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Relation of Serum Free-Testosterone Level to Grasp-Reflex Strength in Human

Neonates with Right-Ear and Left-Ear Facing out in-Utero Positions
Üner Tan a; Nevin Zor b
a
Department of Physiology, Medical Faculty, Atatürk University, Erzurum, Turkey b Department of Obstetrics
and Gynaecology, Medical Faculty, Atatürk University, Erzurum, Turkey

Online Publication Date: 01 March 1994

To cite this Article Tan, Üner and Zor, Nevin(1994)'Relation of Serum Free-Testosterone Level to Grasp-Reflex Strength in Human
Neonates with Right-Ear and Left-Ear Facing out in-Utero Positions',International Journal of Neuroscience,75:1,9 — 18
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 Intern. J . Neurosciettce, 1994. Vol. 75, pp. 9-18 0 1994 Gordon and Breach Science Publishers S.A.
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RELATION OF SERUM FREE-TESTOSTERONE

LEVEL TO GRASP-REFLEX STRENGTH IN
HUMAN NEONATES WITH RIGHT-EAR AND
LEFT-EAR FACING OUT IN-UTERO POSITIONS

UNER TAN
Department of Physiology, Medical Faculty, Atatiirk University, Erzurum, Turkey

NEVlN ZOR
Department of Obstetrics and Gynaecology, Medical Faculty, Atatiirk University,
Downloaded By: [TÜBTAK EKUAL] At: 13:51 7 August 2009

Erzurum, Turkey

(Received August 10, 1993)

The relation of the grasp-reflex strength to serum free-testosterone level was studied in human neonates
with right and left ear facing out in utero positions. The grasp-reflex strengths from the right and left
hands were found to be inversely correlated with testosterone in neonates with right-ear-out position. In
neonates with left-ear-out in utero position, the grasp-reflex strength only from the left hand inversely
correlated with testosterone. Left-dominance decreased and right dominance in grasp reflex increased
linearly with testosterone only in females with left-ear-out in utero position. These results supported the
theory of prenatal origins of cerebral lateralization (Previc, 1991). It was concluded that testosterone
may favour the maturation of both hemispheres in neonates with right-ear-out in utero position, and only
the right-hemispheric development in subjects with left-ear-out in utero position; testosterone may be a
male hormone influencing the cerebral lateralization on the ground of genetically and even environ-
mentally predetermined cerebral organization.

Kejwords: Grasp reflex. cerebral lateralization, testosterone, brain, human neonate.

Previc (1991) has created a new theory concerning the prenatal origins of cerebral
lateralization in humans. According to this theory, cerebral lateralization origins from
the asymmetric prenatal development of the ear and labyrinth. Namely, a vestibular
dominance occurred as a result of the position of the fetus during the final trimester;
the most frequently observed position of the fetus creates them a left-otolithic dom-
inance, which would promote right-sided motoric dominance in neonates. So, the
cerebral lateralization would depend upon the position of the fetus during the final
trimester. The fetal position may be right ear facing out or left ear facing out, but
predominantly right ear facing out. If this is true, the environmental factors must
influence the fetal development of cerebral motor lateralization differently according
to in utero position of the fetus during final trimester. In light of this argument, Tan
and Zor (in press) have recently studied the relationships between serum cortisol
level and grasp-reflex strength in human neonates. These authors have found that
the correlations between grasp reflex and cortisol depended upon fetal positions. This
supported the Previc’s theory of the cerebral motor lateralization.

Address correspondence to Prof. Dr. Uner Tan, Director, Department of Physiology, Medical Faculty,
Atatiirk University, Erzurum, Turkey.

9
 10 U TAN AND N. ZOR

Tan (in press) has reported that the grasp-reflex strength was related to serum free-
testosterone level in human neonates. This depended upon sex and hand dominance
of the neonates. Tan has then suggested that testosterone may influence brain mat-
uration according to a prenatally predetermined cerebral organization. If so, and Previc’s
theory is correct, testosterone should show relationships to testosterone according to
the fetal position during the final trimester. To test this hypothesis, we have mea-
sured the grasp-reflex strength quantitatively and assessed the fetal position in utero.
It will be shown in the present work that correlations between grasp-reflex strength
and testosterone varied according to the fetal positions with right-ear or left-ear fac-
ing out. The results supported the genetic as well as environmental origins of cerebral
lateralization.

METHODS
Subjects
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The results of the present work based on investigations with 24 neonates with right-
ear facing out in utero position, 18 neonates with left-ear facing out in utero position
during the final trimester. All of the neonates were full term and healthy. The po-
sition of the neonates was assessed by one of us (N. Z . ) in the Department of Gyne-
cology.

Hormone Assay
To measure the serum free-testosterone level, blood samples were taken from um-
bilical artery immediately just after birth. The serum free-testosterone level was then
quantitatively measured using a solide-phase, radioimmunoassay technique (Coat-A-
Count), which is commercially available (Diagnostic Products Corporation, USA).

Grasp Reflex
To measure the grasp-reflex strength quantitatively, a small balloon was attached to
a pressure transducer, which was connected to a polygraph. As the balloon was
brought into contact with the palmar surface of the neonate’s hand, the fingers re-
flexly closed, and the pressure was recorded by the polygraph. The grasp-reflex
strengths from the right and left hand were measure alternatively between hands in
ten trials. The mean grasp-reflex strengths were calculated for the right and left
hands.

RESULTS
Total Samples
Neonates with right-ear facing out ( N = 2 4 ) . Figure 1 shows the relations of the
grasp-reflex strengths from right (A) and left (B) hands to serum free-testosterone
levels in the total sample (males and females). The grasp-reflex strength from right
hand was found to be negatively linearly correlated with serum free-testosterone level
in neonates with right-ear facing out in utero. This correlation was found to be sta-
tistically significant ( r = -.52, t = 2.86, df = 23, p = .009; see Figure IA).
 TESTOSTERONE AND GRASP REFLEX 11

A. GRASP REFLEX IRIGHT) us TESTOSTERONE

IN RIGHT-EfiR-OUT NEONATES I TOTAL)

0 3 6 9 1215
testosterone Ipg/mL)
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B . GRASP REFLEX (LEFT) us TESTOSTERONE

IN R IGHT-EAR-OUT NEONATES ITOThL 1
10 ........................... ....................

0 3 6 9 1215
test 0sterone Ipg/mL 1
FIGURE 1 The relationships between the grasp-reflex strengths from the right (A) and left (B) hands
and serum free-testosterone levels in human neonates with right-ear facing out in utero position Abscissa:
serum free-testosterone level (pg/mL) Ordinate: grasp-reflex strength (arbitrary units). A: total sample,
right hand ( y = 8.8 - .08 x); B: total sample, left hand ( y = 8.8 - .09 x).

The grasp-reflex strength from left hand also negatively linearly correlated with
serum free-testosterone level in the total sample. This correlation was higher for that
for the right hand (r = -.67, t = 4.12, df = 22, p = .OOO; see Figure 1B).

Neonates with left-ear facing out (N = 18). Figure 2 shows the relations of the
grasp-reflex strengths from right (A) and left (B) hands to serum free-testosterone
levels in total neonates with left-ear facing out position in utero. There was no sig-
nificant correlation between the grasp-reflex strength from right hand and serum free-
testosterone level in these neonates (r = -.20, t = .85, d ! = 17, p = .41; see Figure
 12 U TAN AND N. ZOR

A . GRISSP REFLEX (RIGHT) us TESTOSTERONE

IN LEFT-EAR-OUT NEONATES (TOTAL)

4.5 6.5 8.5 10.512.514.5

testosterone (pg/mL 1
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GRCISP REFLEX [LEFT) us TESTOSTERONE

IN LEFT-EAR-OUT NEONATES (TOTAL)
I . : :. .: .:..:
I ,: . :. .:
.;. ,; . : . ;. .’..: . : . ;. .’. .: .: . i
.-..
. ._.
.

4.5 6.5 8.5 10,512.514.5

testosterone (pg/rnL)
FIGURE 2 The relationships between the grasp-reflex strengths from the right (A) and left (B) hands
and serum free-testosterone levels in the total sample Abscissa: serum free-testosterone level (pg/mL)
Ordinate: grasp-reflex strength (arbitrary units). A: right hand ( y = 8.9 - .O x x); B: left hand ( y =
9.6 - . I x).

2A). By contrast, the grasp-reflex strength from left hand was found to be negatively
linearly correlated with serum free-testosterone level in the same neonates. This cor-
relation was found to be statistically highly significant (r = -.76, t = 4.66, df =
I7, p = .OOO; see Figure 2B).

Mule Neonates
Mules with right-earfacing out ( N = 1 4 ) . Figure 3 shows the relations of the grasp-
reflex strengths from right and left hands to serum free-testosterone levels in the
 TESTOSTERONE AND GRASP REFLEX 13

fl, G M S P REFLEX (RIGHT) us TESTOSTERONE C. GRASP REFLEX (RIGHI) us IESIOSTERONE

IN RIGHI-EAR-OUT NEONATES (NALES) IN LEFT-EAR-OUT NEONATES (HALES)
10
5

ccr
E 7
0 3 6 9 1215 4.5 6.5 8.5 10.5 12.514.5
testosterone (pg/mL 1 testosterone [pg/mLl

6. 6RASP REFLEX (LEFT) us TESTOSTERONE D . GRASP REFLEX (LEFT) us TESTOSTERONE

IN RIGHT-EAR-OUT NEONATES (NfiLES) IN LEFT-EAR-OUT NEONfiTES (MALES)
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10 10
5 5b,
Ek 9 i
h
9
c, c,
M M
. a . 8
ccr
PI .. .. .. .. .. ..
.............................................
. . .
h 7
0 3 6 9 1215 4.5 6.5 8.5 10.5 12.514.5
testosterone (pg/mL) testosterone (pg/mL)
FIGURE 3 The relationships between the grasp-reflex strengths and serum free-testosterone levels in
neonates with right-ear-out (A, B) and left-ear-out (C, D) in utero positions Abscissa: serum free-tes-
tosterone level (pg/mL) Ordinate: grasp-reflex strength (arbitrary units). A: right hand in right-ear-out
male neonates ( y = 9.0 - .09 x ) ; B left hand in right-ear-out male neonates ( y = 9.1 - , I x); C: right
hand in left-ear-out male neonates ( y = 9.2 - .06 x); D: left hand in left-ear-out male neonates ( y =
9.6 - . I x).

male neonates with right- and left-ear facing out position in utero. The grasp-reflex
strength from right hand was found to be negatively linearly correlated with serum
free-testosterone level in males with right-ear-out position. This correlation was found
to be statistically significant ( r = -.60, t = 2.57, df = 13, p = .024; see Figure
3A). The grasp-reflex strength from left hand was also found to be negatively linearly
correlated with serum free-testosterone level in the same subjects. This correlation
was statistically significant and higher than that for the right hand ( r = -.80, r =
4.47, df = 12, p = .001; see Figure 3B).

Males with left-ear facing out (N = 10). There was no significant correlation be-
tween the grasp-reflex strength from right hand and serum free-testosterone level in
these neonates ( r = -.40,t = 1.23, df = 9, p = .25; see Figure 3C). There was,
however, negative linear correlation between the grasp-reflex strength from left hand
and serum free-testosterone level in these subjects. This correlation was found to be
statistically highly significant ( r = -.93, t = 7.33, df = 9, p = .OOO; see Figure
3D).
 14 U TAN AND N. ZOR

fl. GMP REFLEX (RIGHT) us IESMSTEI#IWEC . GMP REFLEX (RIGHT) us TESTOSTERONE

IN RIGHT-EI\R-WT NWWI\TES IFmLES) IN LEFT-EAR-WT NEONMES (FEIIALES)

0 2 4 6 8 5 . 6 6.6 7.6 8 . 6 9 . 6 10.6

testosterone (pg/mL) testosterone (pg/aL)

8 . GRASP REFLEX (LEFT) us TESTOSTERONE D . GRASP REFLEX (LEFT) us TESTOSTERONE

IN RIGHT-MR-MJT NEUMTES (FEMLES) IN LEFT-EAR-WT NEWTES (FEIIALES)
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0 2 4 6 8 5 . 6 6 . 6 7.6 8 . 6 9.6 10.6

testosterone (pg/nL 1 testosterone (pg/mL)

FIGURE 4 The relationships between the grasp-reflex strengths and serum free-testosterone levels in
female neonates Abscissa: serum free-testosterone level (pg/mL) Ordinate: grasp-reflex strength (arbi-
trary units). A: right hand in right-ear-out females ( y = 8.9 - .15 5 ) ; B: left hand in right-ear-out
females ( y = 8.7 - . I 2 x); C: right hand in left-ear-out neonates ( y = 8.7 - .04 x); D: left hand in
left-ear-out neonates ( s = 10.6 - .27 x).

Female Neonates

Females with right-ear-nut ( N = 10). Figure 4 shows the relations of the grasp-
reflex strengths from right and left hands to serum free-testosterone levels in the
female neonates. There was a negative linear correlation between the grasp-reflex
strength and testosterone in these subjects. This correlation was found to be statis-
tically just significant (r = - .63, t = 2.28, df = 9, p = .052; see Figure 4A). There
was also a negative linear correlation between the grasp-reflex strength from left
hand and testosterone in the same subjects. This correlation was found to be statis-
tically highly significant ( r = -.78, t = 3.55, df = 9, p = .008; see Figure 4B).

Females with left-ear-out ( N = 8 ) . There was no significant correlation between

the grasp-reflex strength from right hand and testosterone in these subjects ( r =
-.14. t = .35, df = 7, p = .74; see Figure 4C). There was, however, statistically
significant negative linear correlation between the grasp-reflex strength from left hand
and testosterone in the same subjects ( r = -.76, t = 2.91, df = 7, p = .027; see
Figure 4D).
 TESTOSTERONE AND GRASP REFLEX 15

R-L GRASP REFLEX US TESTOSTERONE IN

RIGHT-EAR-OUT NEONATES ITOTAL SAMPLE1

0 3 6 9 1215
testosterone (pg/mLl
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R-L GRASP REFLEX US TESTOSTERONE IN

LEFT-EM-OUT NEONATES ITOTAL SAMPLE 1
br
c
0
k
+t4

............................. :.. ......:. .......:

PC 4.5 6.5 8.5 10.512.514.5
testosterone (pg/mL 1
FIGURE 5 The relationships between R-L grasp-reflex strengths and serum free-testosterone levels in
the total sample Abscissa: serum free-testosterone level (pg/mL) Ordinate: R-L grasp-reflex strength
(arbitrary units). A: right-ear-out neonates; B: left-ear-out neonates ( y = -.71 + ,051
x).

Grasp-Reflex Asymmetry and Testosterone

Total samples. Figure 5 shows the relations of the R-L grasp-reflex strengths to
serum free-testosterone levels in neonates with right-ear-out (A) and left-ear-out po-
sitions. There was no significant correlation between the R-L grasp-reflex strength
and testosterone in neonates with right-ear facing out position in utero ( r = .02, t
= .07, df = 22, p = .94; see Figure 5A).
In neonates with left-ear facing out in utero position, the R-L grasp-reflex strength
was found to be positively linearly correlated with testosterone. This correlation was
found to be statistically significant ( r = .59, t = 2.89, df = 17, p = .011; see Figure
SB).
 16 U TAN AND N. ZOR

R-L GRASP REFLEX US TESTOSTERONE IN

LEFT-EAR-OUT NEONATES (FENALES1

0.5

0
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-0.5

-1
5 7 9 11

testosterone (pg/mL 1
FIGURE 6 The relationship between R-L grasp-reflex strength and testosterone in left-ear-out female
neonates Abscissa: serum free-testosterone level (pg/mL) Ordinate: R-L grasp-reflex strength (arbitrary
units; = -1.89 + .23 x).

Right- and lef-ear-out males. There was no significant correlation between the R-
L grasp-reflex strength and testosterone in these subjects ( r = .18, t = .61, df =
12, p = .55). There was also no significant correlation between the R-L grasp-reflex
strength and testosterone in the male neonates with left-ear facing out in utero po-
sition ( r = .47, t = l .49, df = 9, p = .17).
Right- and left-ear-out females. There was no significant correlation between the
R-L grasp-reflex strength and testosterone in right-ear-out females ( r = - . 2 3 , t =
.66, df = 9, p = .53). The R-L grasp-reflex strength was found to be positively
linearly correlated with testosterone in the left-ear-out female neonates. This cor-
relation was found to be statistically highly significant ( r = .92, t = 5.66, df = 7,
p = .001; see Figure 6).

DISCUSSION
The results of the present work showed that the relations of the grasp-reflex strengths
from the right and left hands to serum free-testosterone levels depended upon the
 TESTOSTERONE AND GRASP REFLEX 17

fetal positions in utero. So, this work supported the theory of prenatal origins of
cerebral lateralization (Previc, 1991).
The grasp-reflex strengths from the right and left hands were found to be inversely
correlated with serum free-testosterone levels in neonates with right-ear facing out
position. In neonates with left-ear-out position, however, only the grasp-reflex strength
from the left hand showed inverse correlation with testosterone. These relationships
were not sex-specific. Graph and Perpere (1968) have indeed reported that lateral
positioning immediately prior to birth did not significantly differ between males and
females.
Despite differential correlations in the neonates with right- and left-ear out posi-
tions, the grasp reflex from the left hand seemed to be more influenced by testos-
terone than that from the right hand. Only the grasp reflex form left hand was found
to be influenced by testosterone in neonates with left-ear out position. This strongly
supports the Previc’s theory of cerebral lateralization (see above). Previc has also
stated, however, that “asymmetric reflex strength in neonates cannot universally be
attributed to differential development of the labyrinths, as many of these reflexes
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(such as grasping) are clearly unrelated to antigravity functions. Rather, it is more

likely that greater reflex strength on the right side reflects the slower maturation of
the left posterior cortex and its inhibitory control. . . .” In contrast to this argument,
we have found that the relationship between grasp reflex and testosterone depended
upon fetal position. We do not know, however, the direct or indirect connections
between the vestibular system and grasp reflex in neonates.
If the testosterone effects on the grasp reflexes were considered in conjunction
with hemispheric maturation, it is conceivable that testosterone favours the hemi-
spheric maturation, since the grasp reflex is well known to disappear following cor-
tical maturation. The results of the present work suggest, then, that testosterone may
favour the maturation of both hemispheres in neonates with right-ear-out position.
However, the correlation between grasp reflex and testosterone was higher for the
left hand than the right hand in these subjects. By contrast, testosterone would be
advantageous only for the right-hemispheric maturation in neonates with left-ear-out
position, since testosterone affected only the grasp reflex from the left hand in these
subjects. Following this line of reasoning, it is conceivable that high testosterone
levels with weak grasp-reflex strengths from the right and left hands are compatible
with greater right and left hemispheric development under testosterone in subjects
with right-ear-out position. However, this correlation was particularly high for the
left hand. This indicates that testosterone is more favourable for the rapid maturation
of the right brain than the left brain, which may facilitate the emergence of right-
handedness. In frequently occurring right-ear-out position, testosterone may force
the motor development toward the ambidexterity in males, since testosterone affected
both hemispheric development in these subjects. On the other hand, testosterone may
force the development of right-handedness in females, since there was a direct re-
lationship between R-L grasp reflex and testosterone in these subjects. It is indeed
well established that females are more right-handed than males (Annett, 1973; Lan-
sky et al., 1988; Peters, 1986; Porac & Coren, 1981; Tan, 1988).
In accord with the conclusion that testosterone may favour especially the right-
hemispheric development, Galaburda et al. (1987) have reported that anatomical
asymmetries in the fetal brain would reflect greater right-hemispheric development
rather than reduced left-hemispheric development. On the other hand, Tan (1990)
has reported that the degree of right-hand preference decreased as serum testosterone-
14-levels increased in adult subjects. Probably, they were subjects with right-ear-out
in utero position, which occur most frequently than the left-ear-out in utero positions.
 18 U TAN AND N. ZOR

Moreover, Tan (1992) has also found that the degree of the R-L hand skill depended
upon the degree of the left-hand skill in right-handers, indicating that the relative
degree of the right-hand skill is determined by the right brain in right-handers. This
supports the above mentioned view that testosterone may force the subjects toward
right-handedness in utero.
Tan (in press) has also studied the correlations between the grasp-reflex strengths
and serum free-testosterone levels in neonates. He has reported that there were direct
correlations between grasp-reflex strengths and serum free-testosterone levels in right-
dominant male neonates, whereas the grasp-reflex strength decreased as serum free-
testosterone level increased in right-dominant female neonates. In right- and left-
dominant male and female neonates, the grasp-reflex strength linearly decreased and
increased linearly with testosterone, respectively. These results suggest that testos-
terone cannot be the main factor creating handedness in humans. By contrast, the
present work showed that testosterone was always detrimental for the grasp reflex
from both hands in neonates with right-ear-out, and for the grasp reflex only from
the left hand in neonates with left-ear-out in utero positions. Thus, testosterone is a
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male hormone influencing the cerebral lateralization secondarily on the ground of

genetically and even environmentally determined cerebral organization.

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