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Testosterone and Estradiol in Right-Handed men But Only Estradiol in Right-

Handed Women is Inversely Correlated with the Degree of Right-Hand
Preference
Üner Tan a
a
Department of Physiology, Atatürk University, Medical Faculty, Erzurum, Turkey

Online Publication Date: 01 September 1992

To cite this Article Tan, Üner(1992)'Testosterone and Estradiol in Right-Handed men But Only Estradiol in Right-Handed Women is
Inversely Correlated with the Degree of Right-Hand Preference',International Journal of Neuroscience,66:1,25 — 34
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TESTOSTERONE AND ESTRADIOL IN RIGHT-

HANDED MEN BUT ONLY ESTRADIOL IN
RIGHT-HANDED WOMEN IS INVERSELY
CORRELATEDWITHTHEDEGREEOF
RIGHT-HAND PREFERENCE

UNER TAN
Ataturk University. Medical Faculty, Department of Physiology, Erzurum, Turkey

(Received December 2 0 , 1991)

Relations of sex hormones to the degree of right-hand preference was studied in right-handed male and
female adult subjects. Hand preference was assessed by the Edinburgh and Waterloo Handedness Ques-
tionnaires. Males consisted of weakly, moderately, and strongly right-handed subjects. Females com-
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prised only moderately and strongly right-handed subjects. In females, only serum estradiol was found
to be negatively linearly and significantly correlated with the degree of right-hand preference. In males,
testosterone, as well as estradiol, showed a significant negative linear correlation with the degree of
right-hand preference. Sex hormone binding globulin also showed a similar relation to hand preference
in males. Thus, nearly all sex hormones caused a decrease in the degree of right-hand preference in
males, whereas only estradiol had the same effect on hand preference in females. This would be the
cause of stronger right-hand preference in females than males and vice versa.

Keywords; Handedness, hand preference, testosterone, estradiol, cerebral lateralization

There is now growing evidence that gonadal hormones are involved in neural func-
tions including cerebral organization, behavior, and cognition in human and animal
(Bernardi et al., 1989; Butterbaugh & Hudson, 1991; Corsi-Cabrera et al., 1989; De
Vries, 1990; Earley & Leonard, 1978; Eaton & Enns, 1986; Hampson, 1990; Hamp-
son & Kimura, 1988; Hanske-Petitpierre & Chen, 1985; Hines & Shipley, 1984;
Jiiptner & Hiemke, 1990; Lapchak et al., 1990; Mann et al., 1990; Michard-Vanhee
& Roubertoux, 1990; Nass et al., 1990; Primus & Kellogg, 1990; Schumacher, 1990;
Signorella & Jamison, 1986; Thomas & French, 1985; van Hest et al., 1988; Vijayan
& McCann, 1978). Estrogens have been reported to influence the extrapyramidal
system (Bedard et al., 1977; Demotes-Mainard et al., 1990; Euvrard et al., 1979).
The studies concerned with cerebral lateralization mostly included perinatal effects
of gonadal hormones. Diamond (see 1987) has reported that, in Long-Evans rats,
the male right cortex is thicker than the left from birth to 904 days of age, but the
difference become less significant with age; the female cortex is usually thicker on
the left side from 7 to 400 days of age, but the differences are in general not sta-
tistically significant. Diamond has further reported in the same view that estrogen
receptors are found in both male and female cerebral cortices at birth and apparently
disappear after one month. Sengstake and Chambers (1991) have suggested that the
amount of testosterone required to activate the prolonged extinction of a conditioned
taste aversion in adult rats depends on perinatal exposure to testosterone.
~

I am indebted to my students for providing blood samples and to the Department of Biochemistry for
assistance in hormone determinations

25
 26 U . TAN

The above mentioned effects of gonadal hormones on central nervous system sug-
gest that they may be also involved in human handedness. Therefore, the relation-
ships between serum total testosterone levels and handedness was subjected to a
detailed analysis in young human. Tan (1990 a) has found that hand preference was
usually negatively linearly correlated with serum testosterone levels in young male
and female subjects. Interestingly, there was a positive linear correlation only be-
tween right-hand skill and serum testosterone level in right-handed young men, and
a negative linear correlation only between right-hand skill (peg moving task) and
serum testosterone level in young women; the left hand skill did not show any sig-
nificant relation to testosterone (Tan, 1990 b). Hand performance (dot-filling test)
showed a more complex relation to testosterone in young adults (Tan, 1990 c). I
have also established that the mean serum testosterone level is significantly higher
in subjects with anomalous dominance than those with standard dominance (Tan,
1991). The intramuscularly-injected testosterone reduced the right-paw preference in
cats, but only in female cats (Tan et al., 1991 a). These results only partly supported
the testosterone theory of cerebral lateralization (Geschwind & Behan, 1982; Ge-
schwind & Galaburda, 1985 a,b). According to a psychomotor hypothesis (see Tan,
1988 b), testosterone influencing the motor system is expected to exert associations
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with cognition. Consequently, I have shown that there is a direct relationship be-
tween nonverbal intelligence and testosterone only in young men, not in young women
(Tan, 1990 d). Moreover, nonverbal intelligence was found to be directly correlated
with hand skill especially in young men (Tan, 1990 e).
The above mentioned studies suggest that sex hormones may exert their effects
on cerebral lateralization also in young adults. Therefore, the male and female sex
hormones were subjected to a more detailed analysis in relation to hand preference
in this work. Hand preference was assessed by a more detailed questionnaire. Total
and free testosterone levels in serum along with estradiol levels were determined in
serum of right-handed young men and women. It was shown that total testosterone
and estradiol in men and only estradiol in women are mainly related to the degree
of right hand preference negatively linearly. This is proposed to cause women to be
more right-handed than men.

METHODS
Subjects And Hand Preference
Subjects were right-handed students ranging in age from 17 to 19 years. They par-
ticipated in the study voluntarily, and were healthy (devoid of neurological and psy-
chiatric signs and symptoms).
Hand preference was assessed by two questionnaires: Edinburgh (Oldfield, 197 1)
and Waterloo (Steenhuis & Bryden, 1989). In Edinburgh Handedness Inventory, a
laterality score from 10 questions was calculated. This was called Geschwind score
(see Tan, 1988 a), GS. The Waterloo Handedness Questionnaire comprised 32 ques-
tions. This score was called Waterloo score (WS).

Hormone Assay
The venous blood was taken into a lithium test tube and the plasma was separated.
Serum gonadal hormones were determined using radio-immunoassays (Nieschlag &
Losiaux, 1972).
 j
HAND PREFERENCE AND SEX HORMONES 27

A . GSS IN R-H MALES

15
n 12 . ,. . . .
u
QJE 9
3
.. , ., . ., , .. ., ,.....
E b
I ..I

k
+ 3 ... I .

0 +.
30 50 70 90 118
GSS
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B. GSS I N R-H FEMALES

FIGURE I Distribution of hand preference (GSs) in male (A) and female (B) subjects Abscissa: GS,
ordinate: number of subjects.

RESULTS
Distribution Of Right Hand Preference
Figure 1 shows the distributions of GSs in right-handed male (A) and female (B)
subjects. In males, three subgroup could be distinguished: weakly right-handed sub-
jects (GSs from 30 to 50), moderately right-handed subjects (GSs from 55 to 70).
and strongly right-handed subjects (GSs from 75 to 100). Males could also be con-
sidered in two subgroups as weakly right-handed (GSs from 30 to 5 0 ) and strongly
right-handed (GSs from 55 to 100) subjects.
Females did not include weakly right-handed subjects. Consequently, two subgroups
could be distinguished in these subjects: moderately right-handed (GSs from 55 to
80) and strongly right-handed subjects (GSs from 85 to 100).
 28 U . TAN

ESTRAD IOL us HAND PREFERENCE

IN FEMALE SUBJECTS
70 :. . . .................................
\ :
............... :.............
: ' , \ :
60 .... ........ ......... ............j

50
40
30
20
20 50 80 110 140 170 200
SERUM ESTRfiD IOL (ng/rnL 1
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FIGURE 2 Regression of hand preference (Waterloo score) on serum estradiol level in female subjects
Abscissa: serum estradiol level (ng/mL) Ordinate: the degree of hand preference (Waterloo handedness
score). Y = 60.2 - 0.2 X .

Hand Preference And Sex Hormones In Females

Total testosterone There was no significant correlation between serum total testos-
terone levels and the degree of the right-hand preference in moderately right-handed
females ( r = - . 11, t = 0.48, df = 18, p = .64). There was no significant correlation
between serum total testosterone levels and the degree of the right-hand preference
in strongly right-handed females ( r = .15, t = 0.46, df = 10, p = .66).

Free testosterone There was no significant correlation between serum free testos-
terone levels and the degree of the right-hand preference in moderately right-handed
females ( r = .19, f = 0.80, df = 19, p = .43). The free serum testosterone levels
did also not show any significant correlation with the degree of right-hand preference
in strongly right-handed females ( r = -.08, t = 0.25, df = 10, p = .81).

Sex hormone binding globulin (SHBG) The serum SHBG levels did not exert any
significant correlation with the degree of the right-hand preference in moderately ( r
= -.14, f = 0.60, df = 19, p = .56) and strongly right-handed ( r = .33, = 1.05,
df = 10, p = .32) female subjects.

Estradiol The serum estradiol level was found to be negatively linearly and sig-
nificantly correlated with the degree of right-hand preference in moderately right-
handed female subjects ( r = -.54, t = 2.20, df = 13, p = .048). There was also
a significant negative linear correlation between serum estradiol levels and the degree
of right-hand preference in strongly right-handed female subjects ( r = -.go, t =
3.23, df = 7 , p = .018).
There was also a significant negative linear correlation between serum estradiol
level and the degree of right-hand preference in the total sample of female subjects
( r = -.70, t = 4.40, df = 21, p = .000). Figure 2 illustrates this relationship.
 HAND PREFERENCE AND SEX HORMONES 29

A . HAND PREFERENCE us TESTOSTERONE

lGSs FROM 30 TO 50)
...................................................
35
30
25
20
, . . . . . . . . .' . . . . . . . . .\ . . . . . .
(I:
15 L..........

3
10
300 400 500 600 700 800
TESTOSTERONE (ng/mL 1
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B. GSs FROM 55 TO 100

1;:. .......'. ... ;. ... .:. ......... . I . ......,: .............. ... .:.
70
1
1 : ,

I - .

60
50 1

u
40!
30
3 .....................-. ..
20 1. .
2 ,
. . . . . . . . . . . . . . . . . . . . . . . . . .
. . . . . . . . . . . . . . . . . . . . . .
h

0 2 4 6 8 1 0 1 2
TESTOSTERONE [ng/mL$X 1001
FIGURE 3 Regression of hand preference on serum total testosterone level in male subjects Abscissa:
serum testosterone (ng/ml) Ordinate: the degree of right-handedness (Waterloo Handedness score). A:
weakly right-handed subjects (Y = 33.9 - 0.2 X); B: moderately and strongly right-handed subjects
(Y = 51.6 - 0.1 X).

Sex Hormones And Hand Preference In Male Subjects

Total testosterone In weakly right-handed males (GSs from 30 to 5 0 ) , there was a

significant negative linear correlation between the degree of the right-hand preference
and serum total testosterone level ( r = -.86, t = 3.74, df = 6, p = .013). Figure
3A illustrates this relationship.
There was also a significant negative linear correlation between serum total tes-
tosterone level and the degree of right-hand preference in strongly right-handed males
(GSs > 50; r = -.27, t = 2.49, df = 77, p = .015). Figure 3B illustrates this
relationship.
 30 U. TAN

Free testosterone In weakly right-handed male subjects, there was no significant

correlation between serum free testosterone level and the degree of the right-hand
preference ( r = -.54, t = 1.43, d f = 6, p = .21).
Similarly, there was a negative linear correlation between the degree of right-hand
preference and serum free testosterone level, in moderately right-handed males, but
this relationship was found to be only marginally significant ( r = -.47, t = 2.06,
df = 16, p = .057).
In strongly right-handed males, there was no significant correlation between the
degree of right-hand preference and serum free testosterone level ( r = .04, t = 0.31,
df = 63, p = .76).

Sex hormone binding globulin In weakly right-handed males, the degree of the
right-hand preference was found to be negatively linearly and significantly correlated
with serum SHBG level (Figure 4A: r = -.81, t = 2.79, df = 5 , p = .049).
In moderately right-handed males, there was no significant correlation between
the degree of right-hand preference and serum SHBG levels (Figure 4B: r = .37, t
= 1.55, df = 16, p = .14).
In strongly right-handed males, the degree of the right-hand preference was found
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to be negatively linearly and significantly correlated with serum SHBG level (Figure
4C: r = -.33, t = 2.59, d f = 56, p = .012).

Estrudiol In weakly right-handed males, the degree of the right-hand preference

was found to be negatively linearly and significantly correlated with serum estradiol
level (Figure 5A: r = -.83, t = 2.96, d f = 5 , p = .041). There was also a significant
negative linear correlation between the degree of right-hand preference and serum
estradiol levels in strongly right-handed males including moderately right-handed
males (Figure 5B: r = -.24, t = 2.13, df = 74, p = .037).

DISCUSSION

The results of this work showed that hand preference in males was inversely influ-
enced by almost all gonadal hormones. On the contrary, hand preference in females
was inversely influenced only by estradiol. It is now generally accepted that females
are more right-handed than males (see Annett, 1985; Tan, 1988 a). Preponderance
of right-preferents was also found to be higher in female cats than male cats (Tan
et al., 1990; Tan & Kutlu, 1991 f). Thus, right-preference in handedness seems to
be less pronounced in males than females. It was suggested that right-preference
might be determined by a female right shift factor (Tan & Kutlu, 1991 b). The results
of the present work now show that, indeed, right-preference in females and males
is mainly determined by a female hormone “estradiol.” The results also suggested
that less pronounced right-handedness in males may be caused by additional sex
hormones such as testosterone and SHBG. However, it was also shown that testos-
terone propionate injected intramuscularly reduced the degree of right-paw prefer-
ence only in right-preferent female cats (Tan et al., 1991 a). Thus, if females had
testosterone in significant amounts, they would be equally less right-preferent as
males.
Although the results of the present work are based on young adults, these results
may also be valid for the whole developmental stages of the nervous system in-
cluding fetal development. Sengstake and Chambers (1991) have indeed suggested
that the amount of testosterone required to activate the prolonged extinction of a
 HAND PREFERENCE AND SEX HORMONES 31

A . WATERLOO ON SHRG (WEAK RHs)

35
30
25
20
15
10
40 60 80 100
SERUM SHBG (ny,mL1
B . MODERATELY R-H MALES
60
50
40
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30
20
0 30 60 90 120 150
SHBG Ing/mL)

C. STRONGLY R-H MALES

20 40 60 80 100
SHBG (ng/mL 1
FIGURE 4 Relationship between hand preference and serum SHBG in male subjects Abscissa: serum
SHBG (ng/mL) Ordinate: the degree of the right-hand preference (Waterloo Handedness score). A:
weakly right-handed subjects ( Y = 33.4 - 0.1.5 X): B: moderately right-handed subjects ( Y = 33.3 +
0.09 X); C: strongly right-handed subjects ( Y = 59.04~ 0.21 X).

conditioned taste aversion depends on perinatal exposure to testosterone. If so, the

inverse relation of serum testosterone to the degree of right-hand preference in human
male subjects and female cats partly support the testosterone hypothesis of cerebral
lateralization (Geschwind & Behan, 1982; Geschwind & Behan, 1985 a , b).
The results of the present work suggested that a female right shift factor (see also
Tan & Kutlu, 1991 b) should also be considered as an important factor in emergence
of right handedness. Respectively, Diamond’s experiments (see 1987) carried out in
rats are very impressive. This author reported that there are estrogen receptors in
both male and female rat cerebral cortices at birth, being more in the left cortex of
 32 U. TAN

A. HAND PREFERENCE us ESTRADIOL

[WEAKLY RH MALES)
49
35
30
25
20
15
101: . . . : . . . I
'2-

. . .+-a
5-.
' . ' A
30 50 70 90 110
ESTRAD IOL Ing/mL 1
Downloaded By: [TÜBTAK EKUAL] At: 13:19 7 August 2009

20 40 60 80 100 120
ESTRADIOL Ing#mL1
FIGURE 5 Relationship between hand preference and serum estradiol level in right-handed male sub-
jects Abscissa: serum estradiol level (ng/mL) Ordinate: the degree of right-hand preference (Waterloo
handedness score). A: weakly right-handed subjects (Y = 35.6 - 0.19 X); B: moderately and strongly
right-handed subjects (Y = 51.9 - 0.1 X ) .

males and in the right cortex of females. Accordingly, the male right cortex is thicker
than the left, and the female cortex is thicker on the left side in the majority of cases.
The present work offers some important results supporting a female right shift factor
(most probably estrogen) in emergence and shaping of right-hand preference. The
results also suggested that gonadal hormones may influence cerebral lateralization
throughout the whole developmental stages ranging from fetal life up to the end of
puberty.
I have frequently studied the association of serum testosterone level to hand pref-
erence and hand skill and have reported that serum total testosterone level shows a
negative linear correlation with the degree of right-hand preference (Oldfield Ques-
 HAND PREFERENCE AND SEX HORMONES 33

tionnaire) in young adults -only in FS+ males and in the total sample of females
(Tan, 1990 a). The present work showed that total testosterone is associated with
hand preference (Waterloo questionnaire) only in males. Thus, the inverse relation-
ship between serum testosterone and the degree of right-hand preference in males
seems to be well established. However, this relationship was not always seen in
females, probably because of different questionnaires used. Moreover, testosterone
in females might show more fluctuations than that in males.
As might be expected, females’ manual lateralization seems to be influenced mainly
by the female sex hormone estradiol. However, hand skill and hand performance
was found to be influenced by testosterone in male and female human subjects (Tan,
1990 b,c). Thus, testosterone seems to influence handedness in both males and fe-
males. I have indeed also found that the mean serum testosterone level is signifi-
cantly higher in male and female human subjects with anomalous dominance than
those with standard dominance (Tan, 1991).

REFERENCES
Downloaded By: [TÜBTAK EKUAL] At: 13:19 7 August 2009

Annett, M. (1985). Left, right, hand and brain; The right shqt theory. London: Lawrence Erlbaum
Associates Ltd., Publishers.
Bedard, P., Langelier, P . , & Villeneuve, A . (1977). Estrogens and extrapyramidal system. The lancet,
Dec. 24, 1367-1368.
Berbardi, M., Genedani, S . , Tagliavini, S . , & Bertolini, A . (1989). Effect of castration and testosterone
in experimental models of depression in mice. Behaviorul Neuroscience, 103, 1148-1 150.
Buterbaugh, G . G., & Hudson, G. M. (1991). Estradiol replacement to female rats facilitates dorsal
hippocampal but not ventral hippocampal kindled seizure acquisition. Experimental Neurology,
111, 55-64.
Corsi-Cabrera, M . , Herrera, P., & Malvido, M . (1989). Correlation between EEG and cognitive abil-
ities: sex differences. International Journal of Neuroscience, 45, 133-141.
Demotes-Mainard, J., Arnauld, E . , & Vincent, J . D. (1990). Estrogens modulate the responsiveness of
in vivo recorded striatal neurons to iontophoretic application of dopamine in rats: role of D1 and
D2 receptor activation. Journal of Neuroendocrinology, 2 , 825-832.
De Vries, G . J. (1990). Sex differences in neurotransmitter systems. Journal of Neuroendocrinology,
2, 1-13.
Diamond, M. C. (1987). Sex differences in the rat forebrain. Brain Research Reviews, 12, 235-240.
Earley, C . J . , & Leonard, B. E. (1978). GABA and gonadal hormones. Brain Research, 155, 27-34.
Eaton, W . O., & Enns, L. R. (1986). Sex differences in human motor activity level. Psychological
Bulletin, 100, 19-28.
Euvrard, C . , Labrie, F., & Boissier, J . R. (1979). Effect of estrogen on changes in the activity of striatal
cholinergic neurons induced by DA drugs. Bruin Research, 169, 215-220.
Geschwind, N . , & Behan, P. 0. (1982). Left-handedness: association with immune disease, migraine,
and developmental learning disorder. Proceedings of the National Academy of Sciences, U S A, 79,
5097-5 100.
Geschwind, N., & Galaburda, A. M. (1985 a). Cerebral lateralization: biological mechanisms, and
pathology: I . a hypothesis and a program for research. Archives of Neurology, 42, 428-459.
Geschwind, N . , & Galaburda, A. M. (1985 b). Biological mechanisms, associations, and pathology:
11. a hypothesis and a program for research. Archives of Neurology, 42, 521-552.
Hampson, E. ( 1990). Estrogen-related variations in human spatial and articulatory-motor skills. Psy-
choneuroendocrinology. 15, 97-1 I 1 .
Hampson, E . , & Kimura, D. (1988). Reciprocal effects of hormonal fluctuations on human motor and
perceptual-spatial skills. Behavioral Neuroscience, 102, 456-459.
Hanske-Petitpierre, V . , & Chen, A. C. N . (1985). Sex differences in brain organization: implications
for human communication. International Journal of Neuroscience, 28, 197-2 14.
Hines, M . , & Shipley, C. (1984). Prenatal exposure to diethylstilbestrol (DES) and the development of
sexually dimorphic cognitive abilities and cerebral lateralization. Developmental Psychology, 20,
81-94.
Jiiptner, M . , & Hiemke, C. (1990). Sex differences in GABAa receptor binding in rat brain measured
by an improved in vitro binding assay. Experimental Brain Research, 81, 297-302.
 34 U. TAN

Lapchak, P. A , , Araujo, D. M., Quirion, R . , & Beaudet, A. (1990). Chronic estradiol treatment alters
central cholinergic function in the female rat: effect on choline acetyltransferase activity, acetyl-
choline content, and nicotinic autoreceptor function. Brain Research, 525, 249-255.
Mann, V., Sasanuma, S., Sakuma, N., & Masaki, S. (1990). Sex differences in cognitive abilities: a
cross-cultural perspective. Neuropsychologia, 28, 1063- 1077.
Michard-VanhCe, C . , & Roubertoux, P. (1990). Genetic analysis of differences in behavioral reactivity
to neonatal injection of testosterone in female mice. Behavior Genetics, 20, 63-71,
Nass, R., Baker, S., Sadler, A. E., & Sidtis, J . J. (1990). The effects of precocious adrenarche on
cognition and hemispheric specialization. Brain and Cognition, 14, 59-69.
Nieschlag, E., & Loriaux, D. L. (1972). Radioimmunoassay for plasma testosterone. Zeitschrqt fiir
Klinische Chemie und klinische Biologie, 10, 164-168.
Oldfield, R. C. (1971). The assessment and analysis of handedness: The Edinburgh Inventory. Neu-
ropsychologia, 9, 97-1 14.
Primus, R. J . , & Kellogg, C . K. (1990). Gonadal hormones during puberty organize environment-related
social interaction in the male rat. Hormones and Behavior, 24, 31 1-323.
Schumacher, M. (1990). Rapid membrane effects of steroid hormones: an emerging concept in neu-
roendocrinology. Trends in Neurosciences, 13, 359-361.
Sengstake, C. B., & Chambers, K . C. (1991). Sensitivity of male, female, and androgenized female
rats to testosterone during extinction of a conditioned taste aversion. Behavioral Neuroscience, 105,
120- 125.
Signorellar, M. L., & Jamison, W. (1986). Masculinity, femininity, androgeny, and cognitive perfor-
mance: a meta analysis. Psychological Bulletin, 100, 207-228.
Downloaded By: [TÜBTAK EKUAL] At: 13:19 7 August 2009

Steenhuis, R. E., & Bryden, M. P. (1989). Different dimensions of hand preference that relate to skilled
and unskilled activities. Cortex, 25, 289-304.
Tan, U . (1988 a). The distribution of hand preference in normal men and women. International Journal
of Neuroscience, 4 1 , 35-55.
Tan, U. (1988 b). The relationship between nonverbal intelligence, familial sinistrality and Geschwind
scores in right-handed female subjects. International Journal of Neuroscience, 43, 177- 182.
Tan, U. (1990 a). Relation of testosterone and hand preference in right-handed young adults to sex and
familial sinistrality. International Journal of Neuroscience, 53, 157- 165.
Tan, U . (1990 b). Testosterone and hand skill in right-handed men and women. International Journal
ofNeuroscience. 53, 179-189.
Tan, U. (I990 c). Testosterone and hand performance in right-handed young adults. International Jour-
nal of Neuroscience, 54, 267-276.
Tan, U. (1990 d). Testosterone and nonverbal intelligence in right-handed men and women. International
Journal of Neuroscience, 5 4 , 277-282.
Tan, U. (1990 e). Relationship of testosterone and nonverbal intelligence to hand preference and hand
skill in right-handed young adults. International Journal of Neuroscience, 54, 283-290.
Tan, U . , Yaprak, M., & Kutlu, N. (1990 f). Paw preference in cats: distribution and sex differences.
International Journal of Neuroscience, 50, 195-208.
Tan, U. (1991). Serum testosterone levels in male and female subjects with standard and anomalous
dominance, International Journal of Neuroscience, 58, 21 1-2 14.
Tan, U . , Kara, I., & Kutlu, N. (1991 a). The effects of testosterone on paw preference in adult cats.
International Journal of Neuroscience, 56. 187- 191.
Tan, U . , & Kutlu, N. (1991 b). The distribution of paw preference in right-, left-, and mixed pawed
male and female cats: the role of a female right-shift factor in handedness. International Journal
of Neuroscience, 59. 219-229.
Thomas, J . R., & French, K. E. (1985). Gender differences across age in motor performance: a meta
analysis. Psychological Bulletin, 98, 260-282.
van Hest, A., van Kempen, M., van Haaren. F., & van de Poll, N. E. (1988). Memory in male and
female Wistar rats: effects of gonadectomy, and stimulus presentations during the delay interval.
Behavioural Brain Research, 29, 103-1 10.
Vijayan, E . , & McCann, S. M. (1978). The effects of intraventricular injection of gamma-aminobutyric
acid (GABA) o n prolactin and gonadotropin release in conscious female rats. Brain Research, 155.
35-43.