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Anatomical brain asymmetries in New World and Old World monkeys Stages of temporal lobe development in primate Evolution.

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AMERICAN JOURNAL OF PHYSICAL ANTHROPOLOGY 76:39-48 (1988)
Anatomical Brain Asymmetries in New World and Old World
Monkeys: Stages of Temporal Lobe Development in Primate
Evolution
PETER L. HEILBRONER AND RALPH L. HOLLOWAY
Department ofdnthropology, Columbia Uniuersity New York,
New York 10027
KEY WORDS Brain, Cerebral cortex, Asymmetry, Sylvian fissure,
Sylvian point, Central fissure, Wernicke’s area, Cercopithecoid, New
World monkey, Hominoid, Endocast
ABSTRACT
Relatively large (n = 20-30) samples of formalin-fixed brain
specimens from five Old and New World monkey species were examined in a
study measuring anatomical temporal-lobe asymmetries. Linear measurements of the length of the Sylvian fissure were taken on each cerebral hemisphere to evaluate lateral differences related to development of auditory
association cortex. The results indicate significantly greater Sylvian fissure
length on the left hemisphere than on the right hemisphere in four of these
species. Measurements of a different parameter on Saimiri sciureus brain
specimens (length of anterior portion of the Sylvian fissure) also suggested
temporal-lobe asymmetry favoring the left hemisphere. Other measurements
Oength of the Sylvian fissure lying posterior to the central sulcus, and dorsoventral position of the Sylvian point) in Macaca mulatta and M. fascicularis
did not reveal significant rightAeft-hemisphere differences. Sylvian-fissure
length determined from photographs of M. mulatta hemispheres in contrast to
results of direct measurements did not yield significant right/left-hemisphere
asymmetry. We mention possible reasons why previous anatomical studies of
brains from monkeys did not discern temporal-lobe asymmetry, and we also
discuss whether or not certain of these asymmetries in monkeys foreshadowed
the evolution of language-processing areas of the cerebral cortex in hominids.
“Results of several behavioral studies suggest that in certain macaque species auditory
discrimination abilities often are better developed in the left-hemisphere temporal lobe
of the brain than in the right temporal lobe.
Experimental studies of the Japanese macaque (Macaca fuscatu) (Petersen et al., 1978,
1984;Beecher et al., 1979;Zoloth et al., 1979)
have provided most of the evidence for the
existence of this brain asymmetry. These investigations have evaluated lateralized auditory discrimination function by measuring
macaques’ ability to distinguish between two
semantically distinct fragments from this
species’ vocalizations, presented either to the
right or the left hemisphere via the contralateral ear. Presentation of the vocalization
excerpts to the macaques’ left hemispheres
appears to elicit significantly better discrim-
0 1988 ALAN R.LISS. INC
ination between the two syllables than righthemisphere presentation.
This finding has been corroborated by Heffner and Heffner (1984); these researchers
ablated either right- or left-hemisphere temporal-lobe auditory association cortex from
several M. fuscata prior to conducting the
same test of auditory discrimination function. Only left-hemisphere-ablated monkeys
showed impaired ability to distinguish between the two syllables. This result corroborated the greater importance of left- than
right-hemisphere temporal-lobe cortex for
auditory discrimination functions in macaques. Furthermore, results of an earlier
Received June 18, 1987; revision accepted September 8, 1987.
40
P.L. HEILBRONER AND R.L. HOLLOWAY
study (Dewson, 1977) indicate that in Macaca
rnulatta left-hemisphere temporal-lobecortex
plays a more important role than right-hemisphere cortex in mediating auditory-visual
matching, a related association function.
During much of the ten-year period in
which these behavioral findings were reported, studies of nonhuman primate brain
morphology (LeMay, 1976; Yeni-Komshian
and Benson, 1976; Falk, 1978) failed to identify an anatomical correlate of the lateralized
auditory discrimination abilities reported in
functional studies. These research efforts, in
examining brains or endocranial casts from
macaques or other Old World monkey species, looked for righaeft-hemisphere differences in the anatomy of regions of the
temporal lobe mediating auditory association operations. Only nonsignificant morphological asymmetries were demonstrated.”
Recently, however, Falk et al. (1986) have
presented evidence for anatomical temporallobe asymmetry in the brain of Macaca mulatta. Using a new measurement technique
(image-analysis of composite photographs)
these workers found mean length of the lefthemisphere Sylvian fissure to be significantly greater than mean length of the right
Sylvian fissure, in a sample of cranial endocasts (n = 10)from this species. This finding
is of great interest as the Sylvian fissure
borders cortex subserving auditory association abilities, suggested by behavioral studies to be better developed in the left temporal
lobe than in the right hemisphere in Macaca.
In the present study we investigated a
number of questions to improve our understanding of temporal-lobe asymmetry in nonhuman primates:
1. Why did anatomical studies previous to
Falk et al. (1986) fail to discern temporal-lobe
brain asymmetry in Old World monkeys?
2. Are significant morphological asymmetries between the right- and left-hemisphere
temporal lobe present in monkey taxa other
than Macaca?
3. In what ways does the pattern of temporal-lobe asymmetry in monkeys resemble
the pattern of asymmetry found in Homo
sapiens?
4 . What morphological and functional
changes might have taken place during the
evolution of these brain asymmetries in
primates?
MATERIALS AND METHODS
Linear measurements designed to assess
anatomical development on the temporal lobe
auditorycortex region were taken on the
right and left cerebral hemispheres of formalin-fixed brain specimens from five New
World and Old World monkey species: Macaca fmcicularis, Macaca mulatta, Saguinus
oedipus, Callithrix jacchus, and Saimiri sciureus. Taxonomic diversity and specimen
availability for attaining large sample size
were primary considerations in choosing
these five taxa. Measurements were taken
on the largest possible brain samples obtainable (n = 20-30 brain specimens per species;
see Table 1).
With the exception of S. sciureus, all brain
specimens were from adults or older juvenile
animals, as monkeys from this age range
show fully developed cerebra with respect
both to size and external morphology (Connolly, 1950; Chi et al., 1977). Because of a
scarcity of adult specimens, however, some
brain specimens from infants were by necessity included in the S. sciureus sample.
Separate statistical tests were performed
to distinguish findings €or S. sciureus
TABLE 1. Brain specimens examined in study
Species
M. mulatta
M. fascicularis
S. oedipus
C. jacchus
S. sciureus
S. sciureus (ad.)
Total
N
Males
Females
Source’
30
30
27
26
20
11
14
18
14
14
8
3
16
12
13
12
12
9
WRPC; NE; B G OR
NE; BG; OR
OKRG
OKRG
USAL; BG
USAL; BG
‘Sources of brain tissue are abbreviated as follows: WRPC: Wisconsin Regional Primate Center; NE: New
England Regional Primate Center; BG: Bowman-Gray School of Medicine (N.C.); OR: Oregon Regional
Primate Center; OKRG Oak Ridge Assoc. Univ. (TN); USAL: Univ. of S. Alabama School of Medicine
(Mobile, AL).
41
ANATOMICAL BRAIN ASYMMETRIES
INTERPARIETAL S.
LUNATE S.
CENTRAL
FISSURE
O N S.F.
POSTERIOR P O I N T
O N S.F.
CLOSEST P O I N T O N S.F.
TO CENTRAL FISSURE
Fig. 1. Sylvian fissure landmarks:Macaca.
adults from results for the mixed-age
(adults + infants) S. sciureus sample. All
brain specimens came from monkeys that
had died from a non-neurological cause and
showed no discernable signs of pathology on
the cortex.
In each sample the number of brain specimens representing males and females was as
close to equal as specimen availability permitted. Cerebral asymmetry in several species, including humans, has been shown to
vary as a function of sex (McGlone, 1980;
Diamond, 1984). We therefore attempted to
account for this factor; in addition, a study
by the authors is currently investigating sex
differences in cerebral asymmetry in
monkeys.
Brain specimens were midsagitally sectioned, and slide photographs of the lateral
surfaces were taken for subsequent measurements. Except for two assessments (2 and 5
below) linear measurements of sulcus length
were made by hand directly on the cerebral
cortex of specimens with flexible (plasticcoated fabric) measuring tape. The pia mater
was left on the brain to prevent the measuring tape from falling deeply into the sulcus
being measured. Straight pins were affixed
parallel to each of the first six every centimeter marks on the tape. During each measurement the points became anchored in the
pia mater, preventing slippage of the tape
along the sulcus. The measuring tape was
fitted to the contour of landmarks (portions
of the Sylvian fissure) rostrocaudally between designated endpoints; length was estimated to the nearest 0.5 mm. Each
measurement taken on each brain hemisphere was repeated, and the repeats were
averaged (to ensure accuracy) to provide a
final figure used in statistical operations.
The following estimates were taken on both
the right and left cerebral hemisphere (see
Figs. 1-3):
1. The first estimate was of the length of
the Sylvian fissure. This parameter was defined as the distance along the Sylvian fissure from the most anterior visible point on
the fissure (determined by the investigator
from a vantage point lateral to the temporal
pole) posterior to the caudal endpoint of the
fissure.
2. A second method for measuring length
of the Sylvian fissure was also used. Our
purpose here was to compare the accuracy of
linear measurements taken on photographs
of brain specimens with measurements made
on brain specimens directly by hand. This
comparison was made using Macaca mulatta
specimens;right- and left-hemisphere lateral
cortical surfaces of these specimens were
42
P.L. HEILBRONER AND R.L. HOLLOWAY
CENTRAL SULCUS
ANTERIOR P O I N T
INTERPARIETAL SULCUS
CLOSEST POINT
T O CENTRAL SULCUS
Fig. 2. Sylvian fissure landmarks: Saimiri.
Fig. 3. Position of Sylvian point Macaca.
photographed with slide film, and the course
of the Sylvian fissure and border of the cerebral hemisphere were traced onto paper from
the projected image of each slide (see below
for description of method used for photography and tracing). The length of the sinuous
outline in the tracing representing the Sylvian fissure was then measured by hand with
the flexible measuring tape.
3. The Sylvian fissure in Saimiri sciureus
(and not the other four species) posterior to
the central sulcus comprises the interparietal sulcus. This landmark extends to the longitudinal fissure, bordering for the most part
visual association cortex, mediating functions not relevant to this study. The length
of the part of this fissure complex lying ante
rior to the central sulcus, adjacent mostly to
cortical auditory fields, was therefore measured on brain specimens from S. sciureus.
4. On the 60 Macaca mulatta and Macaca
fmcicularis brain specimens, length of the
part of the Sylvian fissure posterior to the
closest point to the central sulcus (the Sylvian-fissure segment showing the most pronounced rightAeft-hemisphere difference in
length in Homo sapiens: Shellshear, 1937)
was measured. This measurement was not
taken on specimens from the other three species: the central sulcus is not present in C.
jacchus and S. oedipus, and in S. sciureus the
Sylvian fissure posterior to the central sulcus
is referred to as the parieto-occipitalfissure.
5. Dorsoventral position of the posterior
endpoint of the Sylvian fissure (Sylvian point)
was also determined on M. mulatta and M.
fmcicularis specimens. These were the only
brains examined on which the Sylvian fissure terminates before reaching the longitudial fissure and that were also large enough
to allow for an accurate measurement of Sylvian-point height. To measure Sylvian point
position, a slide of the lateral surface of each
Macaca mulatta or Macaca fmcicularis brain
hemisphere was taken. The method used here
was the following: first, the hemisphere was
43
ANATOMICAL BRAIN ASYMMETRIES
TABLE 2. Length of Sylvian fissure (ern)’
Left hemisuhere
Species
Mean
S
si
Mean
Right hemisphere
S
si
t
P<
M.fascicularis
3.218
0.338
0.063
3.093
0.322
0.060
2.82
,008
4.045
0.243
0.046
3.920
0.236
0.046
3.12
,004
1.285
0.139
0.026
1.224
0.120
0.023
2.10
,046
1.177
0.118
0.024
1.117
0.120
0.024
2.23
.035
3.528
0.403
0.092
3.517
0.298
0.068
0.21
.839
3.638
0.401
0.111
3.563
0.281
0.078
1.22
,250
(n = 30)
M. mulatta
(n = 29)
S. oedipus
(n = 27)
C. jacchus
(n = 26)
S.sciureus
(mixed ages)
(n = 20)
S. sciureus
(adults)
(n = 14)
lS = standard deviation; sx = standard error;t
=
Student’s t-statistic (paired samples).
TABLE 3. S. sciureus: Length of Sylvian fissure anterior to central sulcus (cm)’
Sample
n
Mean
Left hemisphere
S
sir
Mean
Right hemisphere
sir
S
Mixedages
Adults
17
11
1.832
1.918
0.107
0.064
0.026
0.020
1.285
1.759
0.106
0.079
0.027
0.024
t
3.75
2.93
P<
.002
.015
‘See Table 2 for abbreviations.
placed medial surface down on a level platform. An Olympus OM-F 35-mm camera with
macrolens adaptor, mounted on a tripod
raised to a standard height for all specimens
that was sufficient to allow the entire lateral
surface of the brain hemisphere to appear in
focus in the viewfinder, was positioned above
the specimen. The camera back was leveled.
The brain hemisphere was positioned so that
in the viewfinder the Sylvian point appeared
in the very center of the focusing circle. A
slide was then exposed. Each developed slide
was projected onto a piece of 8” x 11” white
paper, using a darkroom enlarger kept at a
fixed position (for all slides). The course of
the Sylvian fissure and border of the cerebral
hemisphere were traced by hand onto the
paper from the projected image. The distance
to the posterior endpoint of the Sylvian fissure, perpendicular from a straight line
drawn connecting frontal and occipital poles,
was measured on each tracing with Vernier
calipers to estimate Sylvian point position.
These tracings were also used to estimate
length of the Sylvian fissure in M. mulatta,
as described in point 2 above.
Two-tailed paired-sample t-test (Tables 2,
3 , 6 , 7 , 10) and chi-square test (Tables 4,5,8,
9) values evaluating the statistical significance of asymmetry for each measurement
in each sample were calculated using the
Statistical Package for the Social Sciences
(SPSS, 1985). The &Testsassessed the significance of the rightAeft-hemisphere differences in mean length or height. Two chisquare statistics were calculated. “Chisquare (3)” compared frequences considering
three cells (numbers of cases showing greater
left-hemisphere, greater right-hemisphere, or
equal anatomical development); “chi-square
(L-R)” compared numbers of cases showing
asymmetry only (in other words, not the
L = R cases).
RESULTS
In four of the six brain samples (all species
except S. sciureus) mean length of the lefthemisphere Sylvian fissure was significantly
greater than mean length of the right-hemisphere Sylvian fissure (see Table 2). A tendency toward a disparity between the lengths
of these landmarks, in these species, was also
suggested by chi-square statistics. These values assessed relative numbers of brain specimens showing greater Sylvian fissure length
on the right, or left hemisphere (See Table 6);
most Chi-square values were significant at
the P < .05 level, left-hemisphere predominance being evident in all samples.
44
P.L. HEILBRONER AND R.L. HOLLOWAY
TABLE 4. Length of Syluian fissure from tracings (cm) in M. mulatta only (n = 28)'
Mean
Left hemisphere
S
s,
Mean
S
Si
t
2.030
0.390
12.819
2.172
0.418
0.001
12.807
Right hemisphere
P<
,999
IProjected images from enlarged tracings. See Table 2 for abbreviations.
TABLE 5. Frequency data: length of Syluian fissure from tracings in
M. mulatta'
No cases
L=R
No cases
L>R
No cases
R>L
2
13
Chi-square
(2)
0.00
13
'L > R, No. of cases of greater left hemisphere value; L = R, NO.of cases of
equal right- and left-hemisphere value; R > L, No. of cases of greater right
hemisphere value; Chi-square(2), chi-squarevalue considering all of above cases
(df = 2).
TABLE 6. Frequencies and chi-square statistics: length of Syluian fissure (all species)'
Species
M. fascicularis
M. mulatta
S. oedipus
C. jacchus
S.sciureus
(mixed-age)
S.sciureus
(adults)
L>R
No. of cases
L=R
R>L
Chi-square(3)
Chi-square (L-R)
18
18
16
13
9
3
4
5
9
3
9
7
6
4
8
11.40*
12.20*
8.72*
4.69
3.10
3.00
4.84*
4.54*
4.76*
0.06
7
1
4
1.50
0.81
'Chi-sq.(3), chi-square value considering all of above cases (df = 2); Chi-sq. (L-R), chi-square value considering all but L
= R cases (df = 1). See table 5 for other abbreviations.
*Significant at P < .05 level.
TABLZ Z Frequency statistics: length of Syluian fissure anterior to central sulcus in S.sciureus'
No. L > R
S.sciureus
(mixed-age)
S.sciureus
No. R
=
L
No. R > L
Chi-square (3)
Chi-square (L-R)
12
2
3
10.71*
5.40*
8
1
2
7.83*
3.60
*Significant at P < .05 level.
'See Tables 5 and 6 for abbreviations.
Statistics on length of the Sylvian fissure
from tracings made from slide photographs
of M. mulatta specimens did not indicate the
presence of statistically significant rightAeftside asymmetry (see Tables 4,5). Mean righthemisphere Sylvian-fissure length as determined by the photographyltracing method
was almost identicaI with mean left-hemisphere fissure length, and the number of
brain specimens showing greater Sylvian-fissure length in right-hemisphere tracings was
the same as that showing greater fissure
length in left-hemisphere tracings.
In both S. sciureus samples mean length of
the Sylvian fissure in the left hemisphere,
determined from measurements made by
hand on the cortex, did not differ significantly from the comparable right-hemisphere statistic (Tables 2,6). Chi-square
statistics also did not indicate a significant
difference between the length of the two Sylvian fissures in these samples.
Length of the segment of the Sylvian fissure lying anterior to the central sulcus was,
however, also determined on S. sciureus specimens (see Tables 3,7). It will be recalled that
45
ANATOMICAL BRAIN ASYMMETRIES
TABLE 8. Length of Sylvian fissure posterior to central sulcus (cm) in M. fascicularis and M. mulatta'
Left hemisphere
Right hemisphere
Mean
S
SDecies
Mean
S
Si
SC
t
P<
M. fascicularis
1.597
0.300
0.055
1.525
0.309
0.245
1.32
,197
2.181
0.198
0.037
2.095
0.275
0.051
1.59
.123
t
P<
(n = 30)
M. mulatta
(n
=
29)
'See Table 2 for abbreviations.
TABLE 9. Dorsoventral position of Sylvian point (cm in tracings)'
Left hemisphere
S
sir
S
sir
Right hemisphere
Mean
SS
sx
Mean
sx
Species
Species
Mean
Mean
M. fascicularis
(n = 30)
M. mulatta
(n = 30)
1.880
0.309
0.057
1.679
0.362
0.067
1.59
.124
1.802
0.434
0.081
1.842
0.376
0.070
-0.56
.583
'See Table 2 for abbreviations.
TABLE 10. Frequency and chi-square statistics: length of Sylvian fissure posterior to central sulcus,
dorsoventral position of Sylvian p o d
Species
M. fascicularis
(SF from CS)
M. mulatta
(SF from CS)
M. fascicularis
(Sylvian point)
M. mulatta
(Sylvian point)
L>R
No. of cases
L=R
R>L
Chi-square(3)
15
4
11
6.20*
0.62
18
4
7
11.25*
4.84*
17
2
11
11.90*
1.20
13
4
13
5.40
0.00
Chi-square(L-R)
'See Tables 5 and 6 for abbreviations.
*Significant at P < .05 level.
the anterior part of the Sylvian fissure, in
this species, borders mostly auditory fields.
In both the adult and mixed-age sample from
this species, mean length of the left-hemisphere anterior Sylvian fissure was significantly greater than mean right-side length.
Three of four chi-square statistics for S. sciureus also suggested a tendency toward
greater length of this fissure segment in the
left cerebral hemisphere than in the right.
Results of other measurements did not
suggest morphological righaeft-hemisphere
asymmetry. Most statistics for length of the
portion of the Sylvian fissure lying posterior
to the central sulcus (Tables 8, 10) did not
reveal the existence of a statistically significant right/left hemisphere anatomical difference in the M. mulatta or in the M. fascicularis sample; likewise measurements of
dorsoventral position of the Sylvian point
(Tables 9,lO) did not indicate significant
asymmetry in Macaca.
DISCUSSION
In four of the six monkey brain samples
examined in the present study, mean length
of the left-hemisphere Sylvian fissure was
significantly greater than mean length of the
right-hemisphere Sylvian fissure. This asymmetry was present in the M. mulatta, M.
fascicularis, C. jacchus, and S. oedipus samples. The two S. sciureus brain samples also
exhibited a significant temporal-lobe asymmetry favoring the left hemisphere, as revealed by data for measurements of length of
the part of the Sylvian fissure lying anterior
to the central sulcus.
These findings are consistent with results
reported by Falk et al. (1986) that indicated
Sylvian-fissure asymmetry, favoring the left
hemisphere, in Macaca mulatta.
The fact that both the present study and
Falk et al. (who used a computer image-analyzing system to evaluate configuration of
sulci from composite photographs) discerned
46
P.L. HEILBRONER AND R.L. HOLLOWAY
anatomical temporal-lobe brain asymmetry
in brains of monkeys, while earlier studies
(Yeni-Komshian and Benson, 1976; Falk,
1978) failed to find this asymmetry, may reflect measurement techniques and study
design utilized. Although they were statistically significant, mean rightAeft-hemisphere
sulcus-length differences in the present study
were small (on the order of 1-2 mm). Data on
petalias (asymmetrical lateral or anteroposterior elongations of the right or left cerebral
hemisphere; Gundara and Zivanovic, 1968;
Holloway and DeLacoste-Lareymondie,1982;
LeMay et al., 1982) show that gross anatomical asymmetries of this order of magnitude
are common-even typical-in nonhuman
primate and human brains. These characteristic departures from cerebral symmetry in
the primate brain necessarily cause right1
left-hemisphere differences in the curvature
of the cortex. Cortical curvature can foreshorten the length of a sulcus as it appears
in a photograph; in this respect, we believe it
significant that data for length of the Sylvian
fissure from photographs of M.mulatta hemispheres did not reveal statistically significant asymmetry. Falk’s 1978 anatomical
study of monkey endocasts (Falk, 19781,
which relied on photographs, is also noteworthy for the absence of rightAeft-hemisphere
asymmetries reported.
Aside from unreliable measurement techniques, problems in some previous studies
include conclusions drawn from small samples and the tendency to lump together data
for species in the same genus (presenting
scaling difficulties caused by increased variation in brain size, and obscuring speciesspecific characteristics). Moreover, findings
of a study by the authors that is in preparation suggest that sexual dimorphism in temporal-lobe asymmetry may be evident in
some nonhuman primate species. This observation suggests another possible explanation
for nonsignificant results in previous studies,
as none of the above research efforts accounted for numbers of brain specimens representing females and males in samples
examined.
In summary we would suggest that the
present study succeeded in demonstrating the
existence of a morphological temporal-lobe
brain asymmetry in monkeys by 1) examining adequately large samples of brain specimens 2) analyzing data at the level of the
species, not the genus, 3) using better measurement techniques, and 4) examining sam-
ples reasonably well balanced in terms of
numbers of specimens representing males
and females.
While our study is the first to report anatomical temporal lobe asymmetry in New
World monkeys and is only the second investigation to observe this asymmetry in Macaca, anatomical temporal-lobe lateral differences have been reported in several studies of pongid brains. Investigators have noted
the same rightAeft-hemisphere asymmetry
found in the present study-significantly
greater mean length for the Sylvian fissure
in the left hemisphere than in the right
hemisphere-in Pan troglodytes and Pongo
pygmaeus brain samples (Cunningham, 1892;
Eberstaller, 1884; Yeni-Komshian and Benson, 1976).(It is worth noting that all of these
investigators measured
Sylvian-fissure
length directly on the cortex of brain specimens, using foils shaped to the contour of the
cortex or thread tied to pins embedded at
intervals along the fissure.)
In Homo sapiens the Sylvian fissure is also
usually longer on the left cerebral hemisphere than on the right. This asymmetry
has been reported in neuroanatomical studies dating back almost a century (Cunningham, 1892; Von Economo and Horn,
1930; Connolly, 1950; Yeni-Komshian and
Benson, 1976).Furthermore, it is well known
that in humans left-temporal lobe auditoryassociation cortex plays a more important
role in language functions than does righthemisphere temporal-lobe cortex (Penfeld
and Roberts, 1959).
Did morphological and behavioral temporal-lobe auditory cortex asymmetry in nonhuman primates presage language lateralization in humans? Behavioral studies indicate that monkeys may exhibit left-temporal-lobe specialization for recognition of
acoustic features of species-specificvocalizations (Petersen et al., 1978, 1984; Beecher et
al., 1979; Heffner and Heffner, 1984); crossmodal matching functions also may show
greater development in the left- than in the
right-hemisphere temporal lobe in monkeys
(Dewson, 1977). It might therefore be suggested that these lateralized cognitive abilities in monkeys foreshadowed the evolution
of brain operations used in language, such as
auditory analysis and verbal conceptualization functions.
Caution appears warranted, however, in
extrapolating from evidence for temporallobe asymmetry in nonhuman primates. It
ANATOMICAL BRAIN ASYMMETRIES
will be recalled that a statistically significant rightneft-hemisphere difference in mean
length of the portion of the Sylvian fissure
lying posterior to the central sulcus was not
found in the M. mulatta or in the M. fmcicularis brain sample in the present study. In
contrast, in Homo sapiens this segment typically shows the most pronounced rightnefthemisphere difference of any portion of the
Sylvian fissure (Shellshear, 1937; Penfeld
and Roberts, 1959).This asymmetry in Homo
in turn probably reflects a difference between the two hemispheres in the size of the
planum temporale, a structure on the supratemporal plane adjacent to the posterior part
of the Sylvian fissure, consisting of cortex
necessary for auditory analysis and verbal
comprehension functions; studies have shown
that in most human brains the planum temporale is larger on the left hemisphere than
on the right (Penfield and Roberts, 1959; Geschwind and Levitsky, 1968; Wittleson and
Pallie, 1973; Chi et al., 1977; Galaburda et
al., 1978; Galaburda and Sanides, 1980). It is
probably significant that this structure is not
found in any other primate species (Cunningham, 1892; Connolly, 1950; Yeni-Komshian and Benson, 1976).
Rightneft asymmetry for height of the Sylvian point was not found in the Macaca mulatta and Macaca fmcicularis samples in the
present study. This pattern again differs from
that in humans: in Homo sapiens the Sylvian
point is usually situated more ventrally on
the left cerebral hemisphere than on the right
(Connolly, 1950; LeMay and Geschwind,
1975; Rubens, 1977), an asymmetry that
again may reflect cognitive specialization of
the left cerebral hemisphere. The Sylvian
point lies adjacent to the inferior parietal
lobule, a region on the left hemisphere associated with mediation of verbal conceptualization abilities, naming functions, reading
abilities, and other multimodal processes
(Penfield and Roberts, 1959).
Results of a comparative study of a nerve
fibre tract, the arcuate fasciculus (Galaburda
and Pandya, 1982), suggest other differences
between the temporoparietal area in the human and in the Old World monkey. The arcuate fasciculus connects temporal-lobe cortex to premotor frontal areas, in Homo s a p
iens linking the temporal-lobe auditory area
with the motor speech (Broca’s) region. In
Galaburda and Pandyas’ study the human
arcuate fasciculus was shown to include axons originating from the inferior parietal lob-
47
ule as well as efferent fibres of the temporal
lobe; in the brain of Macaca, by comparison,
the arcuate fasciculus did not make parietallobe connections.
Data on arcuate fasciculus connections in
pongids is lacking. However, results of anatomical studies show that the characteristic
tendency in Homo sapiens for the Sylvian
point to show asymmetry is shared by Pan,
Gorillq and Pongo (LeMay and Geschwind
1975; LeMay, 1976; LeMay et al., 1982). It
can be inferred from these studies that cortex
surrounding the left temporoparietal area
may have started to change, in comparison
to its right-hemisphere analogue, prior to the
divergence of hominids from pongids. On the
basis of evidence from the present study it
can be surmised that this development took
place after the appearance of the first
hominoids.
“Evidence from this and other studies suggests that monkeys may exhibit aspects of
the human pattern of temporal lobe asymmetry. Overall, however, temporal lobe lateralization in these primates appears to differ
from the asymmetry pattern in Homo. It is
of interest that in Heffner and Heffners’
study (1984), anterior temporal-lobe lesions
in Macaca caused impairment, whereas posterior lesions did not cause dysfunction.
Moreover, preliminary results of a study of
cytoarchitectonics in Macaca fuscata suggest
that posterior temporal-lobe subfields do not
show rightlleft-hemisphere asymmetry in
size, as they do in Homo sapiens (Rosen and
Galaburda, personal communication; Galaburda and Sanids, and Geschwind, 1978).
Studies investigating sues of cytoarchitectonic fields in the right and left cerebral
hemispheres of nonhuman primates would
improve our understanding of the anatomical asymmetries reported in this study and
in other investigations. Similarly, research
investigating primates other than Macaca
(especially New World monkeys and apes)
would help establish a sequence for the acquisition of cerebral asymmetries during primate evolution. Knowledge of this sequence
could enable us to formulate theories about
the evolution of the neuroanatomical basis of
language.”
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