Intern. .INeuroscience, . 1992, Vol. 66, pp. 163-175 Reprints available directly from the publisher Photocopying permitted by license only
0 1992 Gordon and Breach Science Publishers S.A. Printed in the United States of America
SIMILARITIES BETWEEN SYLVIAN FISSURE ASYMMETRIES IN CAT BRAIN AND PLANUM TEMPORALE ASYMMETRIES IN HUMAN BRAIN UNER TAN Ataturk University, Medical Faculty, Department of Physiology, Erzurum, Turkey Int J Neurosci Downloaded from informahealthcare.com by Nyu Medical Center on 11/04/14 For personal use only.
(Received December 28, 1991)
Galaburda et al. (1987) have suggested that asymmetry of planum temporale in men would result from an asymmetrical neuronal loss; symmetry would implicate a failure of asymmetrical cell loss. There are several reports indicating a similarity between men and animal in cerebral lateralization. In the present worg, a morphological analysis was performed in sylvian fissure (SF) of cats. Asymmetry coefficients (AC) were distributed symmetrically and normally with a mean of zero. However, female cats exhibited a relatively stronger leftward asymmetry (left SF > right SF), and male cats a relatively stronger rightward asymmetry in SF. The results generally supported those of Galaburda and his coworkers. Deviations from their results depended mainly on paw preference. The similarity between human brain and animal brain was accentuated once more concerning cerebral lateralization. The results were not appropriate to conclude about the mechanisms of cerebral lateralization. Testosterone in males and estrogen in females were suggested to be the main hormones contributing to the emergence of cerebral lateralization. Keywords: Cerebral lateralization, asymmetry. sylvian fissure, cat.
Galaburda et al. (1987) have restudied the asymmetrical organization of 100 human brains examined previously by Geschwind and Levitsky (1968). They found that there are graded asymmetries of the planum temporale in the population, averaging on the side of leftward asymmetry (L > R). These authors have also shown that there is a positive linear correlation between the combined (R L) planum area and asymmetry coefficient, i.e., the brains with leftward asymmetry have a lesser total amount of language substrate than the more symmetrical brains. Moreover, there was a significant positive correlation between combined planum area and decreasing leftward asymmetry, and a negative correlation between combined planum area and increasing rightward asymmetry. The size of the right planum increased with decreasing leftward asymmetry; there was a negative correlation between the area of the left planum and increasing rightward asymmetry. Accordingly, Galaburda et al. have suggested that asymmetry of the planum results from the greater pruning down of one of the sides during fetal life and infancy as a result of developmental neuronal loss. Symmetry, on the other hand, would show a failure of asymmetrical cell loss to occur. These authors have posited that testosterone appears to have a direct effect on the right side in leftward asymmetrical brains and on the left side in rightward asymmetrical brains, probably through interference with the process of neuronal loss. A similar approach to cerebral lateralization was made in the present work, using measurements of the right and left sylvian fissures in male and female, right- and left-pawed (RH and LH) cats. Habib (1989) has reported that the shape of sylvian fissures, which are asymmetrical in roughly the same proportion of brains with asymmetrical planum temporale, affect the appearance of the whole posterior region of the hemispheres. Therefore, the length of SF was taken as an index for planum
+
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164
temporale. Since testosterone would be effective also in cats, it would be justifiable to study the relation of sylvian fissures to cerebral lateralization in cats. Asymmetries in sylvian fissures similar to men were indeed reported to occur in nonhuman primates (see MacNeilage et al., 1987; Bradshaw, 1991). There were also asymmetric distributions in length and height of the sylvian fissures in dogs (Tan & Caliskan, 1987).
METHOD Experiments were performed in adult mongrel cats. Paw preference was assessed by Int J Neurosci Downloaded from informahealthcare.com by Nyu Medical Center on 11/04/14 For personal use only.
a food-reaching test performed for 10 days. According to the significance of the mean difference between right and left paw reaches, the cats were referred to as right-pawed (RH), left-pawed (LH), or ambidextrous. After assessment of paw preference, these animals were sacrificed by a high dosage of pentobarbital. The brain was then removed and fixed in formaline for three days. The length of the right and left sylvian fissures was measured by calipers under a magnifier. An asymmetry coefficient (AC) for the length of the right and left sylvian fissure (SF) was computed for each brain using the formula, AC =
(right SF
-
.5 x (right SF
left SF)
+ left SF)
A positive value indicated a larger right sylvian fissure; a negative value indicated a larger left sylvian fissure (see Galaburda et al., 1987).
RESULTS Distribution Of SF Asymmetries In Cats
Figure 1 shows the distributions of ACs in total sample male, and female cats. The distribution of ACs was found to be normal in the total sample (Figure 1A; N = 60; chi square = 3.35, df = 4, p = .50). There were 30 AC+ values above hypothetized zero median and 25 AC- values below hypothetized zero median. The difference was not significant ( z = .54, p = .59). The sample median was .012 with a sample mean of -.004 (SD = .19). Thus, ACs were distributed normally with a mean of about zero. That is, there was no side difference; ACs did not exhibit a significant asymmetry. The distribution of ACs in the right- and left-pawed male cats (N = 23) was not normal (Figure 1B: chi square = 5.45, df = 1, p = .02). The ACs were found to be normally distributed in the right- and left-pawed female cats (Figure 1C: N = 34; chi square = 1.66, df = 2, p = .44). The mean AC in male cats (-.001) was not significantly different from zero in male cats ( t = .03, df = 22, p = .97). The mean AC in female cats (-0.005) was also not significantly different from zero (t = .15, df = 33, p = .OM). Numbers of ACs above and below hypothetized zero median in RH male cats were found to be 5 and 6, respectively. The difference was not significant ( z = 0; p = 1.O). There were more cats above zero median (9) than below zero median (3) in LH male cats, but the difference was not significant (z = 1.44, p = .15). There was no significant difference between the numbers of AC values
165
SYLVIAN FISSURE IN CATS
A . TOTAL SAMPLE
................. ...............,
-1 -0.6 -0.2 0.2 0.6 Int J Neurosci Downloaded from informahealthcare.com by Nyu Medical Center on 11/04/14 For personal use only.
asymmetry coef f icient
1
B. MALE CATS
L
-
-1 -0.6-0.2 0 . 2 0.6
asymmetry coefficient
1
C . FEMALE CATS
2 2 g
18 ................................................ 15 12 9 k 6 * 3 8 0 -1 -0.6 -0.2 0.2 0 . 6 1 :
asymmetry coefficient
FIGURE 1 Distribution of ACs in the total sample of cats Abscissa: AC Ordinate: number of brains. Negative AC values indicate leftward asymmetry, and positive AC values indicate rightward asymmetry.
above and below zero median in RH female cats (9 vs 7) and in LH female cats (7 vs 9). Thus, FS-ACs did not show an asymmetrical distribution in cats. There were sex-related differences in the distribution of ACs. A close inspection of the histograms from the male and female cats suggests that the histogram for the male cats skewed to the right and that for the female cats skewed to the left. The proportions for the rightward (AC > 0 ) AC values were found to be .61 and .43 for the male and female cats, respectively. The difference between these proportions were found to be marginally significant ( z = 1.404, p = .OSO). The proportions for the leftward (AC < 0) AC values were found to be .39 and .58 for the male and female cats. The difference between these proportions were marginally significant
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( z = 1.404, p = .080). The difference between males and females were found to be more pronounced for smaller AC values (from zero to -0.2 and +0.2). In rightward animals, 52.1% of males and 32.5% of females had ACs ranging from zero to .2. This difference was found to be significant (z = 1.537, p = .062). The difference was more pronounced for the AC- values. Of leftward animals (ACs from zero to --.2), 17.4% of males and 42.5% of females had these leftward ACs. The difference between these proportions was found to be significant ( z = 2.035, p = .021).
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R
+ L SF vs ACs
The combined length of SFs was not standardized, since there was no significant correlation between SF length and brain weight. In RH AC- (leftward asymmetry) cats, there was a significant positive linear correlation between R L SF length and ACs (Figure 2A; r = .52, t = 2.36, df = 16, p = .032). There was a significant negative linear correlation between the total SF length and AC in LH cats (Figure 2B: r = -.67, t = 2.69, df = 10, p = .025). Thus, the leftward asymmetry decreased as the total length of SFs (R + L) increased in RH cats. In other words, symmetrical brains have larger SFs than asymmetrical brains in RH cats. However, the opposite was true in LH cats. The leftward asymmetry in LH cats decreased, as the total SF length decreased. In other words, the symmetrical brains have shorter SFs than asymmetrical brains in LH cats in contrast to RH cats. In rightward asymmetrical brains (AC+) of RH cats, there was a significant negative linear correlation between R + L SF and ACs (Figure 3A: r = - .60, t = 2.38, df = 1 1 , p = .039). That is, R + L SF decreased, as the rightward asymmetry increased. The same trend was also seen in LH cats (AC+), but the correlation was not significant (Figure 3B: r = -.34, t = 1.20, df = 12, p = .26).
+
Right And Left SF vs AC Total sample In RH cats (total sample), the length of the left SF was found to be significantly and negatively linearly correlated with ACs (Figure 4A: r = - . 5 0 , t = 2.78, df = 24, p = .011). The leftward asymmetry decreased toward zero and then rightward asymmetry increased, as the length of the left SF decreased. That is, the left SF was longer in leftward asymmetrical brains than in rightward asymmetrical brains. An opposite relationship was found for the right SF in RH cats (Figure 4B: r = .66, t = 4.47, df = 27, p = .OOO). In these cats, leftward asymmetry decreased and then turned to rightward asymmetry, as the length of the right SF increased. That is, rightward asymmetry in SF was associated with a longer right SF, and a leftward asymmetry was associated with a shorter right SF in RH cats. A similar relationship was found to occur in LH cats as in RH cats (total samples). In LH cats, the left SF length was found to be significantly and negatively linearly correlated with AC (Figure 5A: r = -.56, t = 3.43, df = 26, p = .002). There was a significant positive linear correlation between the right SF length and AC in LH cats (Figure 5B: r = .71, t = 5.20, df = 28, p = .OOO). Leftward asymmetrical brains In RH cats with leftward asymmetry in SF length, there was no significant correlation between the left SF length and AC (Figure 6A: r = .06, t = .20, df = 12, p = .84). On the contrary, the right SF length increased, as AC decreased from leftward asymmetry toward symmetry (Figure 6B: r = .74, t = 4.29, df = 16, p = .OOl).
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SYLVIAN FISSURE IN CATS
A . RH CATS (R+L SYLUIA) a
20 .................................
18 v
16
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14 12 10 8 -0.6
-0.4 -0.2 ASYM. COEFF.
0
B . LH CATS (R+L SYLVIA) a
20
E E
18
v
16
14 12 :
\
:
10 .............................................. -0.3 -0.2 -0.1 0 ASYM. COEFF. Correlation between the length of the R + L SFs and ACs in RH I
I
FIGURE 2 with leftward asymmetry Abscissa: AC Ordinate: R 13.2 - 15.5 X .
+
(A) and LH (B) cats L SF (mm). In A , y = 16.4 + 8.9 x; In B , y =
An opposite relationship was observed in LH cats with leftward asymmetry. There was a significant negative linear relationship between the length of the left SF and AC in these cats (Figure 7A: r = -.78, t = 3.80, df = 10, p = .004). There was, however, no significant correlation between the length of the right S F and AC (Figure 7B: r = -.41, t = 1.36, d f = 10, p = .207). Rightward asymmetrical brains The relationship between S F length and AC in RH cats with rightward asymmetrical brains resembled that in LH cats with leftward asymmetrical brain. Figure 8A illustrates the relationship between left S F length and AC in RH cats with rightward asymmetrical brains. Figure 8B illustrates the relationship between right SF length and AC in RH cats with rightward asymmetrical
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A.
A
RH CATS (R+L S Y L V I A )
20 18
U
U
16
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14
? cr;
12 10
0
0.04 0.08 0.12 0.16 0 . 2 ASYM. COEFF. (rnrn)
B. LH CATS (R+L S Y L V I A ) n
v
s3
$
18 ................................................ 17 16 15 14
0
0 . 1 0.2 0.3 ASYM. COEFF.
0.4
FIGURE 3 Relationship between R + L SF and AC in RH (A) and LH (B) cats with rightward asymmetry Abscissa: AC Ordinate: R + L SF (mm). In A , y = 16.6 - 18.1 x).
brains. There was a significant negative linear correlation between the left SF length and AC in RH AC+ cats (Figure 8A: r = -.73, t = 3.36, df = 11, p = .007). There was, however, no significant correlation between the right SF length and AC in these cats (Figure 8B: r = -.20, t = .69, df = 12, p = .502). In LH cats with rightward SF asymmetry, the left SF length was found to be significantly and negatively linearly correlated with AC (Figure 9A: r = -.62, t = 2.63, df = 12, p = .024). As seen in this Figure, the length of the left SF increased as SF asymmetry decreased. There was a significant, positive linear correlation between the right SF length and AC in LH cats with rightward asymmetry (Figure 9B: r = .73, t = 3.85, df = 14, p = .002). That is, the length of the right SF decreased as interhemispheric asymmetry decreased.
SYLVIAN FISSURE IN CATS
169
A . RH CATS (LEFT SYLUIA) .A.
E E
c
12 . . .............................................. . .'. .\ : .: 1 : \ : : 10 -'1
--.
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Y
w A
4
\
.......< ............... ,....... ..... . A , ,...,i I .
-0.6-0.4-0.2 0 0.2 0.4 0.6 ASYM. COEFF.
B. RH CATS [RIGHT SYLVIA) A
Y
12 ................................................ 10
8
6 4 -0.6-0.4-0.2 0 0.2 0 . 4 0 . 6 ASYM. COEFF. FIGURE 4 Relationships between SF length and AC in RH cats Abscissa: AC Ordinate: length of the left (A) and right (B) SF. In A , y = 7.7 - 3.3 x ; in B , y = 7.8 + 4.8 x .
DISCUSSION Normal Distribution Of The SF-ACs In Cats
The ACs were found to be distributed normally with a mean of zero in the total sample of cats. On the contrary, Galaburda et al. (1987) have found that 63% of the human brains had a larger left planum (leftward asymmetry), and 21% a larger right planum temporale (rightward asymmetry). This can be accounted for by a language substrate in human left brain, which could not emerge in cats. There was, however, an interesting difference between SF-AC distributions of the male and female cats. Statistical analysis indicated that males tended to have a relatively more rightward
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A . LH CATS [LEFT SYLVIA)
10 8
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6 4 -0.6-0.4-0.2 0 0 . 2 0.4 0.6 ASYM. COEFF.
B. LH CATS (RIGHT SYLVIA) n
E E
Y
a m
12
10 8
6 4 -0.6-0.44.2 0 0.2 0.4 0.6 ASYM. COEFF. FIGURE 5 Relationship between SF length and AC in LH cats Abscissa: AC Ordinate: the length of the left (A) and right (B) SF (mm). In A, y = 7 . 3 - 4.1 x; In B , y = 7 . 4 + 5.4 x.
asymmetry and females tended to have a relatively more leftward asymmetry. This means that males tended to have longer right SFs as compared to females, which tended to have longer left SFs as compared to males. It can then be concluded that left parietotemporal cortex in females tended to be larger in females than males. It is generally accepted that language capacities are better developed in women than men, and the left hemisphere is mainly involved in language. Accordingly, the lefthemisphere specialization for language may have evolutionary precursors, and sex hormones may be involved in the development of verbal expression of emotions, which would, in turn, be associated with hand preference. We have indeed found that female cats are more right-pawed than male cats (Tan et al., 1990; Tan & Kutlu, 1991).
SYLVIAN FISSURE IN CATS
171
A . RH C A T S (LEFT S Y L U I A ) 10
A
..:.. :. .........:. ..........:.. : . . :. . :.. :. . :.
.::
'€ E
. .; ..:
:I
m
.......... . . . . . . . . . . . . . . ....*KT . .......
v
mmm
--.&--,?
a
,
/
.w
3 r(
Int J Neurosci Downloaded from informahealthcare.com by Nyu Medical Center on 11/04/14 For personal use only.
n #
-
- -. 6 ...............:._ .- ......................... ; -0.3 -0.2 -0.1 0 c
asymmetry coefficient B . RH CATS (RIGHT S Y L V I A ) 10 :..:....:..: .........' . . . :........ :...:...:...:...:
A
'
B
/
'
v
a
.d
3 d
#
c,
c
b,
.w
k
-0.6
-0.4 -0.2 0 asymmetry coef f icient
FIGURE 6 Relationship between FS length and AC in RH cats with leftward asymmetry Abscissa: AC Ordinate: the length of the left (A) and right (B) SFs (mrn). In A , y = 8 . 4 + 0.6 x; In B , y = 8 . 1 + 7.5 x.
ACs To R
+ L SFs
There was a significant positive linear correlation between R + L SFs and ACs in the RH cats with leftward SF asymmetries. There was a significant negative linear correlation between R L SFs and ACs in LH cats with leftward asymmetries. Similarly, Galaburda et al. (1987) have found a significant positive linear correlation between combined (R + L) area of planum temporale and ACs for planum areas. These authors probably could not determine the handedness of their subjects. Nevertheless, their subjects most probably included those with right-hand preference. In RH cats with rightward SF asymmetries, there was a significant negative linear correlation between R + L SF and AC. The LH cats with rightward asymmetry did not
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f3.
LH CATS [LEFT SYLUIAI
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..................
-0.25 -0.2-0.15-0, 1-0.05 0 ASYM. COEFF.
B. LH CATS [RIGHT SYLUIANI A
I
Y
L U
1; i
'3
10 :.........:. ..................:. ...................
........;. ........;. .......;........ .:.........;
-0.25-0.2 -0.15-0.1-0.05 ASYM. COEFF.
0
FIGURE 7 Relationship between SF length and AC in LH cats with leftward asymmetry Abscissa: AC Ordinate: length of the left (A) and right (B) SF. In A , y = 6.5 - 11.9 X; In B , y = 6 . 6 - 3.6 X.
show a significant correlation between R + L SF and ACs. Galaburda et al. obtained a nearly similar tendency in their work, but the correlation was not significant. The results of the present work now show that these relationships may depend upon hand preference. The conclusion of Galaburda et al. that the brains with leftward asymmetry have a lesser total amount of language substrate than the more symmetrical brains, was thus not supported by the above mentioned results of the present work. These authors could interpret their results in another way, if they had also analyzed the brains of left-handers. This study now suggests that the brains with leftward SF asymmetry may have a lesser total parietotemporal cortex than the more symmetrical brains, but only in R H cats with leftward SF asymmetries. In LH cats with leftward asymmetry and in R H cats with rightward asymmetry, the opposite could be true.
SYLVIAN FISSURE IN CATS
173
A . RH CATS (AC+) 10
::...w'..:.
-.'
;.:. .:.:..: .:.:. .............. .. ... .:.:. . : _
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,
4
\,
;........ ;.........;. . . . . . . .; .........:.>. . . . . ;
0.04 0.08 0.12 0.16 0 . 2 ASY. COEFF.
0
B. RH CATS 1Z
10 .................................................
8
:m
*: #
6 A
1-. - -:--
-
-
:
_
,
............................
0
-. 3,;: -................ -. :
- ; . . . . . . . . < . . . . . . . . . ; . . . I . . . .
:..
-&:
c_
L
0.04 0.08 0.12 0.16 0.2 ASYM. COEFF.
FIGURE 8 Relationship between SF length and AC in RH cats with rightward asymmetry Abscissa: AC Ordinate: length of the left (A) and right (B) SF (mm). In A, y = 8 . 3 12.3 x; In B , y = 8.4 3 . 9 x. ~
Asymmetry And Variability In The Left And Right SFs
The results concerning the correlation between right or left SF lengths and ACs were in accord with Galaburda et al. Namely, the left SF length decreased significantly with decreasing leftward asymmetry; the right SF increased linearly with decreasing leftward asymmetry in RH and LH cats. Hand preference did not change this relationship. Concerning the relationship between SF and AC in cats with leftward asymmetry, Galaburda and his colleagues were confirmed only for the RH cats (no significant correlation for the left SF vs AC and a positive linear correlation for the right SF vs AC). This can be also accounted for in their probably RH subjects. In LH cats
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A. n
E E
w
LH CATS [AC+l
_
10 ................................................. . c .. ._. L
8
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6
',
x
4 :...........:. ..........+. ......* ..;...>.....; 0 0 . 1 0.2 0.3 0.4 ASYHHETRY COEFFICIENT
B. LH CATS (AC+l n
E E w
14 12
10
0
6 U
p:
4 ................................................ 0 0.2 0.4 0.6 I
ASYNMETRY COEFFICIENT FIGURE 9 Relationship between SF length and AC in LH cats with rightward asymmetry Abscissa: AC Ordinate: length of the left (A) and right (B) SF (mm). In A , y = 7.6 - 6.3 x; In B , y = 7.1 + 7 . 6 x.
with leftward asymmetry, these relationships were quite opposite to those from RH cats: a significant negative linear correlation between left SF and AC, and no correlation between right SF and AC. In accordance with Galaburda et al., there was a negative linear correlation between left SF and AC in RH and LH cats with rightward asymmetry, and no significant correlation between right SF and AC in RH cats with rightward asymmetry. However, there was a significant positive linear correlation between right SF and AC in LH cats.
SYLVIAN FISSURE IN CATS
17.5
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CONCLUSIONS The present work showed many similarities of cat SF asymmetries with human planum temporale asymmetries. Sex and paw preference were found to be important factors contributing to some differences between SF (and planum temporale) asymmetries in cat and human. Galaburda et al. could apparently not determine these factors in their human brains. The slight bias to the leftward asymmetry in female cats and a slight bias to the rightward asymmetry in male cats may be related to the testosterone effect on the left brain as suggested by Geschwind and his coworkers (Geschwind & Behan, 1982; Geschwind & Galaburda, 1985a, b). The leftward asymmetry in SFs in females may also be shaped by the female sex hormones (see Tan & Kutlu, 1991), which can increase the chance of being right-pawed in female cats. The results of this work were not appropriate to analyze the effect of testosterone on neuronal cell loss proposed by Galaburda and his coworkers in emergence of cerebral lateralization (Galaburda et al., 1987).
REFERENCES Bradshaw, J . L. (1991). Animal asymmetry and human heredity: Dextrality, tool use and language in evolution-10 years after Walker (1980). British Journal of Psychology, 82, 39-59. Galaburda, A. M., Corsiglia, J . , Rosen, G., & Sherman, G . F. (1987). Planum temporale asymmetry, reappraisal since Geschwind and Levitsky. Neuropsychologia, 25, 853-868. Geschwind, N . , & Behan, P. 0. (1982). Left-handedness: association with immune disease, migraine, and developmental learning disorder. Proceedings of the National Academy of Sciences USA, 7 9 , 5097-5 100. Geschwind, N., & Galaburda, A. M. (1985 a). Cerebral lateralization: biological mechanisms, associations, and pathology, Part I . Archives of Neurology, 42, 428-459. Geschwind, N . , & Galaburda, A. M. (1985 b). Cerebral lateralization: biological mechanisms, associations, and pathology, Part 11. Archives ofNeurology, 42, 521-552. Geschwind, N., & Levitsky, W. (1968). Human brain: left-right asymmetries in temporal speech region. Science, 161, 186-187. Habib, M . (1989). Anatomical asymmetries of the human cerebral cortex. International Journal o f N e u roscience. 47, 67-79. MacNeilage, P . F . , Studdert-Kennedy, M. G . , & Lindblom, B. (1987). Primate handedness reconsidered. Behavioral and Brain Sciences, 10. 247-303. Tan, U . , & Caliskan, S . (1987). Asymmetries in the cerebral dimensions and fissures of the dog. International Journal of Neuroscience, 32, 943-952. Tan, U . , Yaprak, M., & Kutlu, N . (1990). Paw preference in cats: distribution and sex differences. Inrernational Journal of Neuroscience, 50, 195-208. Tan, U. & Kutlu, N. (1991). 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.
0 1992 Gordon and Breach Science Publishers S.A. Printed in the United States of America
SIMILARITIES BETWEEN SYLVIAN FISSURE ASYMMETRIES IN CAT BRAIN AND PLANUM TEMPORALE ASYMMETRIES IN HUMAN BRAIN UNER TAN Ataturk University, Medical Faculty, Department of Physiology, Erzurum, Turkey Int J Neurosci Downloaded from informahealthcare.com by Nyu Medical Center on 11/04/14 For personal use only.
(Received December 28, 1991)
Galaburda et al. (1987) have suggested that asymmetry of planum temporale in men would result from an asymmetrical neuronal loss; symmetry would implicate a failure of asymmetrical cell loss. There are several reports indicating a similarity between men and animal in cerebral lateralization. In the present worg, a morphological analysis was performed in sylvian fissure (SF) of cats. Asymmetry coefficients (AC) were distributed symmetrically and normally with a mean of zero. However, female cats exhibited a relatively stronger leftward asymmetry (left SF > right SF), and male cats a relatively stronger rightward asymmetry in SF. The results generally supported those of Galaburda and his coworkers. Deviations from their results depended mainly on paw preference. The similarity between human brain and animal brain was accentuated once more concerning cerebral lateralization. The results were not appropriate to conclude about the mechanisms of cerebral lateralization. Testosterone in males and estrogen in females were suggested to be the main hormones contributing to the emergence of cerebral lateralization. Keywords: Cerebral lateralization, asymmetry. sylvian fissure, cat.
Galaburda et al. (1987) have restudied the asymmetrical organization of 100 human brains examined previously by Geschwind and Levitsky (1968). They found that there are graded asymmetries of the planum temporale in the population, averaging on the side of leftward asymmetry (L > R). These authors have also shown that there is a positive linear correlation between the combined (R L) planum area and asymmetry coefficient, i.e., the brains with leftward asymmetry have a lesser total amount of language substrate than the more symmetrical brains. Moreover, there was a significant positive correlation between combined planum area and decreasing leftward asymmetry, and a negative correlation between combined planum area and increasing rightward asymmetry. The size of the right planum increased with decreasing leftward asymmetry; there was a negative correlation between the area of the left planum and increasing rightward asymmetry. Accordingly, Galaburda et al. have suggested that asymmetry of the planum results from the greater pruning down of one of the sides during fetal life and infancy as a result of developmental neuronal loss. Symmetry, on the other hand, would show a failure of asymmetrical cell loss to occur. These authors have posited that testosterone appears to have a direct effect on the right side in leftward asymmetrical brains and on the left side in rightward asymmetrical brains, probably through interference with the process of neuronal loss. A similar approach to cerebral lateralization was made in the present work, using measurements of the right and left sylvian fissures in male and female, right- and left-pawed (RH and LH) cats. Habib (1989) has reported that the shape of sylvian fissures, which are asymmetrical in roughly the same proportion of brains with asymmetrical planum temporale, affect the appearance of the whole posterior region of the hemispheres. Therefore, the length of SF was taken as an index for planum
+
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164
temporale. Since testosterone would be effective also in cats, it would be justifiable to study the relation of sylvian fissures to cerebral lateralization in cats. Asymmetries in sylvian fissures similar to men were indeed reported to occur in nonhuman primates (see MacNeilage et al., 1987; Bradshaw, 1991). There were also asymmetric distributions in length and height of the sylvian fissures in dogs (Tan & Caliskan, 1987).
METHOD Experiments were performed in adult mongrel cats. Paw preference was assessed by Int J Neurosci Downloaded from informahealthcare.com by Nyu Medical Center on 11/04/14 For personal use only.
a food-reaching test performed for 10 days. According to the significance of the mean difference between right and left paw reaches, the cats were referred to as right-pawed (RH), left-pawed (LH), or ambidextrous. After assessment of paw preference, these animals were sacrificed by a high dosage of pentobarbital. The brain was then removed and fixed in formaline for three days. The length of the right and left sylvian fissures was measured by calipers under a magnifier. An asymmetry coefficient (AC) for the length of the right and left sylvian fissure (SF) was computed for each brain using the formula, AC =
(right SF
-
.5 x (right SF
left SF)
+ left SF)
A positive value indicated a larger right sylvian fissure; a negative value indicated a larger left sylvian fissure (see Galaburda et al., 1987).
RESULTS Distribution Of SF Asymmetries In Cats
Figure 1 shows the distributions of ACs in total sample male, and female cats. The distribution of ACs was found to be normal in the total sample (Figure 1A; N = 60; chi square = 3.35, df = 4, p = .50). There were 30 AC+ values above hypothetized zero median and 25 AC- values below hypothetized zero median. The difference was not significant ( z = .54, p = .59). The sample median was .012 with a sample mean of -.004 (SD = .19). Thus, ACs were distributed normally with a mean of about zero. That is, there was no side difference; ACs did not exhibit a significant asymmetry. The distribution of ACs in the right- and left-pawed male cats (N = 23) was not normal (Figure 1B: chi square = 5.45, df = 1, p = .02). The ACs were found to be normally distributed in the right- and left-pawed female cats (Figure 1C: N = 34; chi square = 1.66, df = 2, p = .44). The mean AC in male cats (-.001) was not significantly different from zero in male cats ( t = .03, df = 22, p = .97). The mean AC in female cats (-0.005) was also not significantly different from zero (t = .15, df = 33, p = .OM). Numbers of ACs above and below hypothetized zero median in RH male cats were found to be 5 and 6, respectively. The difference was not significant ( z = 0; p = 1.O). There were more cats above zero median (9) than below zero median (3) in LH male cats, but the difference was not significant (z = 1.44, p = .15). There was no significant difference between the numbers of AC values
165
SYLVIAN FISSURE IN CATS
A . TOTAL SAMPLE
................. ...............,
-1 -0.6 -0.2 0.2 0.6 Int J Neurosci Downloaded from informahealthcare.com by Nyu Medical Center on 11/04/14 For personal use only.
asymmetry coef f icient
1
B. MALE CATS
L
-
-1 -0.6-0.2 0 . 2 0.6
asymmetry coefficient
1
C . FEMALE CATS
2 2 g
18 ................................................ 15 12 9 k 6 * 3 8 0 -1 -0.6 -0.2 0.2 0 . 6 1 :
asymmetry coefficient
FIGURE 1 Distribution of ACs in the total sample of cats Abscissa: AC Ordinate: number of brains. Negative AC values indicate leftward asymmetry, and positive AC values indicate rightward asymmetry.
above and below zero median in RH female cats (9 vs 7) and in LH female cats (7 vs 9). Thus, FS-ACs did not show an asymmetrical distribution in cats. There were sex-related differences in the distribution of ACs. A close inspection of the histograms from the male and female cats suggests that the histogram for the male cats skewed to the right and that for the female cats skewed to the left. The proportions for the rightward (AC > 0 ) AC values were found to be .61 and .43 for the male and female cats, respectively. The difference between these proportions were found to be marginally significant ( z = 1.404, p = .OSO). The proportions for the leftward (AC < 0) AC values were found to be .39 and .58 for the male and female cats. The difference between these proportions were marginally significant
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( z = 1.404, p = .080). The difference between males and females were found to be more pronounced for smaller AC values (from zero to -0.2 and +0.2). In rightward animals, 52.1% of males and 32.5% of females had ACs ranging from zero to .2. This difference was found to be significant (z = 1.537, p = .062). The difference was more pronounced for the AC- values. Of leftward animals (ACs from zero to --.2), 17.4% of males and 42.5% of females had these leftward ACs. The difference between these proportions was found to be significant ( z = 2.035, p = .021).
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R
+ L SF vs ACs
The combined length of SFs was not standardized, since there was no significant correlation between SF length and brain weight. In RH AC- (leftward asymmetry) cats, there was a significant positive linear correlation between R L SF length and ACs (Figure 2A; r = .52, t = 2.36, df = 16, p = .032). There was a significant negative linear correlation between the total SF length and AC in LH cats (Figure 2B: r = -.67, t = 2.69, df = 10, p = .025). Thus, the leftward asymmetry decreased as the total length of SFs (R + L) increased in RH cats. In other words, symmetrical brains have larger SFs than asymmetrical brains in RH cats. However, the opposite was true in LH cats. The leftward asymmetry in LH cats decreased, as the total SF length decreased. In other words, the symmetrical brains have shorter SFs than asymmetrical brains in LH cats in contrast to RH cats. In rightward asymmetrical brains (AC+) of RH cats, there was a significant negative linear correlation between R + L SF and ACs (Figure 3A: r = - .60, t = 2.38, df = 1 1 , p = .039). That is, R + L SF decreased, as the rightward asymmetry increased. The same trend was also seen in LH cats (AC+), but the correlation was not significant (Figure 3B: r = -.34, t = 1.20, df = 12, p = .26).
+
Right And Left SF vs AC Total sample In RH cats (total sample), the length of the left SF was found to be significantly and negatively linearly correlated with ACs (Figure 4A: r = - . 5 0 , t = 2.78, df = 24, p = .011). The leftward asymmetry decreased toward zero and then rightward asymmetry increased, as the length of the left SF decreased. That is, the left SF was longer in leftward asymmetrical brains than in rightward asymmetrical brains. An opposite relationship was found for the right SF in RH cats (Figure 4B: r = .66, t = 4.47, df = 27, p = .OOO). In these cats, leftward asymmetry decreased and then turned to rightward asymmetry, as the length of the right SF increased. That is, rightward asymmetry in SF was associated with a longer right SF, and a leftward asymmetry was associated with a shorter right SF in RH cats. A similar relationship was found to occur in LH cats as in RH cats (total samples). In LH cats, the left SF length was found to be significantly and negatively linearly correlated with AC (Figure 5A: r = -.56, t = 3.43, df = 26, p = .002). There was a significant positive linear correlation between the right SF length and AC in LH cats (Figure 5B: r = .71, t = 5.20, df = 28, p = .OOO). Leftward asymmetrical brains In RH cats with leftward asymmetry in SF length, there was no significant correlation between the left SF length and AC (Figure 6A: r = .06, t = .20, df = 12, p = .84). On the contrary, the right SF length increased, as AC decreased from leftward asymmetry toward symmetry (Figure 6B: r = .74, t = 4.29, df = 16, p = .OOl).
167
SYLVIAN FISSURE IN CATS
A . RH CATS (R+L SYLUIA) a
20 .................................
18 v
16
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14 12 10 8 -0.6
-0.4 -0.2 ASYM. COEFF.
0
B . LH CATS (R+L SYLVIA) a
20
E E
18
v
16
14 12 :
\
:
10 .............................................. -0.3 -0.2 -0.1 0 ASYM. COEFF. Correlation between the length of the R + L SFs and ACs in RH I
I
FIGURE 2 with leftward asymmetry Abscissa: AC Ordinate: R 13.2 - 15.5 X .
+
(A) and LH (B) cats L SF (mm). In A , y = 16.4 + 8.9 x; In B , y =
An opposite relationship was observed in LH cats with leftward asymmetry. There was a significant negative linear relationship between the length of the left SF and AC in these cats (Figure 7A: r = -.78, t = 3.80, df = 10, p = .004). There was, however, no significant correlation between the length of the right S F and AC (Figure 7B: r = -.41, t = 1.36, d f = 10, p = .207). Rightward asymmetrical brains The relationship between S F length and AC in RH cats with rightward asymmetrical brains resembled that in LH cats with leftward asymmetrical brain. Figure 8A illustrates the relationship between left S F length and AC in RH cats with rightward asymmetrical brains. Figure 8B illustrates the relationship between right SF length and AC in RH cats with rightward asymmetrical
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168
A.
A
RH CATS (R+L S Y L V I A )
20 18
U
U
16
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14
? cr;
12 10
0
0.04 0.08 0.12 0.16 0 . 2 ASYM. COEFF. (rnrn)
B. LH CATS (R+L S Y L V I A ) n
v
s3
$
18 ................................................ 17 16 15 14
0
0 . 1 0.2 0.3 ASYM. COEFF.
0.4
FIGURE 3 Relationship between R + L SF and AC in RH (A) and LH (B) cats with rightward asymmetry Abscissa: AC Ordinate: R + L SF (mm). In A , y = 16.6 - 18.1 x).
brains. There was a significant negative linear correlation between the left SF length and AC in RH AC+ cats (Figure 8A: r = -.73, t = 3.36, df = 11, p = .007). There was, however, no significant correlation between the right SF length and AC in these cats (Figure 8B: r = -.20, t = .69, df = 12, p = .502). In LH cats with rightward SF asymmetry, the left SF length was found to be significantly and negatively linearly correlated with AC (Figure 9A: r = -.62, t = 2.63, df = 12, p = .024). As seen in this Figure, the length of the left SF increased as SF asymmetry decreased. There was a significant, positive linear correlation between the right SF length and AC in LH cats with rightward asymmetry (Figure 9B: r = .73, t = 3.85, df = 14, p = .002). That is, the length of the right SF decreased as interhemispheric asymmetry decreased.
SYLVIAN FISSURE IN CATS
169
A . RH CATS (LEFT SYLUIA) .A.
E E
c
12 . . .............................................. . .'. .\ : .: 1 : \ : : 10 -'1
--.
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Y
w A
4
\
.......< ............... ,....... ..... . A , ,...,i I .
-0.6-0.4-0.2 0 0.2 0.4 0.6 ASYM. COEFF.
B. RH CATS [RIGHT SYLVIA) A
Y
12 ................................................ 10
8
6 4 -0.6-0.4-0.2 0 0.2 0 . 4 0 . 6 ASYM. COEFF. FIGURE 4 Relationships between SF length and AC in RH cats Abscissa: AC Ordinate: length of the left (A) and right (B) SF. In A , y = 7.7 - 3.3 x ; in B , y = 7.8 + 4.8 x .
DISCUSSION Normal Distribution Of The SF-ACs In Cats
The ACs were found to be distributed normally with a mean of zero in the total sample of cats. On the contrary, Galaburda et al. (1987) have found that 63% of the human brains had a larger left planum (leftward asymmetry), and 21% a larger right planum temporale (rightward asymmetry). This can be accounted for by a language substrate in human left brain, which could not emerge in cats. There was, however, an interesting difference between SF-AC distributions of the male and female cats. Statistical analysis indicated that males tended to have a relatively more rightward
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170
A . LH CATS [LEFT SYLVIA)
10 8
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6 4 -0.6-0.4-0.2 0 0 . 2 0.4 0.6 ASYM. COEFF.
B. LH CATS (RIGHT SYLVIA) n
E E
Y
a m
12
10 8
6 4 -0.6-0.44.2 0 0.2 0.4 0.6 ASYM. COEFF. FIGURE 5 Relationship between SF length and AC in LH cats Abscissa: AC Ordinate: the length of the left (A) and right (B) SF (mm). In A, y = 7 . 3 - 4.1 x; In B , y = 7 . 4 + 5.4 x.
asymmetry and females tended to have a relatively more leftward asymmetry. This means that males tended to have longer right SFs as compared to females, which tended to have longer left SFs as compared to males. It can then be concluded that left parietotemporal cortex in females tended to be larger in females than males. It is generally accepted that language capacities are better developed in women than men, and the left hemisphere is mainly involved in language. Accordingly, the lefthemisphere specialization for language may have evolutionary precursors, and sex hormones may be involved in the development of verbal expression of emotions, which would, in turn, be associated with hand preference. We have indeed found that female cats are more right-pawed than male cats (Tan et al., 1990; Tan & Kutlu, 1991).
SYLVIAN FISSURE IN CATS
171
A . RH C A T S (LEFT S Y L U I A ) 10
A
..:.. :. .........:. ..........:.. : . . :. . :.. :. . :.
.::
'€ E
. .; ..:
:I
m
.......... . . . . . . . . . . . . . . ....*KT . .......
v
mmm
--.&--,?
a
,
/
.w
3 r(
Int J Neurosci Downloaded from informahealthcare.com by Nyu Medical Center on 11/04/14 For personal use only.
n #
-
- -. 6 ...............:._ .- ......................... ; -0.3 -0.2 -0.1 0 c
asymmetry coefficient B . RH CATS (RIGHT S Y L V I A ) 10 :..:....:..: .........' . . . :........ :...:...:...:...:
A
'
B
/
'
v
a
.d
3 d
#
c,
c
b,
.w
k
-0.6
-0.4 -0.2 0 asymmetry coef f icient
FIGURE 6 Relationship between FS length and AC in RH cats with leftward asymmetry Abscissa: AC Ordinate: the length of the left (A) and right (B) SFs (mrn). In A , y = 8 . 4 + 0.6 x; In B , y = 8 . 1 + 7.5 x.
ACs To R
+ L SFs
There was a significant positive linear correlation between R + L SFs and ACs in the RH cats with leftward SF asymmetries. There was a significant negative linear correlation between R L SFs and ACs in LH cats with leftward asymmetries. Similarly, Galaburda et al. (1987) have found a significant positive linear correlation between combined (R + L) area of planum temporale and ACs for planum areas. These authors probably could not determine the handedness of their subjects. Nevertheless, their subjects most probably included those with right-hand preference. In RH cats with rightward SF asymmetries, there was a significant negative linear correlation between R + L SF and AC. The LH cats with rightward asymmetry did not
+
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172
f3.
LH CATS [LEFT SYLUIAI
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..................
-0.25 -0.2-0.15-0, 1-0.05 0 ASYM. COEFF.
B. LH CATS [RIGHT SYLUIANI A
I
Y
L U
1; i
'3
10 :.........:. ..................:. ...................
........;. ........;. .......;........ .:.........;
-0.25-0.2 -0.15-0.1-0.05 ASYM. COEFF.
0
FIGURE 7 Relationship between SF length and AC in LH cats with leftward asymmetry Abscissa: AC Ordinate: length of the left (A) and right (B) SF. In A , y = 6.5 - 11.9 X; In B , y = 6 . 6 - 3.6 X.
show a significant correlation between R + L SF and ACs. Galaburda et al. obtained a nearly similar tendency in their work, but the correlation was not significant. The results of the present work now show that these relationships may depend upon hand preference. The conclusion of Galaburda et al. that the brains with leftward asymmetry have a lesser total amount of language substrate than the more symmetrical brains, was thus not supported by the above mentioned results of the present work. These authors could interpret their results in another way, if they had also analyzed the brains of left-handers. This study now suggests that the brains with leftward SF asymmetry may have a lesser total parietotemporal cortex than the more symmetrical brains, but only in R H cats with leftward SF asymmetries. In LH cats with leftward asymmetry and in R H cats with rightward asymmetry, the opposite could be true.
SYLVIAN FISSURE IN CATS
173
A . RH CATS (AC+) 10
::...w'..:.
-.'
;.:. .:.:..: .:.:. .............. .. ... .:.:. . : _
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,
4
\,
;........ ;.........;. . . . . . . .; .........:.>. . . . . ;
0.04 0.08 0.12 0.16 0 . 2 ASY. COEFF.
0
B. RH CATS 1Z
10 .................................................
8
:m
*: #
6 A
1-. - -:--
-
-
:
_
,
............................
0
-. 3,;: -................ -. :
- ; . . . . . . . . < . . . . . . . . . ; . . . I . . . .
:..
-&:
c_
L
0.04 0.08 0.12 0.16 0.2 ASYM. COEFF.
FIGURE 8 Relationship between SF length and AC in RH cats with rightward asymmetry Abscissa: AC Ordinate: length of the left (A) and right (B) SF (mm). In A, y = 8 . 3 12.3 x; In B , y = 8.4 3 . 9 x. ~
Asymmetry And Variability In The Left And Right SFs
The results concerning the correlation between right or left SF lengths and ACs were in accord with Galaburda et al. Namely, the left SF length decreased significantly with decreasing leftward asymmetry; the right SF increased linearly with decreasing leftward asymmetry in RH and LH cats. Hand preference did not change this relationship. Concerning the relationship between SF and AC in cats with leftward asymmetry, Galaburda and his colleagues were confirmed only for the RH cats (no significant correlation for the left SF vs AC and a positive linear correlation for the right SF vs AC). This can be also accounted for in their probably RH subjects. In LH cats
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174
A. n
E E
w
LH CATS [AC+l
_
10 ................................................. . c .. ._. L
8
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6
',
x
4 :...........:. ..........+. ......* ..;...>.....; 0 0 . 1 0.2 0.3 0.4 ASYHHETRY COEFFICIENT
B. LH CATS (AC+l n
E E w
14 12
10
0
6 U
p:
4 ................................................ 0 0.2 0.4 0.6 I
ASYNMETRY COEFFICIENT FIGURE 9 Relationship between SF length and AC in LH cats with rightward asymmetry Abscissa: AC Ordinate: length of the left (A) and right (B) SF (mm). In A , y = 7.6 - 6.3 x; In B , y = 7.1 + 7 . 6 x.
with leftward asymmetry, these relationships were quite opposite to those from RH cats: a significant negative linear correlation between left SF and AC, and no correlation between right SF and AC. In accordance with Galaburda et al., there was a negative linear correlation between left SF and AC in RH and LH cats with rightward asymmetry, and no significant correlation between right SF and AC in RH cats with rightward asymmetry. However, there was a significant positive linear correlation between right SF and AC in LH cats.
SYLVIAN FISSURE IN CATS
17.5
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CONCLUSIONS The present work showed many similarities of cat SF asymmetries with human planum temporale asymmetries. Sex and paw preference were found to be important factors contributing to some differences between SF (and planum temporale) asymmetries in cat and human. Galaburda et al. could apparently not determine these factors in their human brains. The slight bias to the leftward asymmetry in female cats and a slight bias to the rightward asymmetry in male cats may be related to the testosterone effect on the left brain as suggested by Geschwind and his coworkers (Geschwind & Behan, 1982; Geschwind & Galaburda, 1985a, b). The leftward asymmetry in SFs in females may also be shaped by the female sex hormones (see Tan & Kutlu, 1991), which can increase the chance of being right-pawed in female cats. The results of this work were not appropriate to analyze the effect of testosterone on neuronal cell loss proposed by Galaburda and his coworkers in emergence of cerebral lateralization (Galaburda et al., 1987).
REFERENCES Bradshaw, J . L. (1991). Animal asymmetry and human heredity: Dextrality, tool use and language in evolution-10 years after Walker (1980). British Journal of Psychology, 82, 39-59. Galaburda, A. M., Corsiglia, J . , Rosen, G., & Sherman, G . F. (1987). Planum temporale asymmetry, reappraisal since Geschwind and Levitsky. Neuropsychologia, 25, 853-868. Geschwind, N . , & Behan, P. 0. (1982). Left-handedness: association with immune disease, migraine, and developmental learning disorder. Proceedings of the National Academy of Sciences USA, 7 9 , 5097-5 100. Geschwind, N., & Galaburda, A. M. (1985 a). Cerebral lateralization: biological mechanisms, associations, and pathology, Part I . Archives of Neurology, 42, 428-459. Geschwind, N . , & Galaburda, A. M. (1985 b). Cerebral lateralization: biological mechanisms, associations, and pathology, Part 11. Archives ofNeurology, 42, 521-552. Geschwind, N., & Levitsky, W. (1968). Human brain: left-right asymmetries in temporal speech region. Science, 161, 186-187. Habib, M . (1989). Anatomical asymmetries of the human cerebral cortex. International Journal o f N e u roscience. 47, 67-79. MacNeilage, P . F . , Studdert-Kennedy, M. G . , & Lindblom, B. (1987). Primate handedness reconsidered. Behavioral and Brain Sciences, 10. 247-303. Tan, U . , & Caliskan, S . (1987). Asymmetries in the cerebral dimensions and fissures of the dog. International Journal of Neuroscience, 32, 943-952. Tan, U . , Yaprak, M., & Kutlu, N . (1990). Paw preference in cats: distribution and sex differences. Inrernational Journal of Neuroscience, 50, 195-208. Tan, U. & Kutlu, N. (1991). 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.
