Psychoneuroendocrinology, Vol. 16, No. 4, pp. 323-334, 1991
0306- 4530/91 $3.00 ÷ 0.00 @1991 Pergamon Press plc
Printed in Great Britain
THE RELATIONSHIP BETWEEN TESTOSTERONE LEVELS AND COGNITIVE ABILITY PATTERNS CATHERINE GOUCHIE and DOREEN KIMURA Department of Psychology, University of Western Ontario, London Ontario, Canada (Received 27 June 1990; in finalform 22 October 1990)
SUMMARY The cognitive performance of normal men and women was studied, grouped according to whether the subjects had relatively high or low salivary testosterone (T) concentrations. Men with lower T performed better than other groups on measures of spatial/mathematical ability, tasks at which men normally excel. Women with high T scored higher than low-T women on these same measures. T concentrations did not relate significantly to scores on tests that usually favor women or that do not typically show a sex difference. These results support suggestions of a nonlinear relationship between T concentrations and spatial ability, and demonstrate some task specificity in this respect.
INTRODUCTION WOMEN are reported to perform better than men, on average, on tasks involving verbal skill (e.g., verbal fluency), perceptual speed and fine manual dexterity, while men demonstrate superior visual-spatial ability, mathematical reasoning ability, and targeting (Maccoby & Jacklin, 1974; Wittig & Petersen, 1979; Harris, 1981; Harshman et al., 1983; Benbow, 1988; Watson & Kimura, 1991). There is evidence that some variation in cognitive performance is related to inter-individual differences in chronic levels of sex hormones. Though circadian and circannual rhythms in testosterone (T) levels exist (Nieschlag, 1974; Smals et al., 1976; Reinberg & Lagoguey, 1978), levels of T may be relatively constant after puberty. For example, plasma testosterone concentrations of 15 men in April of one year were strongly correlated with their T concentrations in April of the following year, suggesting that, even though there are seasonal fluctuations in levels, overall they remain quite stable (Smals et al., 1976). A few studies relating hormone concentrations to cognitive performance have inferred the hormone levels of their subjects from the degree of secondary sex characteristic development, which is under the influence of sex hormones (Tanner, 1975; Farthing et al., 1982). Others reported that physically androgynous subjects, whether male or female, performed better on spatial tests than more sex-typical subjects (Petersen, 1976; Berenbaum & Resnick, 1982; McKeever, 1986). The purported relationship between cognitive performance and sex hormone levels was strengthened by the work of Shute et al. (1983), who studied the spatial ability of normal male Address correspondence and reprint requests to: Dr. Doreen Kimura, Department of Psychology, University of Western Ontario, London, CANADA N6A 5C2. 323
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and female subjects in w h o m they also had measured plasma androgen concentrations. They selected, from 33 subjects, the six men and six women with highest androgen levels and the six men and six women with the lowest androgen levels. There was a significant sex by androgenlevel interaction in that low-androgen men performed better on spatial tests than high-androgen men, and high-androgen women were better than low-androgen women. This pattern of performance among groups suggests a nonlinear relationship between androgen levels and spatial ability. However, Shute et al. m a y not have distinguished between the effects of T and other androgens, since the antibody used in the radioimmunoassay was assumed to bind to other androgens biochemically similar to T. They also did not attempt to determine the relationship between androgens and non-spatial tests. The present study attempted a broader investigation of the effects of T levels on cognitive abilities, both spatial and nonspatial, and in larger samples o f both men and women. Each subject completed several cognitive and m o t o r tests that were c h o s e n because they were expected to favor either women or men. It was predicted that tests of abilities normally better in men would be influenced by T levels, at least in men. Further, if a curvilinear relationship exists between T levels and spatial ability, women with higher levels of T, and men with lower levels, would be expected to score higher on spatial tests. The same pattern might be predicted for scores on mathematical reasoning tests, given the strong sex difference favoring men in mathematical ability. T was not expected to influence the tasks at which women usually excel, such as perceptual speed and verbal articulation, or tasks which do not typically show sex differences, such as vocabulary. T concentrations were determined from saliva, since obtaining saliva samples is a less invasive procedure than drawing blood. Moreover, only free T (not bound to sex-hormone binding globulin) is present in saliva. It is assumed that only free T is biologically active and can be taken up and metabolized by target tissues, including the brain (Vermeulen & Verdonck, 1972). A high correlation between salivary T concentrations and total serum concentrations has been demonstrated (e.g., Baxendale et al., 1980: r=.81; Wang et al., 1981: r =.94). SUBJECTS AND METHODS
Subjects Eighty-eight right-handed volunteers (42 men, 46 women) were solicited through advertisements posted around the campus. They were predominantly undergraduates at the University of Western Ontario. The mean age of the men was 21.0 yr (range: 18-27 yr), and of the women was 21.5 yr (range: 18-31 yr). Fifteen of the 46 women and 13 of the 42 men were in a science program. The rest were in an arts or social science program. Subjects were paid for their participation in the study. They were not aware of the hypotheses being tested. Forty-eight (24 men, 24 women) of the subjects were participants in a two-phase study, which employed the same tests as those used here. Test results from the first phase of that study were therefore included here. T assays for these subjects were conducted separately from those for the second group of subjects (see below). Procedures Subjects were tested individually. At the beginning and end of the test session, they were asked to provide a 7-ml sample of saliva for radioimmunoassay determination of T concentrations. Subjects completed a battery of cognitive and motor tasks. Tests measuring abilities in which either a sex difference has previously been noted, or which were demonstrably sensitive to hormone fluctuations, were used. The tests included measures of spatial ability, perceptual speed, mathematical reasoning ability, and verbal-articulatory ability. A vocabulary test was employed as a measure of general intellectual level. Subjects also answered questions on their physical development and characteristics. These data will be presented elsewhere.
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Tests Most tests, with the exception of the tongue twister, were multiple-choice paper-and-pencil tests. A correction factor for guessing was used in the scoring of all multiple choice tests. Tests of spatial ability and mathematical ability were chosen as measures of skills typically performed better by men. Soatial Ability: Two tests of spatial ability were included - - Paper Folding and Mental Rotations. These tests were chosen because men have been reported to score higher than women on tests involving mental rotation or shape transformation (Vandenberg & Kuse, 1978; Sanders et al., 1982; Harshman et al., 1983). (1) For the Paper Folding test (Ekstrom et al., 1976), each item consisted of a series of pictures which illustrated a square piece of paper being folded and a hole being punched through. The subject had to determine where holes would appear once the paper was unfolded and to choose the appropriate representation from among five pictures. There are 10 items in this test, and 3 min are allowed for completion. Watson and Kimura (1991) reported a strong trend for men to do better on this test. (2) On the Mental Rotations Test (Vandenberg & Kuse, 1973, adaptation of the Shepard-Metzler test; Shepard & Metzler, 1971), the subject was presented with a two-dimensional representation of a three-dimensional, asymmetric set of cubes, and had to identify the same stimulus depicted as having rotated in space. There are four choices for each item, two of which are correct. Four minutes are allowed to complete the 12 items; the maximum possible score is 24. MathemaIi~al Ability: Mathematical ability was measured with the Mathematics Aptitude Test (Ekstrom et al., 1976), classified as a test of general reasoning. Ten minutes are allowed for the completion of 15 mathematical reasoning problems. Men are usually superior on mathematical reasoning tests (Benbow, 1988). Several tests of abilities on which men were not expected to excel were also included. In some of these tests, women were expected to do better than men, while in others, no sex difference was expected. Percentual Soeed: Two perceptual speed tests from the ETS kit of Factor-Referenced Cognitive Tests (Ekstrom et at., 1976) were administered, since a female advantage has been reported on several tests of perceptual speed (Maccoby & Jacklin, 1974; Harshman et al., 1983). (1) On the Finding A's test, subjects were given lists of words and had to cross out each word that contained the letter "a". The final score was the number of words crossed out in 2 min. (2) Identical Pictures test required the subject to choose the one of five choices which was identical to the stimulus figure. There are 48 items, with a time limit of 1.5 min. Verbal Articulation: Verbal articulation was measured by having the subject say a tongue twister as quickly as possible. The time was recorded for the criterion of five consecutive correct repetitions of the tongue twister "A box of mixed biscuits and a biscuit mixer." Though sex differences have not been reported on this particular test, it has been shown to be sensitive to fluctuations in exogenous estrogen (Kimura, 1989): Verbal articulation was enhanced when estrogen levels were higher. Vocabulary: The Advanced Vocabulary test (Ekstrom et al., 1976) was administered as a measure of general intellectual ability. The subject was asked to select, from among five alternatives, the word most similar in meaning to the stimulus word. There were 18 items. No sex difference or hormone effect was predicted for performance on this test. Radioimmunoassays Following completion of the study, T concentrations were determined from saliva samples collected at the beginning and end of the test session. Saliva production was stimulated by having subjects chew gum containing citric acid (Gatorgum). Samples were collected in borosilicate vials, frozen immediately after collection, and stored at -20 ° C until they were assayed. All samples were analyzed by the same technician at University of Michigan, Ann Arbor, though assays for the first 48 subjects were analyzed at different times and therefore by different kits from those for the final 40 subjects. A Coat-a-Count kit for Total Testosterone (Diagnostic Products, Los Angeles, CA) was used for the assay. The procedure, devised for the measurement of serum T, was modified to allow for measurement of the lower hormone concentrations in saliva. The Coat-a-Count kit contains polypropylene tubes with a T-specific antibody immobilized to the wall of the tube. The procedure involved pipetting 200 ~1 saliva into each of the coated tubes and adding 1.0 ml 12SI-labelled T. The tubes were shaken and incubated for 20 hr at room temperature before being decanted and counted for 1 min in a gamma counter. The antiserum used in the assay is considered to be highly specific for T, with very little cross-reactivity with other compounds. As little as 0.04 ng T per ml can be detected in a sample. Each saliva sample was
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assayed in duplicate and the mean value for the two duplicates taken as the value for each sample. The assay values for samples collected at the beginning and end of the session also were averaged. The latter value was felt to provide the most reliable estimate of T concentrations for the whole session and consequently was used in all the statistical analyses. As mentioned, the initial 48 subjects were tested on two occasions. Only the test results from the first test session were used, to avoid practice effects which might have been present in the second session. Consequently, the T concentration values from only the first testing were used for these subjects. RESULTS
Cognitive Tests The means of the raw scores for all tests, for men and women, are given in Table I, as well as the results o f t-tests of sex differences. Sex differences in the directions predicted were observed on several tests. Men scored significantly higher on Mental Rotations and Mathematical Ability, and with a one-tailed test, also on Paper Folding. There were no significant differences on any other tests, though the direction of differences on Identical Pictures was as predicted; i.e., women tended to do better.
Testosterone Assay Results In the assay for T concentrations, each saliva sample was assayed in duplicate. The intraassay reliability, estimated from a correlation between the duplicates, was r = .69 for men and r = .64 for w o m e n in the first group of 48 subjects, and r = . 8 2 for men and r = .73 for women in the second group of 40 subjects. The mean T concentration from the samples obtained at the beginning of the session were also compared to concentrations from the end of the session. Correlations for the assays from the first group of subjects were r = .71 and .74 for men and women, respectively. Equivalent values for the second group o f subjects were r = .90 and r = .73 for males and females, respectively. Although the latter coefficients are lower than those
TABLE I. MEAN SCORES (AND STANDARD DEVIATIONS), T-TESTS, AND SIGNIFICANCE LEVELS FOR ALL TESTS
Test (Maximum Score) Mental Rotation (24) Paper Folding (10) Mathematical Aptitude (15) Identical Pictures (48) Finding A's (# words) Tongue Twister (sec) Advanced Vocabulary (18)
X Females
X Males
t
p
8.63 (5.37) 5.48 (2.43) 4.98 (2.65) 34.72 (6.66) 31.63 (8.39) 13.90 (2.87) 5.92 (2.74)
10.98 (5.46) 6.29 (2.08) 6.84 (3.08 33.24 (7.07) 31.24 (8.38) 13.85 (2.39) 5.02 (2.90)
2.03
0.05
1.68
0.10
3.02
0.003
1.01
0.32
.22
0.83
.08
0.93
1.49
0.14
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usually reported for plasma concentrations, they compare favorably with some reliability coefficients reported for saliva (e.g., Dabbs et al., 1988) and are high enough to permit significant relationships to be found with other behavioral variables. The mean T level for all 42 men was 175.2 (SD = 46.8) pg/ml, and for all 46 women was 51.1 (SD = 23.0) pg/ml. These values are similar to concentrations of T in saliva found by others, ranging from 129 to 360 pg/ml for men and 34 to 108 pg/ml for women (Luisi et al., 1980; Sannikka et al., 1983; Besch et al., 1984; Christiansen & Knussman, 1987). There was no difference between the mean T concentrations of the initial 48 subjects, based on their first test session saliva samples [men: 178.4 (SD = 47.6) pg/ml; women: 51.1 (SD = 22.7) pg/ml], and the values obtained from the remaining 40 subjects [men: 170.8 (SD = 46.8) pg/ml; women: 5 I. 1 (SD = 23.9) pg/ml]. Subjects then were divided into high T and low T groups by making a median split of T concentrations, done separately for all 42 men and all 46 women. Thus, four groups were created: high T women, low T women, high T men and low T men. The mean T values for the high- and low-T men were 212.1 (SD=35.5) and 138.2 (SD=19.1) pg/ml, respectively. The mean T concentrations for high- and low-T women were 68.9 ( S D = 16.6) and 33.2 ( S D = 11.9) pg/ml, respectively.
Hormone Level and Cognitive Performance The mean test scores for each of the four groups are shown in Figs. 1 and 2. A multivariate sex x hormone level analysis of variance was conducted with all tests. The results are summarized in Table II. There was a main effect of sex, related to the predicted male superiority on spatial and mathematical tests, but no female superiority on any tests. There was also a significant sex x hormone level interaction. This was investigated by conducting analyses of variance on each test to determine which tests had significant sex x hormone level interactions (Table III). The results indicated that, of the individual tests, only
TABLE II. SUMMARYOF EFFECTSIN SEX x HORMONEMULTIVARIATEANALYSIS Effect
Sex Hormone Level Sex x Hormone Level
F
p
2.17 .89 2.39
< 0.05 0.52 < 0.03
TABLE III. SUMMARYOF SEX × HORMONEINTERACTIONSON TESTS Test
Paper Folding Mental Rotations Mathematics Aptitude Identical Pictures Finding A's Tongue Twister Advanced Vocabulary
F
p
11.86 .93 3.56 .94 .14 .97 .57
0.001 0.34 0.06 0.33 0.71 0.33 0.45
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MENTAL ROTATIONS
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FIG. 1: M e a n s c o r e s + s t a n d a r d e r r o r s o n t e s t s w h i c h t y p i c a l l y f a v o r m e n . IDENTICAL
PICTURES
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A'S
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TONGUE TWISTERS 15.00
HI-T
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HI-T
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ADVANCED VOCABULARY 7.00 6.00
14.00 5.00 13.00
4.00
12,00
11.00
10.00 LO-T
HI-T
WOMEN
I LO-T
3.00 2.00 1.00 0.00 HI-T
O-T
MEN
HI-T
LO-T
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MEN
FIG. 2: M e a n s c o r e s _+s t a n d a r d e r r o r s o n t e s t s w h i c h d o n o t t y p i c a l l y f a v o r m e n . TESTS THAT FAVOR MEN
TESTS THAT DO NOT FAVOR MEN
070
0.70
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FIG. 3: M e a n s c o r e s + s t a n d a r d e r r o r s o n c o m p o s i t e s o f s t a n d a r d i z e d z - s c o r e s f o r (a) t e s t s w h i c h t y p i c a l l y f a v o r m e n , a n d (b) t e s t s w h i c h d o n o t t y p i c a l l y f a v o r m e n , f o r s u b j e c t s g r o u p e d b y s a l i v a T (low o r h i g h ) .
TESTOSTERONEAND COGNITIVEABILITY
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Paper Folding showed a significant interaction between sex and hormone level, though the pattern was the same for Mental Rotations and Mathematical Ability, and in the latter case closely approached significance. The pattern of performance, as seen in Fig. 1, was for low-T men to be superior to high-T men, and for high-T women to perform better than low-T women. Post-hoc t-tests, used to compare Paper Folding scores of the four groups, indicated that low-T men achieved significantly higher scores than both high-T men and low-T women [t(40) = 2.50, p < 0.02, and t(42) = 3.68, p < 0.001, respectively] but did not differ significantly from high-T women [t(42)= 1.35]. High-T women achieved higher scores than low-T women [t(44)--2.36, p < 0.03] but did not differ from high-T women [t(42) = 1.20]. Since we predicted that low-T men would be superior on the mathematical test, post-hoc comparisons of test scores among groups were made. Post-hoc t-tests revealed that low-T men were superior, with significantly better scores on Mathematics Aptitude than either high- or low-T women [t(42) = 2.82, p < 0.01; t(42) = 3.53, p < 0.01, respectively], with, however, only a trend for better performance than high-T men [t(40)=1.93, p < 0 . 1 0 ) . Similarly, since it was predicted that low-T men would show superior performance on Mental Rotations, the scores of l o w - T m e n were c o m p a r e d to the scores of the other groups. L o w - T m e n p e r f o r m e d significantly better than only the low-T women [t(42)=2.12, p < 0 . 0 5 ] . No other group comparisons showed significant differences, though the pattem relative to T levels was the same as that for Paper Folding.
Standardized Scores and Composites Standardized z-scores for all tests were calculated to enable comparisons of the four groups across tests and to allow computation of composites. The z-scores for the tongue twister, a timed task, were multiplied by -1, so that on all tests higher scores represented better performance. A sex × hormone level × test analysis of variance then was conducted on the z-scores to determine if there were any interactions of sex or hormone level with test. There was a significant sex × test interaction (F = 2.16, p = 0.04), reflecting male superiority on the spatial and mathematics tests but not on others, as previously reported. Neither a significant hormone level × test interaction (F =.27, p = 0.95), nor sex × hormone level × test interaction (F = 1.25, p =0.28) were found. Several composites of standard scores also were calculated, since multiple measures are generally more reliable than single measures - - a "male" composite representing abilities in which T was expected to have an effect (Paper Folding, Mental Rotations, Mathematics Aptitude), and a "non-male" composite of abilities not expected to be influenced by T (Advanced Vocabulary, Finding A's, Identical Pictures, and the tongue twister). Each composite was calculated by finding the mean score of all tests included in that composite. A three-way analysis of variance revealed a strong trend towards a sex × hormone level x composite interaction (F = 2.7, p = 0.10). Since a sex × hormone level interaction was predicted for the "male" composite, but not for the "non-male" composite, post-hoc analyses were performed for each composite. In addition to the expected sex difference on the "male" composite (F = 9.96, p = 0.002), there was the predicted sex × hormone level interaction (F = 8.27, p = 0.005). The strong performance by low-T men on the "male" composite is apparent in Fig. 3. They achieved higher scores than the high-T males [t(40) = 2.24, p < 0.05]. High-T women had higher scores than low-T women [t(44)=2.54, p < 0 . 0 2 ] . For the women, there was no sex difference or sex x hormone level interaction for the "non-male" composite (F=.55, p =0.46; F = 1.40, p = 0.24, respectively).
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Correlation of Testosterone with Spatial Tests Multiple regression analyses were conducted to determine any significant relationship between T concentrations and cognitive performance. There were no significant correlations, though there was a trend in men for a positive linear relationship between T concentrations and Paper Folding scores (R=.29, p=0.06). In women, there was a trend for a quadratic relationship between testosterone concentrations and Mental Rotations scores (R =.33, p = 0.08). DISCUSSION Our findings are consistent with the suggestion that a nonlinear relationship exists between T concentrations and spatial ability (Shute et al., 1983). In addition, our findings suggest that T levels may be related to mathematical reasoning. Men with comparatively low T levels performed better on spatial and mathematical tasks than men with higher T levels, and women with high T concentrations were superior to those with low T. While this pattem of performance was evident on spatial and mathematical tests, as well as a composite of these tests, the interaction between sex and hormone level reached significance on only one spatial test, and on a composite score composed of tests usually better in men. There was no evidence for a consistent relationship between T concentrations and performance on the perceptual speed tasks, the tongue twister, or vocabulary test, abilities at which men are not usually better. This suggests that, within the limits of our tests, the relationship between T levels and cognitive function may be task-specific. An early theory on the effect of gonadal hormones on adult behavior suggested that, during development, hormones influence the organization of the neural tissues that mediate behavior (Phoenix et al., 1959). The animal literature offers many examples of the influence of early exposure to sex hormones on sex differences in brain morphology (e.g., Diamond et al., 1981; Dohler et al., 1983; Stewart & Kolb, 1988) and subsequent adult behavior (e.g., Goy & Phoenix, 1971; Nordeen & Yahr, 1982). In addition, there is evidence that sex-typical behavior in animals is related not only to the presence of sex hormones during perinatal development but also to the concentration of these hormones. Perinatal exposure to normal amounts of T is associated with the development, in the adult male, of typical male sexual behavior, while above-normal concentrations diminish this behavior (Diamond et al., 1973; Baum & Schretlen, 1975). Thus there is a general suggestion in the literature that medium concentrations of androgens are optimal for "normal" development, and that above-normal concentrations do not further enhance male abilities, and may in fact, reduce them. In humans, at least, we might entertain the idea that stereotypical male behavior includes superior spatial and mathematical ability. If we further postulate a relationship between relative T levels in the fetus and in the adult, it is logical to conclude that men with moderate levels of T would be better on spatial and mathematical skills than men with relatively higher T levels. We have focused on T as the hormone related to spatial and mathematical ability in this study. However, since T may be aromatized to estradiol in the brain (McEwen, 1981), it is possible that estradiol is the critical hormone which affects cognitive performance. Nyborg (1988) suggested that spatial ability is enhanced when estradiol is at an optimum level. He hypothesized that this optimum level of estradiol is present in physically more androgynous men, who are presumed to have higher estradiol levels relative to other men. Estradiol levels higher than the optimum, as found in women, or lower than the optimum, as in men with more characteristic masculine features, would be associated with poorer spatial ability. This theory is
TESTOSTERONE AND COGNITIVE ABILITY
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compatible with the findings of Petersen (1976), since androgynous male and female adolescents in her study did indeed score higher on spatial tests. Though neural systems that mediate some types of behavior may have already been organized under the influence of a sex hormone, adequate amounts of the same hormone also may be necessary in the adult before the behavior can be activated (Goy & McEwen, 1980). These activational effects are transient and last only as long as the hormone is present. Among the possible mechanisms whereby sex hormones can influence cognitive performance are their effects on the activities of enzymes in brain regions which contain hormone receptors, the modification of uptake of neurotransmitters, and the generalized increase or decrease of neuronal electrical activity (McEwen, 1980). Whatever the operational mechanisms, it should be noted that circulating hormones in the adult are acting on neural circuits which may not be the same in men and women (McEwen, 1987). Because of these activational effects, fluctuations in estrogen levels may influence spatial ability, even within an individual. Hampson (1990), in a study of cognitive changes in women across the menstrual cycle, found that women in the low-estrogen phase of the menstrual cycle were better on spatial tasks relative to their performance during the estrogen peak. She also related fluctuating estrogen levels across individuals (some tested during the low estrogen phase of the menstrual cycle, some tested at the high estrogen phase) to spatial performance, reporting a weak curvilinear relationship between performance on a spatial test and estrogen levels measured at the time of testing. Thus, as predicted by Nyborg's (1983) optimum estrogen range theory, high estrogen levels in these women were not conducive to good spatial ability. The possibility therefore exists that T levels are systematically related to estrogen levels, and that test performance in the present study is related to the concentrations of estradiol, rather than to T. However, based on other studies, this argument would predict that T levels would also relate to performance on other tests usually performed better by women. According to Hampson's study (1990), women in the low-estrogen phase of the menstrual cycle were slower on tests of verbal articulation relative to their performance during the high-estrogen phase. Kimura (1989) also reported that post-menopausal women in the off-phase of their estrogen replacement therapy scored lower on Finding A's and on a tongue twister, relative to women in the on-phase. However, in the current study, there were no differences between scores of highT and low-T women on the tongue twister or Finding A's, nor indeed any relation of T levels to scores on these tasks. It therefore seems unlikely that the T levels of our subjects were systematically related to estrogen levels, or at least that estrogen alone influenced test scores in this study. Nevertheless, until estrogen concentrations are measured, it is not possible to rule this out. Another possibility is that the estrogen/T ratio may influence cognitive performance (Nyborg, 1983). Some support for the potential importance of such a ratio comes from a report, in the animal literature, of a brain receptor mechanism that has a high affinity for both estrogen and T (Fox, 1975). Fox hypothesized that this receptor detects relative concentrations of androgens and estrogens. Again, the possible consequence of the estrogen/T ratio for cognitive functioning cannot be determined from the current study, and no other study has yet attempted to determine such an influence. However, some studies have shown a small, but significant positive relationship between spatial ability and the dihydroT (a metabolite of T)/T ratio (Christiansen & Knussmann, 1987; McKeever & Deyo, 1990). Several studies have investigated the correlation between T levels and spatial ability and have reported correlations ranging from near zero (McKeever & Deyo, 1990) through small though significant correlations (Shute et al., 1983; Christiansen & Knussmann, 1987), to as high as .53 for a spatial orientation task (Gordon & Lee, 1986). Our data showed small,
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nonsignificant correlations. If there were a multi-level or stepwise relationship between T and spatial ability, the small positive correlations may reflect only one part of that curve. Indeed, it would be difficult to make predictions about the nature of linear or quadratic correlations, particularly across sexes. We must also expect the relationships to vary, depending on the particular samples employed. Thus non-university samples might show somewhat different results, but most studies to date have employed university or college students. Though the precise brain systems influenced by sex hormones are not fully known at present, some suggestions have been made concerning the functions sampled in this study. Manual performance and articulatory skills, previously shown to be especially dependent on left anterior systems of the brain in women (Kimura, 1983), are enhanced by relatively high estrogen levels (Hampson & Kimura, 1988; Kimura, 1989; Hampson, 1990), suggesting that estrogen may facilitate the functioning of the left hemisphere, and/or the anterior regions of the brain. An increased right-ear superiority on a dichotic listening task during the estrogen peak of the menstrual cycle further supports the suggestion of enhanced left-hemisphere functioning (Hampson, 1990). In contrast, we might speculate that T enhances right-hemisphere functioning. We know that performance on spatial rotational tasks, one of which is similar to Mental Rotations, is mediated preferentially (though not necessarily exclusively) by the right hemisphere in men and women (Kimura & Hampson, in press). Animal studies suggest that T increases righthemisphere growth relative to left (Diamond et al., 1981; Stewart & Kolb, 1988). It is therefore possible that men, exposed to normal T levels during early development, have enhanced neural growth of the right hemisphere. This has been suggested as the mechanism whereby men apparently excel on right-hemisphere mediated functions compared to left-hemisphere mediated functions (Levy & Reid, 1978; Geschwind & Galaburda, 1985). The brains of women subjected to T concentrations above those of average women levels may be influenced in a similar manner, even if not to the same extent as in men. The extent of input from the left hemisphere to spatial function is not known. Conceivably, certain levels of T may have a damping effect on the left hemisphere, perhaps through right-toleft callosal inhibition. Any left-hemisphere contribution to spatial ability might thus become critically reduced when T concentrations become too high. This offers one of several possible explanations for the poorer spatial ability of high-T males relative to low-T males. Additionally, there may be sex differences in the anterior/posterior organization of spatial ability, with T preferentially facilitating development of posterior systems. One reason for thinking a sex hormone may favor certain areas of the brain is that estrogen has been shown to favor some functions dependent on anterior systems. The neural organization of praxic (motor programming) function is more dependent on the posterior regions in men, but on more anterior regions in women (Kimura, 1983; Kimura & Hampson, in press). Performance on tests of praxic function is enhanced in women when estrogen levels are high, relative to performance when estrogen is low, as reviewed earlier. However, at this stage, we should not rule out the possibility that the contribution of androgens to spatial ability may be effected through a more generalized influence on the brain. An optimal level of T, diffusely affecting the brain, might enhance the development and functioning of more extensive neural systems essential for spatial ability. Whatever the mechanisms may be that are involved in spatial ability, their optimal organization seems to depend on exposure to androgens during early development. Stable levels of androgens in the adult may either reflect this early organization and/or continue to influence brain functions and cognitive performance dependent on these systems.
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Acknowledgements: This research was funded by a grant to Doreen Kimura from the Medical Research Council, Ottawa, Canada. We gratefully acknowledge Dr. A. Rees Midgeley, Dr. Jill Becker, and Ms. Monika Naegeli at the University of Michigan, Ann Arbor, for their assistance with the saliva radioimmunoassays. We also thank Ms. Corinne Toussaint for her assistance in testing subjects. REFERENCES Baum MJ, Schretlen P (1975) Neuroendocrine effects of perinatal androgenization in the male ferret. Progr Brain Res 42: 343-355. Baxendale PM, Reed MJ, James VI-IT (1980) Testosterone in saliva of normal men and its relationship with unbound and total testosterone levels in plasma. J Endocrino187: 46-47. Benbow CP (1988) Sex differences in mathematical reasoning ability in intellectually talented preadolescents: their nature, effects, and possible causes. Behav Brain Sci 11: 169-232. Berenbaum SA, Resnick S (1982) Somatic androgyny and cognitive abilities. Dev Psychol 18: 418-423. Besch NF, Ruetzel CH, Younes MA, Huang NH, Besch PK (1984) Non-chromatographic determination of salivary testmterone in women. In: Read GF, Riad-Fahmy D, Walker RF, Griffiths K (Eds) lmmunoassays of Steroids in Saliva: Proceedings of the Ninth Tenovus Workshop. Alpha Omega Publishing, Cardiff, Wales, pp 221-227. Christiansen K, Knussmann R (1987) Sex hormones and cognitive functioning in men. Neuropsychobiology 18: 27-36. Dabbs JM, Ruback RB, Frady RL, Hopper CH, Sgoutas DS (1988) Saliva testosterone and criminal violence among women. Person Individ Diff9: 269-275. Diamond M, Llacuna A, Wong CL (1973) Sex behavior after neonatal progesterone, testosterone, estrogen, or antiandrogens. Horm Behav 4: 73-88. Diamond M, Dowling G, Johnson R (1981) Morphologic cerebral cortical asymmetry in male and female rats. Exp Neuro171: 261-268. Dohler KD, Coquelin A, Hines M, Davis F, Shryne JE, Gorski R (1983) Hormonal influence on sexual differentiation of rat brain anatomy. In: Balthazart J, Prove E, Gilles R (Eds) Hormones and Behavior in Higher Vertebrates. Springer-Verlag, New York, pp 194-203. Ekstrom RB, French J, Harman HH, Dermen D (1976) Kit of Factor-Referenced Cognitive Tests. Educational Testing Service, Princeton NJ. Farthing MJG, Mattel AM, Edwards CRW, Dawson AM (1982) Relationship between plasma testosterone and dihydrotestosterone concentrations and male facial hair growth. Br J Dermatol 107: 559-564. Fox TO (1975) Androgen- and estrogen-binding macromolecules in developing mouse brain: biochemical and genetic evidence. Proc Natl Acad Sci USA 72: 4303- 4307. Geschwind N, Galaburda A (1985) Cerebral lateralization: biological mechanisms, associations, and pathology: I. A hypothesis and a program for research. Arch Neuro142: 428-459. Gordon HW, Lee PA (1986) A relationship between gonadotropins and visuospatial function. Neuropsychologia 24: 563-576. Goy RW, McEwen BS (1980) Sexual Differentiation of the Brain. MIT Press, Cambridge MA. Goy RW, Phoenix CH (1971) The effects of testosterone propionate administered before birth on the development of behavior in genetic female rhesus monkeys. In: Sawyer CH, Gorski RA (Eds) Steroid Hormones and Brain Function. University of California Press, Los Angeles, pp 193-201. Hampson E (1990) Estrogen-related variations in human spatial and articulatory-motor skills. Psychoneuroendocrinology 15: 97-111. Hampson E, Kimura D (1988) Reciprocal effects of hormonal fluctuations on human motor and perceptualspatial skills. Behav Neurosci 102: 456-459. Harris LJ (1981) Sex-related variations in spatial skill. In: Liben LS, Patterson AH, Newcombe N (Eds) SpatiaI Representation and Behavior Across the Life Span. Academic Press, New York, pp 83-125. Harshman RA, Hampson E, Berenbaum SA (1983) Individual differences in cognitive abilities and brain organization - I. Sex and handedness differences in ability. Can J Psycho137: 144-192. Kimura D (1983) Sex differences in cerebral organization for speech and praxic functions. Can J Psycho137: 19-35.
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Kimura D (1989) The effect of exogenous estrogen on motor programming skills in post-menopausal women. Univ West Ont Dept Psychol Res Bull 684. Kimura D, Hampson E (in press) Neural and hormonal mechanisms mediating sex differences in cognition. In: Vernon PA (F_xl)Biological Approaches to the Study of Human Intelligence. Ablex. Levy J, Reid M (1978) Variations in cerebral organization as a function of handedness, hand posture in writing, and sex. J Exp Psychol:Gen 107: 119-144. Luisi M, Bernini GP, DelGenovese A, Birindelli R, Barletta D, Gasperi M, Franchi F (1980) Radioimmunoassay for"free" testosterone in human saliva. J SteroidBiochem 12: 513-516. Maccoby EE, Jacklin CN (1974) The Psychology of Sex Differences. Stanford University Press, Stanford CA. McEwen BS (1980) Gonadal steroids: humoral modulators of nerve-cell function. Mol Cell Endocrinol 18: 151-164. McEwen BS (1981) Neural gonadal steroid actions. Science 211: 1303-1311. McEwen BS (1987) Observations on brain sexual differentiation: a biochemist's view. In: Reinisch JM, Rosenblum LA, Sanders SA (Eds) Masculinity~Femininity. Oxford, New York, pp 68-79. McKeever WF (1986) The influence of handedness, sex, familial sinistrality and androgeny on language laterality, verbal ability, and spatial ability. Cortex 22: 521-537. McKeever WF, Deyo RA (1990) Testosterone, dihydrotestosterone, and spatial task perforrgances of males. Bull Psychonom Soc 28: 305-308. Nieschlag E (1974) Circadian rhythm of plasma testosterone. In: Aschoff J, Ceresa F, Halberg F (Eds) Chronobiological Aspects of Endocrinology. Schattauer Verlag, New York, pp 117-128. Nordeen EJ, Yahr P (1982) Hemispheric asymmetries in the behavioral and hormonal effects of sexually differentiating mammalian brain. Science 218: 391-394. Nyborg H (1983) Spatial ability in men and women: review and new theory. Adv Behav Res Ther 5: 89-140. Nyborg H (1988) Mathematics, sex hormones, and brain function. Behav Brain Sci 11: 206-207. Petersen AC (1976) Physical androgyny and cognitive functioning in adolescence. Dev Psychol 12: 524-533. Phoenix CH, Goy RW, Gerall AA, Young WC (1959) Organizing action of prenatally administered testosterone propionate on the tissues mediating mating behavior in the female guinea pig. Endocrinology 65" 369-382. Reinberg A, Lagoguey M (1978) Circadian and circannual rhythms in sexual activity and plasma hormones (FSH, LH, testosterone) of five human males. Arch Sex Behav 7: 13-30. Sanders B, Soares M, D'Aquila J (1982) The sex difference on one test of spatial visualization: a nontrivial difference. Child Dev 53" 1106-1110. Sannikka E, Terho P, Suominen J, Santti R (1983) Testosterone concentrations in human seminal plasma and saliva and its correlation with non-protein bound and total testosterone levels in serum. Int J Androl 6: 319-330. Shepard RN, Metzler J (1971) Mental rotation of three-dimensional objects. Science 171: 701-701. Shute VJ, Pellegrino JW, Hubert L, Reynolds RW (1983) The relationship between androgen levels and human spatial abilities. Bull Psychonom Soc 21: 465-468. Smals AGH, Kloppenborg PWC, Benraad ThJ (1976) Circannual cycle in plasma testosterone levels in man. J Clin Endocrinol Metab 42: 979-982. Stewart J, Kolb B (1988) The effects of neonatal gonadectomy and prenatal stress on cortical thickness and asymmetry in rats. Behav Neural Bio149: 3 4 4 - 3 6 0 . Tanner JM (1975) Growth and endocrinology of the adolescent. In: Gardner LI (Ed) Endocrine and Genetic Diseases of Childhood and Adolescence. WB Saunders, Toronto, pp 14-64. Vandenberg SG, Kuse AR (1978) Mental rotations, a group test of three-dimensional spatial visualization. Percept Mot Skills 47: 599-601. Vermeulen A, Verdonck L (1972) Some studies on the biological significance of free testosterone. J Steroid Biochem 3: 421-426. Wang C, Plymate S, Nieschlag E, Paulsen CA (1981) Salivary testosterone in men: further evidence of a direct correlation with free serum testosterone. J Clin Endocrinol Metab 53: 102i-1024. Watson NV, Kimura D (1991) Nontrivial sex differences in throwing and intercepting: relation to psychometrically-defined spatial functions. Person lndivid Diff 12: 375- 385. Wittig MA, Petersen AC (1979) Sex-Related Differences in Cognitive Functioning. Academic Press, New York.
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THE RELATIONSHIP BETWEEN TESTOSTERONE LEVELS AND COGNITIVE ABILITY PATTERNS CATHERINE GOUCHIE and DOREEN KIMURA Department of Psychology, University of Western Ontario, London Ontario, Canada (Received 27 June 1990; in finalform 22 October 1990)
SUMMARY The cognitive performance of normal men and women was studied, grouped according to whether the subjects had relatively high or low salivary testosterone (T) concentrations. Men with lower T performed better than other groups on measures of spatial/mathematical ability, tasks at which men normally excel. Women with high T scored higher than low-T women on these same measures. T concentrations did not relate significantly to scores on tests that usually favor women or that do not typically show a sex difference. These results support suggestions of a nonlinear relationship between T concentrations and spatial ability, and demonstrate some task specificity in this respect.
INTRODUCTION WOMEN are reported to perform better than men, on average, on tasks involving verbal skill (e.g., verbal fluency), perceptual speed and fine manual dexterity, while men demonstrate superior visual-spatial ability, mathematical reasoning ability, and targeting (Maccoby & Jacklin, 1974; Wittig & Petersen, 1979; Harris, 1981; Harshman et al., 1983; Benbow, 1988; Watson & Kimura, 1991). There is evidence that some variation in cognitive performance is related to inter-individual differences in chronic levels of sex hormones. Though circadian and circannual rhythms in testosterone (T) levels exist (Nieschlag, 1974; Smals et al., 1976; Reinberg & Lagoguey, 1978), levels of T may be relatively constant after puberty. For example, plasma testosterone concentrations of 15 men in April of one year were strongly correlated with their T concentrations in April of the following year, suggesting that, even though there are seasonal fluctuations in levels, overall they remain quite stable (Smals et al., 1976). A few studies relating hormone concentrations to cognitive performance have inferred the hormone levels of their subjects from the degree of secondary sex characteristic development, which is under the influence of sex hormones (Tanner, 1975; Farthing et al., 1982). Others reported that physically androgynous subjects, whether male or female, performed better on spatial tests than more sex-typical subjects (Petersen, 1976; Berenbaum & Resnick, 1982; McKeever, 1986). The purported relationship between cognitive performance and sex hormone levels was strengthened by the work of Shute et al. (1983), who studied the spatial ability of normal male Address correspondence and reprint requests to: Dr. Doreen Kimura, Department of Psychology, University of Western Ontario, London, CANADA N6A 5C2. 323
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and female subjects in w h o m they also had measured plasma androgen concentrations. They selected, from 33 subjects, the six men and six women with highest androgen levels and the six men and six women with the lowest androgen levels. There was a significant sex by androgenlevel interaction in that low-androgen men performed better on spatial tests than high-androgen men, and high-androgen women were better than low-androgen women. This pattern of performance among groups suggests a nonlinear relationship between androgen levels and spatial ability. However, Shute et al. m a y not have distinguished between the effects of T and other androgens, since the antibody used in the radioimmunoassay was assumed to bind to other androgens biochemically similar to T. They also did not attempt to determine the relationship between androgens and non-spatial tests. The present study attempted a broader investigation of the effects of T levels on cognitive abilities, both spatial and nonspatial, and in larger samples o f both men and women. Each subject completed several cognitive and m o t o r tests that were c h o s e n because they were expected to favor either women or men. It was predicted that tests of abilities normally better in men would be influenced by T levels, at least in men. Further, if a curvilinear relationship exists between T levels and spatial ability, women with higher levels of T, and men with lower levels, would be expected to score higher on spatial tests. The same pattern might be predicted for scores on mathematical reasoning tests, given the strong sex difference favoring men in mathematical ability. T was not expected to influence the tasks at which women usually excel, such as perceptual speed and verbal articulation, or tasks which do not typically show sex differences, such as vocabulary. T concentrations were determined from saliva, since obtaining saliva samples is a less invasive procedure than drawing blood. Moreover, only free T (not bound to sex-hormone binding globulin) is present in saliva. It is assumed that only free T is biologically active and can be taken up and metabolized by target tissues, including the brain (Vermeulen & Verdonck, 1972). A high correlation between salivary T concentrations and total serum concentrations has been demonstrated (e.g., Baxendale et al., 1980: r=.81; Wang et al., 1981: r =.94). SUBJECTS AND METHODS
Subjects Eighty-eight right-handed volunteers (42 men, 46 women) were solicited through advertisements posted around the campus. They were predominantly undergraduates at the University of Western Ontario. The mean age of the men was 21.0 yr (range: 18-27 yr), and of the women was 21.5 yr (range: 18-31 yr). Fifteen of the 46 women and 13 of the 42 men were in a science program. The rest were in an arts or social science program. Subjects were paid for their participation in the study. They were not aware of the hypotheses being tested. Forty-eight (24 men, 24 women) of the subjects were participants in a two-phase study, which employed the same tests as those used here. Test results from the first phase of that study were therefore included here. T assays for these subjects were conducted separately from those for the second group of subjects (see below). Procedures Subjects were tested individually. At the beginning and end of the test session, they were asked to provide a 7-ml sample of saliva for radioimmunoassay determination of T concentrations. Subjects completed a battery of cognitive and motor tasks. Tests measuring abilities in which either a sex difference has previously been noted, or which were demonstrably sensitive to hormone fluctuations, were used. The tests included measures of spatial ability, perceptual speed, mathematical reasoning ability, and verbal-articulatory ability. A vocabulary test was employed as a measure of general intellectual level. Subjects also answered questions on their physical development and characteristics. These data will be presented elsewhere.
TESTOSTERONEAND COGNITIVEABILITY
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Tests Most tests, with the exception of the tongue twister, were multiple-choice paper-and-pencil tests. A correction factor for guessing was used in the scoring of all multiple choice tests. Tests of spatial ability and mathematical ability were chosen as measures of skills typically performed better by men. Soatial Ability: Two tests of spatial ability were included - - Paper Folding and Mental Rotations. These tests were chosen because men have been reported to score higher than women on tests involving mental rotation or shape transformation (Vandenberg & Kuse, 1978; Sanders et al., 1982; Harshman et al., 1983). (1) For the Paper Folding test (Ekstrom et al., 1976), each item consisted of a series of pictures which illustrated a square piece of paper being folded and a hole being punched through. The subject had to determine where holes would appear once the paper was unfolded and to choose the appropriate representation from among five pictures. There are 10 items in this test, and 3 min are allowed for completion. Watson and Kimura (1991) reported a strong trend for men to do better on this test. (2) On the Mental Rotations Test (Vandenberg & Kuse, 1973, adaptation of the Shepard-Metzler test; Shepard & Metzler, 1971), the subject was presented with a two-dimensional representation of a three-dimensional, asymmetric set of cubes, and had to identify the same stimulus depicted as having rotated in space. There are four choices for each item, two of which are correct. Four minutes are allowed to complete the 12 items; the maximum possible score is 24. MathemaIi~al Ability: Mathematical ability was measured with the Mathematics Aptitude Test (Ekstrom et al., 1976), classified as a test of general reasoning. Ten minutes are allowed for the completion of 15 mathematical reasoning problems. Men are usually superior on mathematical reasoning tests (Benbow, 1988). Several tests of abilities on which men were not expected to excel were also included. In some of these tests, women were expected to do better than men, while in others, no sex difference was expected. Percentual Soeed: Two perceptual speed tests from the ETS kit of Factor-Referenced Cognitive Tests (Ekstrom et at., 1976) were administered, since a female advantage has been reported on several tests of perceptual speed (Maccoby & Jacklin, 1974; Harshman et al., 1983). (1) On the Finding A's test, subjects were given lists of words and had to cross out each word that contained the letter "a". The final score was the number of words crossed out in 2 min. (2) Identical Pictures test required the subject to choose the one of five choices which was identical to the stimulus figure. There are 48 items, with a time limit of 1.5 min. Verbal Articulation: Verbal articulation was measured by having the subject say a tongue twister as quickly as possible. The time was recorded for the criterion of five consecutive correct repetitions of the tongue twister "A box of mixed biscuits and a biscuit mixer." Though sex differences have not been reported on this particular test, it has been shown to be sensitive to fluctuations in exogenous estrogen (Kimura, 1989): Verbal articulation was enhanced when estrogen levels were higher. Vocabulary: The Advanced Vocabulary test (Ekstrom et al., 1976) was administered as a measure of general intellectual ability. The subject was asked to select, from among five alternatives, the word most similar in meaning to the stimulus word. There were 18 items. No sex difference or hormone effect was predicted for performance on this test. Radioimmunoassays Following completion of the study, T concentrations were determined from saliva samples collected at the beginning and end of the test session. Saliva production was stimulated by having subjects chew gum containing citric acid (Gatorgum). Samples were collected in borosilicate vials, frozen immediately after collection, and stored at -20 ° C until they were assayed. All samples were analyzed by the same technician at University of Michigan, Ann Arbor, though assays for the first 48 subjects were analyzed at different times and therefore by different kits from those for the final 40 subjects. A Coat-a-Count kit for Total Testosterone (Diagnostic Products, Los Angeles, CA) was used for the assay. The procedure, devised for the measurement of serum T, was modified to allow for measurement of the lower hormone concentrations in saliva. The Coat-a-Count kit contains polypropylene tubes with a T-specific antibody immobilized to the wall of the tube. The procedure involved pipetting 200 ~1 saliva into each of the coated tubes and adding 1.0 ml 12SI-labelled T. The tubes were shaken and incubated for 20 hr at room temperature before being decanted and counted for 1 min in a gamma counter. The antiserum used in the assay is considered to be highly specific for T, with very little cross-reactivity with other compounds. As little as 0.04 ng T per ml can be detected in a sample. Each saliva sample was
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assayed in duplicate and the mean value for the two duplicates taken as the value for each sample. The assay values for samples collected at the beginning and end of the session also were averaged. The latter value was felt to provide the most reliable estimate of T concentrations for the whole session and consequently was used in all the statistical analyses. As mentioned, the initial 48 subjects were tested on two occasions. Only the test results from the first test session were used, to avoid practice effects which might have been present in the second session. Consequently, the T concentration values from only the first testing were used for these subjects. RESULTS
Cognitive Tests The means of the raw scores for all tests, for men and women, are given in Table I, as well as the results o f t-tests of sex differences. Sex differences in the directions predicted were observed on several tests. Men scored significantly higher on Mental Rotations and Mathematical Ability, and with a one-tailed test, also on Paper Folding. There were no significant differences on any other tests, though the direction of differences on Identical Pictures was as predicted; i.e., women tended to do better.
Testosterone Assay Results In the assay for T concentrations, each saliva sample was assayed in duplicate. The intraassay reliability, estimated from a correlation between the duplicates, was r = .69 for men and r = .64 for w o m e n in the first group of 48 subjects, and r = . 8 2 for men and r = .73 for women in the second group of 40 subjects. The mean T concentration from the samples obtained at the beginning of the session were also compared to concentrations from the end of the session. Correlations for the assays from the first group of subjects were r = .71 and .74 for men and women, respectively. Equivalent values for the second group o f subjects were r = .90 and r = .73 for males and females, respectively. Although the latter coefficients are lower than those
TABLE I. MEAN SCORES (AND STANDARD DEVIATIONS), T-TESTS, AND SIGNIFICANCE LEVELS FOR ALL TESTS
Test (Maximum Score) Mental Rotation (24) Paper Folding (10) Mathematical Aptitude (15) Identical Pictures (48) Finding A's (# words) Tongue Twister (sec) Advanced Vocabulary (18)
X Females
X Males
t
p
8.63 (5.37) 5.48 (2.43) 4.98 (2.65) 34.72 (6.66) 31.63 (8.39) 13.90 (2.87) 5.92 (2.74)
10.98 (5.46) 6.29 (2.08) 6.84 (3.08 33.24 (7.07) 31.24 (8.38) 13.85 (2.39) 5.02 (2.90)
2.03
0.05
1.68
0.10
3.02
0.003
1.01
0.32
.22
0.83
.08
0.93
1.49
0.14
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usually reported for plasma concentrations, they compare favorably with some reliability coefficients reported for saliva (e.g., Dabbs et al., 1988) and are high enough to permit significant relationships to be found with other behavioral variables. The mean T level for all 42 men was 175.2 (SD = 46.8) pg/ml, and for all 46 women was 51.1 (SD = 23.0) pg/ml. These values are similar to concentrations of T in saliva found by others, ranging from 129 to 360 pg/ml for men and 34 to 108 pg/ml for women (Luisi et al., 1980; Sannikka et al., 1983; Besch et al., 1984; Christiansen & Knussman, 1987). There was no difference between the mean T concentrations of the initial 48 subjects, based on their first test session saliva samples [men: 178.4 (SD = 47.6) pg/ml; women: 51.1 (SD = 22.7) pg/ml], and the values obtained from the remaining 40 subjects [men: 170.8 (SD = 46.8) pg/ml; women: 5 I. 1 (SD = 23.9) pg/ml]. Subjects then were divided into high T and low T groups by making a median split of T concentrations, done separately for all 42 men and all 46 women. Thus, four groups were created: high T women, low T women, high T men and low T men. The mean T values for the high- and low-T men were 212.1 (SD=35.5) and 138.2 (SD=19.1) pg/ml, respectively. The mean T concentrations for high- and low-T women were 68.9 ( S D = 16.6) and 33.2 ( S D = 11.9) pg/ml, respectively.
Hormone Level and Cognitive Performance The mean test scores for each of the four groups are shown in Figs. 1 and 2. A multivariate sex x hormone level analysis of variance was conducted with all tests. The results are summarized in Table II. There was a main effect of sex, related to the predicted male superiority on spatial and mathematical tests, but no female superiority on any tests. There was also a significant sex x hormone level interaction. This was investigated by conducting analyses of variance on each test to determine which tests had significant sex x hormone level interactions (Table III). The results indicated that, of the individual tests, only
TABLE II. SUMMARYOF EFFECTSIN SEX x HORMONEMULTIVARIATEANALYSIS Effect
Sex Hormone Level Sex x Hormone Level
F
p
2.17 .89 2.39
< 0.05 0.52 < 0.03
TABLE III. SUMMARYOF SEX × HORMONEINTERACTIONSON TESTS Test
Paper Folding Mental Rotations Mathematics Aptitude Identical Pictures Finding A's Tongue Twister Advanced Vocabulary
F
p
11.86 .93 3.56 .94 .14 .97 .57
0.001 0.34 0.06 0.33 0.71 0.33 0.45
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MENTAL ROTATIONS
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FIG. 1: M e a n s c o r e s + s t a n d a r d e r r o r s o n t e s t s w h i c h t y p i c a l l y f a v o r m e n . IDENTICAL
PICTURES
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ADVANCED VOCABULARY 7.00 6.00
14.00 5.00 13.00
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FIG. 2: M e a n s c o r e s _+s t a n d a r d e r r o r s o n t e s t s w h i c h d o n o t t y p i c a l l y f a v o r m e n . TESTS THAT FAVOR MEN
TESTS THAT DO NOT FAVOR MEN
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FIG. 3: M e a n s c o r e s + s t a n d a r d e r r o r s o n c o m p o s i t e s o f s t a n d a r d i z e d z - s c o r e s f o r (a) t e s t s w h i c h t y p i c a l l y f a v o r m e n , a n d (b) t e s t s w h i c h d o n o t t y p i c a l l y f a v o r m e n , f o r s u b j e c t s g r o u p e d b y s a l i v a T (low o r h i g h ) .
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Paper Folding showed a significant interaction between sex and hormone level, though the pattern was the same for Mental Rotations and Mathematical Ability, and in the latter case closely approached significance. The pattern of performance, as seen in Fig. 1, was for low-T men to be superior to high-T men, and for high-T women to perform better than low-T women. Post-hoc t-tests, used to compare Paper Folding scores of the four groups, indicated that low-T men achieved significantly higher scores than both high-T men and low-T women [t(40) = 2.50, p < 0.02, and t(42) = 3.68, p < 0.001, respectively] but did not differ significantly from high-T women [t(42)= 1.35]. High-T women achieved higher scores than low-T women [t(44)--2.36, p < 0.03] but did not differ from high-T women [t(42) = 1.20]. Since we predicted that low-T men would be superior on the mathematical test, post-hoc comparisons of test scores among groups were made. Post-hoc t-tests revealed that low-T men were superior, with significantly better scores on Mathematics Aptitude than either high- or low-T women [t(42) = 2.82, p < 0.01; t(42) = 3.53, p < 0.01, respectively], with, however, only a trend for better performance than high-T men [t(40)=1.93, p < 0 . 1 0 ) . Similarly, since it was predicted that low-T men would show superior performance on Mental Rotations, the scores of l o w - T m e n were c o m p a r e d to the scores of the other groups. L o w - T m e n p e r f o r m e d significantly better than only the low-T women [t(42)=2.12, p < 0 . 0 5 ] . No other group comparisons showed significant differences, though the pattem relative to T levels was the same as that for Paper Folding.
Standardized Scores and Composites Standardized z-scores for all tests were calculated to enable comparisons of the four groups across tests and to allow computation of composites. The z-scores for the tongue twister, a timed task, were multiplied by -1, so that on all tests higher scores represented better performance. A sex × hormone level × test analysis of variance then was conducted on the z-scores to determine if there were any interactions of sex or hormone level with test. There was a significant sex × test interaction (F = 2.16, p = 0.04), reflecting male superiority on the spatial and mathematics tests but not on others, as previously reported. Neither a significant hormone level × test interaction (F =.27, p = 0.95), nor sex × hormone level × test interaction (F = 1.25, p =0.28) were found. Several composites of standard scores also were calculated, since multiple measures are generally more reliable than single measures - - a "male" composite representing abilities in which T was expected to have an effect (Paper Folding, Mental Rotations, Mathematics Aptitude), and a "non-male" composite of abilities not expected to be influenced by T (Advanced Vocabulary, Finding A's, Identical Pictures, and the tongue twister). Each composite was calculated by finding the mean score of all tests included in that composite. A three-way analysis of variance revealed a strong trend towards a sex × hormone level x composite interaction (F = 2.7, p = 0.10). Since a sex × hormone level interaction was predicted for the "male" composite, but not for the "non-male" composite, post-hoc analyses were performed for each composite. In addition to the expected sex difference on the "male" composite (F = 9.96, p = 0.002), there was the predicted sex × hormone level interaction (F = 8.27, p = 0.005). The strong performance by low-T men on the "male" composite is apparent in Fig. 3. They achieved higher scores than the high-T males [t(40) = 2.24, p < 0.05]. High-T women had higher scores than low-T women [t(44)=2.54, p < 0 . 0 2 ] . For the women, there was no sex difference or sex x hormone level interaction for the "non-male" composite (F=.55, p =0.46; F = 1.40, p = 0.24, respectively).
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Correlation of Testosterone with Spatial Tests Multiple regression analyses were conducted to determine any significant relationship between T concentrations and cognitive performance. There were no significant correlations, though there was a trend in men for a positive linear relationship between T concentrations and Paper Folding scores (R=.29, p=0.06). In women, there was a trend for a quadratic relationship between testosterone concentrations and Mental Rotations scores (R =.33, p = 0.08). DISCUSSION Our findings are consistent with the suggestion that a nonlinear relationship exists between T concentrations and spatial ability (Shute et al., 1983). In addition, our findings suggest that T levels may be related to mathematical reasoning. Men with comparatively low T levels performed better on spatial and mathematical tasks than men with higher T levels, and women with high T concentrations were superior to those with low T. While this pattem of performance was evident on spatial and mathematical tests, as well as a composite of these tests, the interaction between sex and hormone level reached significance on only one spatial test, and on a composite score composed of tests usually better in men. There was no evidence for a consistent relationship between T concentrations and performance on the perceptual speed tasks, the tongue twister, or vocabulary test, abilities at which men are not usually better. This suggests that, within the limits of our tests, the relationship between T levels and cognitive function may be task-specific. An early theory on the effect of gonadal hormones on adult behavior suggested that, during development, hormones influence the organization of the neural tissues that mediate behavior (Phoenix et al., 1959). The animal literature offers many examples of the influence of early exposure to sex hormones on sex differences in brain morphology (e.g., Diamond et al., 1981; Dohler et al., 1983; Stewart & Kolb, 1988) and subsequent adult behavior (e.g., Goy & Phoenix, 1971; Nordeen & Yahr, 1982). In addition, there is evidence that sex-typical behavior in animals is related not only to the presence of sex hormones during perinatal development but also to the concentration of these hormones. Perinatal exposure to normal amounts of T is associated with the development, in the adult male, of typical male sexual behavior, while above-normal concentrations diminish this behavior (Diamond et al., 1973; Baum & Schretlen, 1975). Thus there is a general suggestion in the literature that medium concentrations of androgens are optimal for "normal" development, and that above-normal concentrations do not further enhance male abilities, and may in fact, reduce them. In humans, at least, we might entertain the idea that stereotypical male behavior includes superior spatial and mathematical ability. If we further postulate a relationship between relative T levels in the fetus and in the adult, it is logical to conclude that men with moderate levels of T would be better on spatial and mathematical skills than men with relatively higher T levels. We have focused on T as the hormone related to spatial and mathematical ability in this study. However, since T may be aromatized to estradiol in the brain (McEwen, 1981), it is possible that estradiol is the critical hormone which affects cognitive performance. Nyborg (1988) suggested that spatial ability is enhanced when estradiol is at an optimum level. He hypothesized that this optimum level of estradiol is present in physically more androgynous men, who are presumed to have higher estradiol levels relative to other men. Estradiol levels higher than the optimum, as found in women, or lower than the optimum, as in men with more characteristic masculine features, would be associated with poorer spatial ability. This theory is
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compatible with the findings of Petersen (1976), since androgynous male and female adolescents in her study did indeed score higher on spatial tests. Though neural systems that mediate some types of behavior may have already been organized under the influence of a sex hormone, adequate amounts of the same hormone also may be necessary in the adult before the behavior can be activated (Goy & McEwen, 1980). These activational effects are transient and last only as long as the hormone is present. Among the possible mechanisms whereby sex hormones can influence cognitive performance are their effects on the activities of enzymes in brain regions which contain hormone receptors, the modification of uptake of neurotransmitters, and the generalized increase or decrease of neuronal electrical activity (McEwen, 1980). Whatever the operational mechanisms, it should be noted that circulating hormones in the adult are acting on neural circuits which may not be the same in men and women (McEwen, 1987). Because of these activational effects, fluctuations in estrogen levels may influence spatial ability, even within an individual. Hampson (1990), in a study of cognitive changes in women across the menstrual cycle, found that women in the low-estrogen phase of the menstrual cycle were better on spatial tasks relative to their performance during the estrogen peak. She also related fluctuating estrogen levels across individuals (some tested during the low estrogen phase of the menstrual cycle, some tested at the high estrogen phase) to spatial performance, reporting a weak curvilinear relationship between performance on a spatial test and estrogen levels measured at the time of testing. Thus, as predicted by Nyborg's (1983) optimum estrogen range theory, high estrogen levels in these women were not conducive to good spatial ability. The possibility therefore exists that T levels are systematically related to estrogen levels, and that test performance in the present study is related to the concentrations of estradiol, rather than to T. However, based on other studies, this argument would predict that T levels would also relate to performance on other tests usually performed better by women. According to Hampson's study (1990), women in the low-estrogen phase of the menstrual cycle were slower on tests of verbal articulation relative to their performance during the high-estrogen phase. Kimura (1989) also reported that post-menopausal women in the off-phase of their estrogen replacement therapy scored lower on Finding A's and on a tongue twister, relative to women in the on-phase. However, in the current study, there were no differences between scores of highT and low-T women on the tongue twister or Finding A's, nor indeed any relation of T levels to scores on these tasks. It therefore seems unlikely that the T levels of our subjects were systematically related to estrogen levels, or at least that estrogen alone influenced test scores in this study. Nevertheless, until estrogen concentrations are measured, it is not possible to rule this out. Another possibility is that the estrogen/T ratio may influence cognitive performance (Nyborg, 1983). Some support for the potential importance of such a ratio comes from a report, in the animal literature, of a brain receptor mechanism that has a high affinity for both estrogen and T (Fox, 1975). Fox hypothesized that this receptor detects relative concentrations of androgens and estrogens. Again, the possible consequence of the estrogen/T ratio for cognitive functioning cannot be determined from the current study, and no other study has yet attempted to determine such an influence. However, some studies have shown a small, but significant positive relationship between spatial ability and the dihydroT (a metabolite of T)/T ratio (Christiansen & Knussmann, 1987; McKeever & Deyo, 1990). Several studies have investigated the correlation between T levels and spatial ability and have reported correlations ranging from near zero (McKeever & Deyo, 1990) through small though significant correlations (Shute et al., 1983; Christiansen & Knussmann, 1987), to as high as .53 for a spatial orientation task (Gordon & Lee, 1986). Our data showed small,
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nonsignificant correlations. If there were a multi-level or stepwise relationship between T and spatial ability, the small positive correlations may reflect only one part of that curve. Indeed, it would be difficult to make predictions about the nature of linear or quadratic correlations, particularly across sexes. We must also expect the relationships to vary, depending on the particular samples employed. Thus non-university samples might show somewhat different results, but most studies to date have employed university or college students. Though the precise brain systems influenced by sex hormones are not fully known at present, some suggestions have been made concerning the functions sampled in this study. Manual performance and articulatory skills, previously shown to be especially dependent on left anterior systems of the brain in women (Kimura, 1983), are enhanced by relatively high estrogen levels (Hampson & Kimura, 1988; Kimura, 1989; Hampson, 1990), suggesting that estrogen may facilitate the functioning of the left hemisphere, and/or the anterior regions of the brain. An increased right-ear superiority on a dichotic listening task during the estrogen peak of the menstrual cycle further supports the suggestion of enhanced left-hemisphere functioning (Hampson, 1990). In contrast, we might speculate that T enhances right-hemisphere functioning. We know that performance on spatial rotational tasks, one of which is similar to Mental Rotations, is mediated preferentially (though not necessarily exclusively) by the right hemisphere in men and women (Kimura & Hampson, in press). Animal studies suggest that T increases righthemisphere growth relative to left (Diamond et al., 1981; Stewart & Kolb, 1988). It is therefore possible that men, exposed to normal T levels during early development, have enhanced neural growth of the right hemisphere. This has been suggested as the mechanism whereby men apparently excel on right-hemisphere mediated functions compared to left-hemisphere mediated functions (Levy & Reid, 1978; Geschwind & Galaburda, 1985). The brains of women subjected to T concentrations above those of average women levels may be influenced in a similar manner, even if not to the same extent as in men. The extent of input from the left hemisphere to spatial function is not known. Conceivably, certain levels of T may have a damping effect on the left hemisphere, perhaps through right-toleft callosal inhibition. Any left-hemisphere contribution to spatial ability might thus become critically reduced when T concentrations become too high. This offers one of several possible explanations for the poorer spatial ability of high-T males relative to low-T males. Additionally, there may be sex differences in the anterior/posterior organization of spatial ability, with T preferentially facilitating development of posterior systems. One reason for thinking a sex hormone may favor certain areas of the brain is that estrogen has been shown to favor some functions dependent on anterior systems. The neural organization of praxic (motor programming) function is more dependent on the posterior regions in men, but on more anterior regions in women (Kimura, 1983; Kimura & Hampson, in press). Performance on tests of praxic function is enhanced in women when estrogen levels are high, relative to performance when estrogen is low, as reviewed earlier. However, at this stage, we should not rule out the possibility that the contribution of androgens to spatial ability may be effected through a more generalized influence on the brain. An optimal level of T, diffusely affecting the brain, might enhance the development and functioning of more extensive neural systems essential for spatial ability. Whatever the mechanisms may be that are involved in spatial ability, their optimal organization seems to depend on exposure to androgens during early development. Stable levels of androgens in the adult may either reflect this early organization and/or continue to influence brain functions and cognitive performance dependent on these systems.
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