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Relation of testosterone and hand preference in right-handed young adults to


sex and familial sinistrality
Üner Tan a
a
Atatürk University, Medical Faculty, Institute of Physiology, Erzurum, Turkey

Online Publication Date: 01 August 1990

To cite this Article Tan, Üner(1990)'Relation of testosterone and hand preference in right-handed young adults to sex and familial
sinistrality',International Journal of Neuroscience,53:2,157 — 165
To link to this Article: DOI: 10.3109/00207459008986597
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Intern. J . Neuroscience, 1990, Vol. 53, pp. 157-165 0 1990 Gordon and Breach Science Publishers S.A.
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RELATION OF TESTOSTERONE AND HAND


PREFERENCE IN RIGHT-HANDED YOUNG ADULTS
TO SEX AND FAMILIAL SINISTRALITY
UNER TAN
Atatiirk University, Medical Faculty, Institute of Physiology, Erzurum, Turkey

(Received March I , 1990)

The relationship between serum testosterone level and the degree of hand preference was studied in
right-handed young adults. Hand preference was assessed by the Edinburgh Handedness inventory. Serum
testosterone level was determined using tritium-marked-radioimmunoassay.There was no significant
correlation between these variables in males without FS. In males with FS and in females with and without
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FS, the serum testosterone levels were found to be negatively linearly correlated with the degree of the
right-hand preference. Similar results were obtained with respect to foot and eye preferences. It was
concluded that not only prenatal testosterone but adult testosterone also may exert a life long influence on
cerebral lateralization; this effect seems to be much more pronounced in the female than male brain, which
may exert a female-like pattern under genetic control.

Keywords: testosterone. hand preference. sex, cerebral lateralization, male, female

It now seems to be well established that there are sex-related differences in motor and
cognitive lateralization in humans and animals. The idea of a chance variation in the
origin of the hand or paw preference in animals as apparently substantiated empiric-
ally now exhibits a transformation toward a more plausible notion compatible with
findings in humans that have suggested that cerebral asymmetry is largely determined
by biological factors (see for review Geschwind & Galaburda, 1984; Arnold & Bottjer,
1985; Denenberg & Yutzey, 1985; Diamond, 1985; Galaburda et al., 1985; Gesc-
hwind, 1985; Glick & Shapiro, 1985; Robinson, 1985; Robinson et al., 1985; Sherman
& Galaburda, 1985; Tan, 1987; Bianki, 1988). Accordingly, we have recently reported
that there is a slight right-bias in the distribution of paw preferences in cats, which was
essentially induced by a preponderance of right preference in female cats indicating
that biological factors such as sex hormones may be involved in the origin of motor
lateralization in these animals (Tan et al., in press b). We have also shown that the
degree of paw preference in cats may reflect a biochemical asymmetry in the brain,
since imipramine and lithium were found to increase and decrease the asymmetry in
paw preference, respectively (Tan et al., in press a).
Sex hormones were shown to be capable of affecting electrical and biochemical
features of the neurons (Vernikos-Danellis, 1972; Clark & Peck, 1979; Whalen, 1982;
Vague, 1983). It was indeed reported that there are steroid hormone receptors in the
human brain for all five classes of steroids: estrogens, progestins, androgens, gluco-
corticoids, and mineralocorticoids (see for review Greenstein, 1978; Pfaff & McEwen,
1983). Geschwind and Behan (1982) have speculated that testosterone may play a
major role in the development of brain asymmetry in humans, which may create
differences in motor and cognitive asymmetris observed between the sexes. The
contribution of prenatal sex hormones, especially testosterone, to motor-cognitive
lateralization was clearly demonstrated by animal research (Rosen et al., 1983;
Denenberg, 1984; Glick & Shapiro, 1984; Diamond, 1984, 1985; Denenberg 8z Yut-

157
158 u. TAN
zey, 1985). Sanders and Ross-field (1987) have suggested as a new research strategy
that prenatal gonodal hormones influence the development of the brain to produce
the differences in cerebral asymmetry that are thought to be the basis of sex differences
in cognitive ability.
The above mentioned studies are concerned with the prenatal hormonal effects on
the developing brain. It is also conceivable that prenatal hormone levels can be related
to hormone levels at birth and childhood, which may further influence motor and
cognitive development. Moreover, the circulating hormones may also be of impor-
tance in adolescence with respect to motor-cognitive abilities. Diamond (1985) has
provided evidence for a significant relationship between age and asymmetry in rat
forebrain morphology. There are also reports emphasizing the importance of the
adult levels of sex hormones for cognitive differences between the sexes (Petersen, et
al.. 1976; Broverman et al., 1964, 1968; Klaiber et al., 1967). Christiansen and
Knussmann (1987) have studied the relation of the serum concentration of testos-
terone to cognitive ability in young men, and found that serum androgen levels are
positively correlated with measures of spatial ability, and negatively correlated with
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measures of verbal production.


As seen from the above summarized literature, there are some reports on the
relation of serum testosterone levels to cognitive ability in adults. However, there is
no such study concerning the relation of testosterone to hand preference, which has
been frequently reported to show important correlations with cognitive abilities. It is
then conceivable to assume that serum testosterone levels may also be associated with
the degree of hand preference in adults. In the present work, an attempt was made to
tesf this hypothesis. The results provided evidence that there are important relation-
ships between the serum testosterone levels and the degree of hand preference in
young adults depending upon sex and history of familial left-handedness.

METHODS

Subjects and Assessment of Hand, Foot, and Eye Preference


Subjects were 44 male and 17 female right-handed students ranging in age from 17 to
19 years. They were healthy, devoid of neurological and psychiatric signs and symp-
toms.
Hand preference was assessed by the Edinburgh Handedness Inventory (Oldfield,
197I). Following Geschwind’s suggestion (personal communication), a laterality
score was obtained, and no quotient was calculated. In memory of Norman Gesc-
hwind, this laterality score was called a s Geschwind score, which was abbreviated as
GS (see Tan, 1988). Factor analysis of the Edinburgh handedness factor showed that
it does indeed measure a unitary handedness factor that is stable across sex over a
test-retest interval (McFarland & Anderson, 1980; White & Ashton, 1976).
Eye preference was tested by sighting through a hollow tube; they were first asked
which eye they would prefer. Subjects were also asked about the preferred foot in
kicking a ball.
Familial sinistrality was scored as positive where there was left-handedness in at
least one first degree, or two second degree relatives, according to the subjects
self-report.

Hormone Assay
The venous blood was taken into a lithium test tube. The plasma was separated.
TESTOSTERONE AND HANDEDNESS 159
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i ? ! 3 8 8 F % 4 -8 2
HAND PREFERENCE (GS)
FIGURE 1 Relation of serum testosterone level to the degree of right-hand preference in male right-
handers *Abscissa: hand preference (GS) Ordinate: serum concentration of testosterone (ng/dL). Open
squares, dashed line: subjects without Fs (Y = 1005.2 - 3.3X, r = - .24, df = 31, p > .05). Crosses,
straight line: subjects with FS (Y = 1205.0 - 6.2X, r = - .62, df = 9, p < .05).

Serum testosterone level was determined by using tritium-marked radio-immunoas-


says (Nieschlag & Loriaux, 1972).

RESULTS

Relation of Serum Testosterone Level to Hand Preference

Male subjects ( N = 44). Figure 1 shows the relationship between the degree of the
right-hand preference and serum testosterone level in male right-handers. In subjects
without FS ( N = 33), these two parameters were found to be negative by linearly
related (open squares, dashed line), but the correlation was not significant at 5%
significance level (r = - .24, df = 31, p > -05, CD% = 5.8). In subjects with FS
( N = I I ) , there was a significant negative by linear relationship between serum
testosterone level and the degree of the right-hand preference (crosses, straight line)
with a coefficient of determination (CD%) of 38.3%; the correlation was found to be
significant at 5% significance level (r = .62, r = - .62, df = 9, p < .05,
CDYo = 38.30.

Female subjects ( N = 17). Figure 2 shows the relationship between serum testos-
terone level and the degree of the right-hand preference in femal right-handers. In the
total sample, there was a negative linear relationship between these parameters (open
squares, dashed line). The correlation was found to be significant ( r = - .66;
p < .01; CD% = 43.8). In subjects without FS ( N = 14), a similar relationship was
established (r = - .67, p < .01; CD% = 44.7). There were only three subjects with
FS. Therefore their data were not subjected to a statistical analysis.
I 60 u. TAN
0 Total
X FS-
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8 R 8 s: 8
r
5!
r

HANG PREFERENCE (GS)

FIGURE 2 Relation of serum testosterone level to the degree of the right-hand preference in femal
right-handers *Abscissa: hand preferences (GS) Ordinate: serum concentration of testosterone (ng/dL).
Open squares, dashed line: total sample (Y = 224.8 - 2.0X, r = - .66, df = 15, p < .01). Crosses,
straight line: subjects without FS (Y = 266.4 - 2SX, r = - .67, p < .01).

Relation of Serum Testosterone Level to Hand Preference With Respect to Foot


Preference

Male subjecfs ( N = 3 2 ) . Figure 3 shows the relationship between testosterone level


and the degree of the right-hand preference in male subjects with right-foot prefer-
ence. In the total sample, there was a significant negative by linear relationship
between these parameters (open squares, dashed line). This correlation was found to
be significant (r = - . 3 6 , p < .05; CD% = 13.1). In subjects without FS (N = 22),
there was no significant relationship between serum testosterone level and the degree
of the right-hand preference (crosses, straight line). However, the relation could be
described by a linear equation (r = - .22, p > .05, CD% = 4.8). The serum testos-
terone level was found to be significantly related to the degree of hand preference in
subjects with FS ( N = 10). The correlation was found to be negative by linear and
significant at 5% significance level (r = - .73, CD% = 53.7).
In subjects with ambilaterality in foot preference, there was a negative linear
relationship between serum testosterone level and the degree of the right-hand prefer-
ence. The correlation was found to be significant r = - .66, df = 10, p < .05,
CD% = 44.2).

Feniale subjects ( N = 16). There was a negative linear relationship between serum
testosterone level and the degree of right-hand preference in female subjects with
right-foot preference and no FS (Figure 4: open squares, dashed line). The correlation
was found to be highly significant ( r = - .78, df = 14, p <.001, CD% = 60.5).
The subjects with FS could not be analyzed because of very small sample size
( N = 3).
TESTOSTERONE AND HANDEDNESS 161

0 TOTAL
x Fs-
0 Fs+
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0
x 8 0
k. 8 B 8c
2
r

HAND PREFERENCE (GS)


FIGURE 3 Relationship between serum testosterone level and the degree of the right-hand preference in
male left-handers to foot preference *Abscissa: had preferences (GS) Ordinate: serum concentration of
testosterone (ng/dL). Open squares, dashed line: subjects with right-foot preference, total sample
(Y = 1079.1 - 4.6X, r = - .36, df = 30,p < .05). Crosses, straight line: subjects with right-foot prefer-
ence and no FS (Y = 845.3 - 2.2X, r = - .22, df = 20, p > .05). Triangles, dotted line: subjects with
right-foot preference and FS (Y = 1357.8 - 7.8X, r = - .73, df = 6, p < .05).

Relationship Between Serum Testosterone Level and The Degree of Hand Preference
in Subjects With Respect to Eye Preference

Female subjects ( N = 11). In female subjects with right-eye preference, there was
a negative linear relationship between serum testosterone level and the degree of
right-hand preference in the total sample (Figure 4: crosses, straight line). The
correlation was found to be highly significant ( r = - .76, df = 9, p < .01,
DC% = 57.2). In subjects with ambilaterality in eye preference ( N = 4), the serum
testosterone level was also found to be negative by linearly related to the degree of the
right-hand preference (Figure 4: triangles, dotted line). The correlation was significant
at 5% significance level ( r = - .96, df = 2, p < .05, CD% = 92.7).

Male Subjects ( N = 29). Figure 5 shows the relation of serum testosterone level to
the degree of the right-hand preference in male right-handers with right-eye prefer-
ence. In the total sample, a negative linear relationship was established between these
parameters (squares, dashed line), but the correlation was not significant at 5%
significance level ( r = - .33, CD% = 10.8). In subjects with right-eye preference
and no FS ( N = 23), there was also no significant correlation between these variables
(crosses, straight line, r = - .28, CD% = 7.8). In subjects with FS ( N = 7), the
serum testosterone level was found to be negative by linearly related to the degree of
the right-hand preference (triangles, dotted line). The correlation was found to be
significant ( r = - .85, df = 5, p <.05, CD% = 72).
In subjects with ambilaterality in eye preference, there was no significant correla-
tion between the serum testosterone levels and the degree of the right-hand preference
162 u. TAN
0 R-fWED
K R-EYED
0 M- NED
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0 S 8 R B P 8
r
2
r

HAND PREFERENCE (CS)


FIGURE 4 Relationship between serum testosterone level and the degree of right-hand preference with
respect to foot and eye preference in female right-handed subjects *Abscissa: hand preference (GS)
Ordinate: serum concentration level (ng/dL). Open circles, dashed line: subjects with right-foot preference
and no FS (Y = 247.2 - 2.3X, r = - .76, df = 9, p <.Ol). Triangles, dotted line: subjects with am-
bilaterality in eye preference (Y = 482.2 - S.OX, r = - .96, df = 2, p < .05).

D TOTAL
x FS-
V FS+

x 8 z 8 ti: 8
r
E
r

HAND PREFERENCE (GS)


FIGURE 5 Relationship between serum testosterone level and the degree of the right-hand preference
with respect to eye preference in male subjects *Abscissa: hand preference (GS)Ordinate: serum testos-
terone level (ng/dL). Squares, dashed line: total sample with right-eye preference (Y = 1139.5 - 5.3X,
r = - .33, d / = 27, p > .05). Crosses, straight line: subjects with right-eye preference and no FS
(Y = 1125.8 - 5.1X, r = - .28, df = 2 1 , p > .05). Triangles, dotted line: subjects with right-eye prefer-
ence and FS (Y = 1198.8 - 6.1X. r = - .85. df = 5 , p <.05).
TESTOSTERONE A N D HANDEDNESS 163

in the total sample ( v = - .31, df = 10, p>.O.5, C D % = 9.9, and in subjects


without FS (Y = - .42, df = 8, p>.O5, CD% = 17.6). However, these relations
could be described by linear equations. The subjects with ambilateral eye preference
and FS could not subjected to a statistical analysis because of the small sample size.

DISCUSSION

Interestingly, the results of this work showed that the serum testosterone level is
associated with the degree of the right-hand preference in young adults, indicating no
significant difference from studies accomplished in animals with prenatal testosterone
treatment. This is the first study in the literature providing evidence that there is a
sex-related negative correlation between the concentration of the serum testosterone
and the degree of the right-hand preference, which was assessed by the Edinburgh
Handedness Inventory measuring a unitary handedness factor that is stable across sex
and test-retest interval (McFarland & Anderson, 1980; White & Ashton, 1976).
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Geschwind and Behan ( 1982) have proposed that testosterone may delay the
growth of the left cerebral hemisphere in utero, and this effect will be greater in males
because the fetal testes secrete testosterone. It was assumed in the present work that
prenatal hormonal levels can be related to hormonal levels at birth, childhood, and
adolescence. This proposal and the Geshwind-Behan hypothesis suggested that serum
testosterone levels in young adults may be related to the degree of hand preference.
The results of this work are in accord with this hypothesis with the exception of the
male right-handers without FS. In fact, male subjects should be more vulnerable to
changes in the serum testosterone concentrations than females according to Gesch
wind-Behan hypothesis.
It was established that FS is an important factor creating a female-like male brain
with regard to androgen sensitivity of the sensory-motor system, since there was a
significant negative-linear relationship between the serum testosterone level and the
degree of the right-hand preference in males with FS like females and unlike males
without FS. It is conceivable that a sensitization against testosterone occurs in the
male brain during early prenatal development under some unknown genetic factors
creating a female-like pattern in the male brain.
The mechanisms of hormonal effects on the brain are not yet known. The working
hypothesis posits two types of effects: sensitization and activation (see Jacklin, 1989).
Sensitization probably occurs during the prenatal period, circulating hormones acting
to program the fetal brain. The circulating hormones during and after puberty may
then activate or interact with the sensitized brain to produce behavioral effects.
Jacklin et al. (1988) have provided support for this theory. In light of this theory, it
is plausible to assume that the circulating testosterone cannot interact with testos-
terone receptors in the male brain in utero provided that there is no facilitatory genetic
factors. In contrast, an early sensitization of the female or a female-like brain by
testosterone may occur during the prenatal period, and then the circulating testos-
terone may activate this sensitized female brain during and after puberty to produce
several degrees of motor lateralization.
An alternative hypothesis would be that hormonal levels at birth are related to
hormonal levels throughout childhood and adolescence. This may also contribute to
motor-cognitive development and its continuity to the end. Accordingly, Diamond
(1985) has reported that the definite asymmetric patterns in the rat brain, with the
right side being larger than the left, is more marked in the early than in the later part
of the animals’s life. Christiansen and Knussmann (1987) have shown that serum
164 u. TAN
testosterone levels are positively related to spatial skill and negatively related to verbal
skill in young men. Several researchers have argued that hormonal events at puberty
are also implicated in the development of cognitive sex differences. Waber (1 976,
1977) has reported that the late maturing adolescents of both sexes are more lat-
eralized for speech perception and exhibit better spatial skill than earlier maturing
adolescents of the same age.
The results of this work are in accord with animal research. It was demonstrated
that only a female or a feminized brain is appropriate for androgen-receptor interac-
tions within the motor system. Rosen et al. (1983) have reported that, in rat, prenatal
testosterone treatment causes a right shift in the neonatal tail posture for female pups,
but not for males. Denenberg (1984) stated, “The lack of differences among the male
groups is consistent with other data in the literature suggesting that at least in the rat
the female, but not the male, appears to be a more sensitive animal model to evaluate
many of the prenatal effects of androgens.” This conclusion seems now to be justi-
fiable in accord with the relation of androgens to motor lateralization even in young
human adults, which, however, may be modulated genetically, at least, in men.
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REFERENCES

Arnold, A.P., & Bottjer, S.W. (1985). Cerebral lateralization in birds. In S.D. Glick (Ed.), Cerebral
lateralization in nonhumun species. New York: Academic Press.
Bianki, V.L. (1988). The right a n d k j i hemispheres of the aniniul brain. New York: Gordon and Breach
Science Publishers.
Broverman, D.M., Broverman, J.K., Vogel, W., & Palmer, R.D. (1964). The automatization cognitive style
and physical development. Child Development, 35, 1343-1359.
Broverman, D.M., Klaiber, E.L., Kobayashi, Y., & Vogel, W. (1968). Roles of activation and inhibition
in sex differences in cognitive abilities. Psychological Reviews, 75, 23-50.
Christiansen, K., & Knussmann, R. (1987). Sex hormones and cognitive functioning in men. Neuropsycho-
biology, 18, 27-36.
Denenberg, V.H. (1984). Behavioral asymmetry. In N . Geschwind & A.M. Galaburda (Eds.), Cerebral
lateralirurion. Cambridge, Massachusets: Harvard University Press.
Denenberg, V.H., & Yutzey, D.A. (1985). Hemispheric laterality, behavioral asymmetry, and the effects of
early experience in rats. In S.D. Click (Ed.), Cerebral lateralization
Diamond, M.C. (1984). Age, Sex, and environmental influences. In N. Geschwind & A.M. Galaburda
(Eds.), Cerebral dominance. Cambridge, Massachusets: Harvard University Press.
Diamond, M.C. (1985). Rat forebrain morphology: right-left; male-female; young-old; enriched-
impoverished. In S.D. Click (Ed.), Cerebral laterulizution in nonhuman species. New York: Academic
Press.
Galaburda, A,, Sherman, G., & Geschwind, N. (1985). Cerebral lateralization on animal studies. In S.D.
Click (Ed.), Cerebral lateralization in nonhuman species. New York: Academic Press.
Geschwind, N. (1985). Implications for evolution, genetics, and clinical syndromes. In S.D. Click (Ed.),
Cerebral lateraliza/ion in nonhumun species. New York: Academic Press.
Geschwind, N., & Behan, P. (1982). Left-handedness: asociation with immune disease, migraine, and
developmental learning disorder. Proceedings of /he National Academy of Sciences, USA, 79, 5097-
5100.
Geschwind, N., & Galaburda, A.M. (1984). Cerebral dominance. Cambridge, Massachusets: Harvard
University Press.
Glick, S.D., & Shapiro, R.M. (1984). Functional and neurochemical asymmetries. In N . Geschwind &
A.M. Galaburda (Eds.). Cerebral luleraliztr/ion. Cambridge, Massachusets: Harvard Univeresity
Press.
Click, S.d., & Shapiro, R.M. (1985). Functional and neurochemical mechanisms of cerebral lateralization
in rats. In S.D. Click (Ed.), Cerebral lateralization in nonhuman species. New York: Academic Press.
Greenstein, B.D. (1978). Steroid hormone receptors in the brain. Trends in Neurosciences, 1, 4-6.
Jacklin, C.D. (1989). Female and male: issues of gender. American Psychologist, 44, 127-133.
Jacklin, C.N., Wilcox, K.T., & Maccoby, E.E. (1988). Neonatal sex-steroid hormones and intellectual
abilities of six year old boys and girls. Developmental Psychobiology, 21, 567-574.
Klaiber, E.L., Broverman, D.M., & Kobayashi, Y. (1967). The automatization cognitive style, androgens,
and monoamine oxidase. P.s.ychopharmacolo~y,II, 320-336.
TESTOSTERONE A N D HANDEDNESS 165

McFarland, K., & Anderson, J. (1980). Factor stability of the Edinburgh Handedness Inventory as a
function of test-retest performance, age, and sex. British Journal qf Psychology, 71, 135-142.
MacNeilage, P.F., Studdert-Kennedy, M.G., & Lindblom, B. (1987). Primate handedness reconsidered.
Behavioral and Brain Sciences. 10, 247-303.
Nieschlag, E., & Loriaux, D.L. (1972). Radioimmunoassay for plasma testosterone. Zeitschrift ,fir Kli-
nische Chemie und klinische Biologie, 10, 164-168.
Oldfield, R.C. (1971). The assessment and analysis of handedness: The Edinburgh Inventory. Neuropsy-
chologia, 9, 97-1 14.
Petersen, A.C. (1976). Physical androgyny and cognitive functioning in adolescence. Developmental Psv-
chology, 12, 524-533.
Pfaff, D.W., & McEwen, B.S. (1983). Actions of estrogens and progestins on nerve cells. Science, 219,
808-8 14.
Robinson, R.G. (1 985). Lateralized behavioral and neurochemical consequences of unilateral brain injury
in rats. In S.D. Glick (Ed.), Cerebral laterulizarion in nonhuman species. New York: Academic Press.
Robinson, T.E., Becker, J.B., Camp, D.M., & Mansour, A. (1985). Variation in the pattern of behavioral
and brain asymmetries due to sex differences. In S.D. Glick (Ed.), Cerebral lateralization in nonhuman
species. New York: Academic Press.
Rosen, G.D., Berrebi, A.S., Yutzey, D.A., & Deneberg, V.H. (1983). Prenatal testosterone causes shift of
asymmetry in neonatal tail posture of the rat. Developmental Brain Research. 9 , 99-101.
Sanders, G., & Ross-Field, L. (1987). Neuropsychological development of cognitive abilities: A new
Downloaded By: [TÜBTAK EKUAL] At: 13:28 7 August 2009

research strategy and some preliminary evidence for sexual orientation model. International Journal
of Neuroscience, 36, 1-16.
Sherman, G.F., & Galiiburda. A.M. (1985). Asymmetries in Anatomy and pathology in the rodent brain.
In S.D. Glick (Ed.), Cerebral lateralization in nonhuman species. New York: Academic Press.
Tan, 0.(1987). Paw preferences in dogs. International Journal of Neuroscience, 32, 825-829.
Tan, 0. (1988). The distribution of hand preference in normal men and women. International Journal of
Neuroscience, 41, 35-55.
Tan, u., Kara, I.. & Tan, S. (in press a). Lithium and imipramin effects on the paw preference in cats.
In!ernational Journal of Neuroscience.
Tan, U., Yaprak. M., & Kutlu. N. (in press b). Paw preference in cats: distribution and sex differences.
International Journal qf Neuroscience.
Waber, D.P. (1976). Sex differences in cognition: A function of maturation rate? Science, IY2, 572-574.
Waber, D.P. (1977). Sex differences in mental abilities, hemispheric lateralization, and rate of physical
growth a t adolesecence. Developmenla1 Psychology. 13, 29-38.
White, K., & Ashton, R . (1976). Handedness assessment inventory. Neuropsychologia, 14, 261-264.

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