the first to investigate healthy young women (n = 24) and men (n = 10). Four times within a month they measured the concentration of FSH, LH, testosterone, estradiol, and progesterone in plasma. On each of the days, simple repetitive tasks and a nonverbal test of field-independence were administered. Only the performance on the verbal tasks was positively related to estradiol in males. None of the other hormones exhibited a significant relationship to cognitive performance in men or women.

In a relatively large sample of 43 men between 20 and 40 years Shute etal. (1983) detected a distribution of visual-spatial test scores as a function of androgen levels with the best-fitting third-order polynomial function describing the curve. Shute et al. reported that normal males selected for low plasma androgens were superior on certain spatial tests, while in their sample of 48 females the reverse was true, that is, highest-androgen females were superior to low-androgen women. However, due to the high cross-reactivity of the antibody used in their radioimmunoassays the authors speak of "general androgen" level instead of free, non SHBG-bound testosterone, which they originally intended to measure. Gouchie and Kimura (1991) found an effect similar to that of Shute and co-workers, using not only the extremes of the group, but a simple median split to divide all subjects on the basis of saliva testosterone levels in normal men andwomen. For one of the two spatial tests (paper folding test) there is a significant sex-by-hormone level interaction, indicating that low levels of testosterone in males and high levels of testosterone in females are associated with superior performance. A composite score for tests on which males

Table 4.6 Serum and saliva androgens and cognitive abilities in normal males and females

Study

Cognitive task

Hormonal-cognitive relation

Komnenich etal. 1978

verbal

non-significant (m) (f)

visual-spatial

curvilinear (m+f)

visual-spatial

non-significant linear (m)

visual-spatial

positively linear (f)

Shute etal. 1983

visual spatial

curvilinear (m)

visual-spatial

positively linear (f)

Gordon and Lee 1986

visual-spatial

positively linear (m)

Christiansen and

visual-spatial

positively linear (m)

Knussmann 1987b

field-in dependence

positively linear (m)

verbal fluency

negatively linear (m)

McKeever and Deyo 1990

visual-spatial

positively linear (m)

Gouchie and Kimura 1991

visual-spatial (paper folding)

curvilinear (m+f)

visual-spatial (paper folding)

positively linear (f)

visual-spatial + mathematical

curvilinear (m+f)

reasoning

non-significant (m) (f)

verbal

non-significant (m) (f)

perceptual speed

Tan and AkgUn 1992

non-verbal

positively linear (m)

non-significant (f)

Christiansen 1993

tactual-spatial

positively linear (m)

field independence

positively linear (m)

verbal fluency

negatively linear (m)

Janowsky etal. 1998

spatial recall

positively linear (m)

verbal recall

positively linear (m)

visual-spatial

non-significant (m) (f)

Silverman etal. 1999

mental rotation

positively linear (m)

Davison and Susman 2001

mental rotation

positively linear (m) (f)

block design

positively linear (m)

verbal meaning

non-significant (m) (f)

m = males f = females m+f = mixed group of males and females m = males f = females m+f = mixed group of males and females normally excel (paper folding, mathematical reasoning, mental rotations) shows a similar relationship. On the other hand, multiple regression analyses of the male data alone revealed a trend in men for a positive linear relationship between saliva testosterone levels and visual spatial abilities (R = 0.29; p < 0.06). Gouchie and Kimura noted no evidence or consistent relationship between testosterone concentrations in men or women and their performance on perceptual speed tasks or vocabulary tests (at which females usually excel over males).

The interpretation of such findings is complicated by the fact that testosterone may exert some of its effects through aromatization to estradiol in the brain. The suggestion has been made that it may in fact be the estrogen level which is related in a curvilinear fashion to spatial ability (Nyborg 1988). However, his hypothesis of a correlationbetween circulating serum estradiol and cognitive functioning could not be supported by the only two studies which, in addition to testosterone, measured serum estradiol (Christiansen 1993; Shute etal. 1983).

In contrast to Shute etal. (1983) and Gouchie and Kimura (1991), several studies have shown a significant linear testosterone-cognitive relationship. Gordon and Lee (1986) investigated 32 men with four visual-spatial and four verbal tests and determined testosterone levels of their subjects. Testosterone concentrations correlated significantly positively with one spatial orientation task, but not with any of the other spatial or verbal tests. The study by Christiansen and Knussmann (1987b) attempted a broader investigation of the effects of androgens on spatial and non-spatial cognitive abilities in a larger sample of 117 men in their twenties. They collected blood and saliva samples to determine serum concentrations of testosterone, non SHBG-bound saliva testosterone, and 5a-dihydrotestosterone (DHT). Cognitive functioning was ascertained by 11 spatial and verbal ipsative test scores, reflecting intraindividual variance in the performance of these tasks, independent of the person's general level of achievement. The relationship between androgens and cognitive performance exhibited a clear pattern. All significant correlations between hormone values and verbal tests were negative. In contrast, significant correlations between androgens and spatial and field independence tests were all positive. Correspondingly, a more "masculine" cognitive pattern (superior skills on spatial tests as compared to verbal tests) was positively correlated to all three androgens. It should be noted that total serum testosterone clearly showed the greatest number of significant relations with verbal and spatial test scores. Three years later, McKeever and Deyo (1990) confirmed these findings of a positive correlation between androgen levels and spatial tasks with regard to DHT. Further evidence for a linear androgen-cognitive relationship comes from Tan and Akgtin (1992) who noted a positive correlation between nonverbal tasks and testosterone in a sample of Turkish university students. This was only the case for a subsample of right-handed men with right eye preference, but mixed-dominant males and young females showed no relationship. Janowsky et al. (1998) who investigated healthy male and female volunteers between 23-34 years of age with a comprehensive cognitive test battery found their male subjects with higher free testosterone levels excelled in verbal and spatial recall tasks, but spatial cognition (block design, card rotation) did not relate to salivary testosterone in males or females (compare Anderson et al.'s (1995) study involving boys at the onset of puberty). Nevertheless, recent studies confirm that visual-spatial abilities seem to have a rather stable relationship to endogenous testosterone levels in males, but also in females.

Silverman et al. (1999) measured salivary testosterone in men and found a general linear relationbetween individual differences in testosterone levels and performance on a three-dimensional mental rotation task. Davison and Susman (2001) tested boys and girls ranging in age from 9 to 14 years. Testosterone and estradiol were assessed at three test sessions every 6 months. The results showed positive relations between spatial scores and testosterone in boys at all three sessions and in girls at the third session. In addition, the data supported a link between longitudinal change in testosterone levels and longitudinal change in spatial performance in both girls and boys.

As all the previous data were collected from individuals living in Western cultures, Christiansen (1993) tried to validate the findings in a non-Western group of healthy males. Althogether 256 !Kung San hunter-gatherers ("bushmen") and Kavango farmers from Nambia (southern Africa) were investigated. They lived mainly on the subsistence level in their traditional lifestyle with a low degree of transition to Western culture. Testosterone, DHT, estradiol, and "free" salivary testosterone were determined. In order to make a sensible comparison of previous findings of hormone-related cognitive performance, spatial and verbal tests were the same or similar to those used in the study by Christiansen and Knussmann (1987b), but were adapted for testing of illiterate subjects with no experience in paper and pencil tasks. The African data yielded the same hormonal cognitive pattern as was found in Western samples. Total and salivary testosterone showed the greatest number of significant relationships, a positive one with visual- or tactual-spatial tasks and a negative association with verbal tests.

The summary of sex hormone effects on cognitive abilities makes it reasonable to conclude that testosterone plays a role in cognitive functioning throughout life -from the prenatal period through adulthood till old age. But it has to be noted that explanations of inter- and intraindividual differences in cognitive abilities are complex and any causal model will have to recognize the reciprocal effects that environment and biology have on each other.

4.8 Key messages

• The interaction of testosterone with behaviour is bidirectional: testosterone can influence behaviour, and behaviour can alter testosterone levels.

• Testosterone affects brain development by organizing certain brain regions during fetal and neonatal life. At puberty, these brain structures and hence the behavioural repertoire are thought to be activated with increasing sex hormone concentrations. However, in humans behaviour is predominantly determined by intrapsychic, social and cultural factors; hormonal influences are less powerful than in animals.

• Male sexual behaviour is related to androgens. It becomes overt and powerful in puberty when the testes begin to secrete androgens.

• In hypogonadal males testosterone replacement provides convincing evidence of its role in some aspects of sexual behaviour. In eugonadal males testosterone substitution has only very limited influence.

• Endogenous testosterone levels in eugonadal men may be positively correlated to sexual interest and frequency of orgasms, but the findings are contradictory.

• In women, correlational and experimental studies show that testosterone is associated with an enhancement of sexual behaviour.

• Due to the endocrine effects of sexual stimulation and activities, an increase in testosterone was observed in both sexes.

• Stress responses of the pituitary-gonadal axis show a remarkable sensibility. In males, testosterone levels decrease under psychosomatic and psychic stress, even under anticipation of stressful events, while testosterone concentrations in females rise.

• Compared to untrained men, well-trained athletes have lowered testosterone levels in a resting state.

• During and after prolonged submaximal exercise decreased testosterone levels in males and increased levels in females were measured. Acute effects of short exercise are a rise in testosterone concentrations, followed by a decline below baseline levels.

• Human aggression and endocrine activity are mutually dependant. Prenatal exposure to exogenous androgenic steroids results in slight increases of aggressive behaviour in boys and girls.

• Aggressive behaviour and self-report measures of aggression are predominantly positively correlated to endogenous testosterone levels in men and women although the aggressive act is generally removed in time from the hormone assessment.

• In both sexes, testosterone replacement therapy or anabolic steroid abuse can result in increased aggressiveness, but this effect is not universal.

Assertive or aggressive behaviour followed by a rise in status - even more so when associated with the person's elevated mood or elation - leads to a rise in testosterone levels.

• The relationship between mood and androgens is less clear. Neither clinical research on depressive men nor studies on mood and endogenous testosterone concentrations in normal males and females provided consistent results. However, early reports on castrates and studies involving mostly hypogonadal men and menopausal women described an improvement in emotional stability following treatment with testosterone.

• Androgens play a critical role in sex-typical cognitive functioning throughout life in normal men and women. Several studies have shown both linear and curvilinear effects of testosterone on visual-spatial abilities. Direct manipulation of testosterone supports the conclusion of its important role in cognition in females and males, predominantly positive effects on visual-spatial tasks, perceptual speed and memory.

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