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Brain lateralization in primates and its evolution in hominids.

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Brain Lateralization in Primates and Its Evolution in
Department of Sociology and Anthropology, Purdue University,
West Lafayette, Indiana 47907
Handedness, Visuospatial skills, Language, Musical abilities, Cerebral asymmetries, Left-handedness, Sex differences, Macaca
Recent studies suggest that vocal communication and visuospatial processing are lateralized to left and right hemispheres respectively
in monkeys of the genus Macaca, as they are in humans. The fundamental
neurological substrate that forms the basis for complex cerebral asymmetries
in Homo sapiens may therefore have been established remarkably early in
anthropoid evolution. The tendency toward cortical lateralization has been
greatly elaborated in human evolution, such that at least 90% of extant
humans are right-handed. Numerous data support an association of the left
human hemisphere with time-sequencing, language skills, certain neurochemical asymmetries, and specific psychiatric disorders. The right hemisphere, on the other hand, is associated with holistic processing, visuospatial
and musical abilities, emotional processing, and its own neurochemical and
psychiatric properties. Although a controversial topic, there appears to be
slight but significant sexual dimorphism in certain skills associated with
cortical lateralization in humans. Females excel at language and fine motor
skills, as well as emotional decoding and expression; males are relatively
adept at composing music and exhibit visuospatial and mathematical skills.
Various scenarios that account for these differences are reviewed, and it is
concluded that dimorphism in these behaviors may be due in part to hormonal priming involved in prenatal gender differentiation.
The purpose of this paper is to review the literature on lateralization in primates
and, in particular, to assess the evidence regarding sexual dimorphism in lateralization. The present review is written from an evolutionary perspective that covers
the topics of handedness, verbalhisual functions, psychiatric findings, and musical
abilities. The reader is referred to other reviews for discussions of lateralization and
emotion (Leventhal and Tomarken, 1986), the effects of gonadal hormones on sex
differences in play and spatial behavior (Beatty, 19841, and sex differences in brain
organization for verbal and nonverbal functions (Kimura and Harshman, 1984). An
especially comprehensive review of cerebral lateralization is provided by Geschwind
and Galaburda (1985a-c, 1987),who emphasize the possible genetic bases of lateralization as well as its relationship to immunological responses, sex hormones, and
other chemicals. Finally, a review of lateralization in nonhuman species is provided
by Glick (1985).
Lateralization refers to the concept that a given function is controlled preferentially by one side of the brain andor body. Some of the functions which are said to
be lateralized or asymmetrical in humans include handedness, language, recognition of faces, facial expressions, other visual skills, spontaneous sideward shifts of
0 1987 Alan R. Liss, Inc.
[vol. 30, 1987
the eyes, certain musical abilities, sense of body scheme, depression, and euphoria.
Methods for detecting asymmetry in primates include (1)clinical research on braindamaged individuals, subjects whose carotid arteries have been injected with sodium
amytal, and epileptic patients with surgically severed corpus callosums, (2) dichotic
listening and tachistoscopic visual tests in normal individuals, (3) observations of
somatosensory and manual asymmetries, (4) electrophysiological studies including
EEG and neurophysiological mapping, and (5)basic anatomical studies. The reader
is referred to McGlone (1980)for a review of these procedures. Research in all five of
these categories has been carried out on humans, whereas investigations on nonhuman primates have mostly (but not entirely) utilized methods 3-5.
The literature on lateralization is complex and contains many apparent contradictions, i.e., investigations of similar phenomena that arrive at seemingly opposite
conclusions. However, many of these apparent contradictions may be due to differences in methodologies or theoretical perspectives, and these are pointed out in the
appropriate sections below. Similarly, some of the sociopolitical implications are
discussed briefly in the concluding portion of the paper, but a wider discussion of
that topic is beyond the scope of this review.
One of the most obvious lateralized functions in humans is handedness. At least
90%of humans are right-handed and that hand is controlled largely by motor areas
in the left frontal lobe. Thus, right-handedness is generally believed to be a consequence of “dominance” of the left hemisphere. Populations of nonhuman primates
are not handed in the way that human populations are (see below). In order to gain
an evolutionary perspective on the origins of neurological asymmetry, it is important
to explore when and why right-handedness appeared in hominid evolution and to
ask what its relationship is to lateralization of language functions. One can do this
by the comparative approach of examining handedness in nonhuman and human
primates and by the direct method of investigating the archeological record for the
earliest signs of right-handedness in hominids.
Handedness in nonhuman primates
The literature on handedness in nonhuman primates is confusing and many
workers have concluded that populations of nonhuman primates fail to exhibit
statistically significant handedness, although individual monkeys may be righthanded, left-handed, or ambidextrous. In earlier reviews of handedness in nonhuman primates, Warren (1977, 1981) concluded that handedness in monkeys is not
the expression of any organismic asymmetry and that it is not homologous with
handedness in humans. Similarly, Marchant and Steklis (1986) have found that
cerebral asymmetries in chimpanzees are apparently not associated with handedness in the human sense.
The suggestion that nonhuman primates are not handed has recently been questioned in a study that required rhesus monkeys to produce specific pressures for
specific durations of time with the fingertips of right vs. left hands (Preilowski et
al., 1986). A number of separate experiments in this study show that (1)there is a
lack of intermanual transfer of the learned skills; (2) individual monkeys display
extreme degrees of hand preference, which, however, are independent of levels of
hand performance; (3)a forced change of hands during an experiment is frequently
accompanied by a change in finger position; and (4) when levels of difficulty are
adjusted to the performance of each hand, monkeys perform better with the right
hand (although the authors stress that this hand is not necessarily the preferred
hand). Preilowski et al. reach the cautious conclusion that monkeys exhibit independent development of skill in each hand and within each brain half, and they suggest
that similar characteristics may have resulted in handedness in humans.
A recent review has synthesized and made sense of the confusing literature on
handedness across the Primate order, and has done so from an evolutionary perspective (MacNeilage et al., 1987). This excellent review lends support to the findings of
Preilowski et al. discussed above. MacNeilage and his co-workers surveyed studies
from prosimians to apes and found that left-hand preferences, when they occurred,
were for visually guided reaching that “may reflect a spatio-motor specialization of
the right hemisphere related to the right hemisphere visuo-spatial specialization of
humans.” On the other hand, right-hand preferences (which occurred for some
monkeys and apes but not prosimians) were for acts that required manipulation
andlor practiced performance. This “mixed” handedness pattern, whereby primates
may be left-handed for some activities and right-handed for others, accounts for the
apparent inconsistency between the findings of MacNeilage et al. (1987) that nonhuman primates are right-handed for some tasks, and those of other workers who
have concluded that nonhuman primates are not handed in the human sense (e.g.,
Marchant and Steklis, 1986). Clearly, both of the above statements can be true.
Although monkeys are right-handed for some tasks, they are not unilaterally handed,
as are most humans.
MacNeilage et al. suggest that the “mixed” handedness that characterizes nonhuman anthropoids is the result of adaptations to feeding during the earliest stages
of primate evolution. To wit, left hands were engaged in ballistic reaching for insects
and small animals (guided by visual skills lodged in the right hemisphere) while
right hands were occupied clinging to vertical supports. Such postural clinging of
the right hand eventually evolved into fine somatic sensorimotor control as right
hands became more prehensile through time. Eventually, relatively skilled right
hands were able to participate in processing food (e.g., peeling fruit), a specialization
that developed in the context of the evolution of bimanual coordination. The authors
suspect that right-hand preference for manipulation is lacking in prosimians and
they therefore believe that left-handedness may have occurred before its coexistence
with right-handedness in other nonhuman primates. In humans (MacNeilage et al.,
1987:280) “the importance of the ability t o operate on the environment, including
the use of bimanual coordination, and the consequent right hand preference, has so
increased that the right hand now normally preempts the left, even for visually
guided movement.”
MacNeilage et al.’s finding of a dichotomy in the types of activities engaged in by
right and left hands of nonhuman primates is convincing, as is their visualkpatial
explanation of why primates prefer to reach with their left hands (right hemisphere).
In keeping with this, a recent finding of skeletal asymmetry in the forelimb of
rhesus monkeys has been interpreted as support for the notion that this species may
rely preferentially on the right hand for certain manipulations (Falk et al., 1987).
Furthermore, the feeding hypothesis outlined above is concordant with Cartmill’s
(1974) “bug-snatching theory” that accounts for an array of early primate specializations. The suggestion that right-handedness for manipulation resulted from vertical clinging seems less convincing. An alternate explanation might be that
manipulations of the right hand require motor sequencing skills already laid down
in left hemispheres of monkeys in conjunction with vocalization systems (Falk,
1980a; Falk et al., 1986; Falk et al., 1987; and see below). If so, the basic verbal/
visual dichotomy that characterizes hemsispheric asymmetry in humans may have
had precursors in primates that lived over 50 million years ago.
Handedness in people
Estimates of the incidence of left-handedness in the general population range from
4 to lo%, with a mean of 8%for the three largest samples (n=3,298, 3,542, 7,688)
included in a survey by Springer and Searleman (1980). These findings fit well with
another finding of 9% left-handedness in a sample of 1,880 subjects Onglis and
Lawson, 1984).The latter study reported that 10%of 940 men and 8%of 940 women
were left-handed, i.e., that there is not a “reliable interaction between sex and
handedness.” Nevertheless, many workers accept the earlier notion of a higher
frequency of left-handedness in men than in women (Geschwind and Galaburda,
p o l . 30, 1987
Studies of EEG alpha activity show that being left-handed, or evenjust having lefthanded relatives, has important implications for various cognitive tasks. Thus (Glass
et al., 1984:169):
In particular, it is known that the specialisation of the left hemisphere
for verbal processes is more consistent among right handed people than
among left handers. . . . It appears that this asymmetry is absent or
reversed in a significant proportion of left handers. A family history of
left handedness also predisposes to deviation from the classical pattern
of cerebral lateralisation, even in overtly right handed individuals.
Glass and his colleagues found that right-handed males and females without lefthanded relatives utilize left hemispheres (i.e., parietal alpha rhythm is suppressed
therein) during tasks that involve mental arithmetic, recognition of faces, and a
tactile shape unification test (the latter two are surprising since they have previously been regarded as right-hemisphere tasks). Both right-handed males and females with left-handed relatives “switch” to right-hemisphere dominance for
recognition of faces and the shape unification test, whereas only females also switch
t o this hemisphere for the mental arithmetic test.
The authors of another study of EEG measures of hemisphere specialization (Galin
et al., 1982) correctly note that “language is not a unitary function.” Accordingly, in
their studies they monitor EEG activity for a variety of tasks including writing,
speaking, reading, listening, and reproducing block designs. Greater engagement of
the left vs. right hemisphere was found in a significant order among the tasks, such
that: write > speak > read > listen. Although unnoted by the authors, this
hierarchy suggests that left-hemisphere dominance correlates with the extent to
which a task is motor (with writing being more motor than speaking because
presumably both Broca’s area and hand areas of motor cortex would be involved).
Glass et al. also found the greatest relative right-hemisphere activation (no matter
which hand is used) in spatial motor tasks such as block design (see, however,
Nagae, 1985). Finally, “no sex difference was found among right-handers on any
task with any measure at any lead.” However, left-handed females showed 46%
reversed laterality for speak versus blocks as opposed to 27% of male left-handers
which suggests ‘‘ a possible sex difference among non-right-handers.”
The question of whether or not there are subtle sex differences in handedness in
the majority of the population ke., right-handers) is problematical (McGlone, 1980).
McGlone’s survey of the literature showed that direct measures of unimanual motor
skills on tasks of speeded coordination, strength, or flexion of individual fingers
revealed no significant differences in left-right asymmetry between the sexes. She
therefore concluded that “hemisphere control over basic motor skills of the contralateral limb or facial musculature . . . is not more asymmetrical in one sex compared
to the other, at least in adult samples.” Nevertheless, McGlone shows that for a
greater variety of tasks, females more often claim right-hand preferences than do
males, whereas males show greater asymmetry of function for certain spatiaUmotor
tasks such as making judgments about line-orientation (Benton et al., 1978) or
balancing a dowel (Lomas and Kimura, 1976).
Recently discovered sexual dimorphism in anatomical asymmetries
LeMay (1976; Galaburda et al., 1978) has pioneered the study of the relationship
between “petalias” (asymmetric brain shapes) and handedness, based on radiographic studies in conjunction with personal histories. The posterior portion of the
left hemisphere and the anterior portion of the right hemisphere are wider and
protrude far more often than their contralateral counterparts (left occipital and right
frontal petalias). LeMay and her colleagues showed that these “normal” conditions
are statistically associated with right-handedness, whereas the reverse conditions
(right occipital and left frontal petalias) occur in high frequency in left-handers.
LeMay’s findings have recently been confirmed (Shapiro et al., 1986) and extended
to include an investigation of the relationship between sex and petalias (Bear et al.,
1986). Results of the latter study show that greater degrees of frontal and occipital
asymmetries are present in men than in women and that reversals of typical
asymmetries are more common in women.
Another anatomical structure of recent interest is the massive nerve pathway that
connects right and left hemispheres, i.e., the corpus callosum. The preliminary
observation of sexual dimorphism in certain aspects of the corpus callosum (de
Lacoste-Utamsing and Holloway, 1982) has recently been questioned (Demeter et
al., 1985). Witelson (1985) found that the midsagittal area of the corpus callosum is
11%larger in left-handed and ambidextrous individuals than in right-handed people,
and she suggests that this finding may provide the anatomical basis for the greater
bihemispheric representation of cognitive functions typically found in left-handers
and ambidextrous individuals. She also notes that while there is no sexual dimorphism in right-handers, mixed-handed males may tend to have a relatively larger
posterior half of the corpus callosum than mixed-handed females. See McGlone
(1980)for a review of other anatomical asymmetries.
The evolution of handedness
What of the relationship of handedness in human populations to the evolutionary
scenario presented above for nonhuman primates? Is left-handedness in humans
similar to left-handedness in nonhuman primates? Apparently not. Just as righthanded (i.e., left hemisphere) manipulations “took over” in humans compared to
nonhuman primates, left-handedness (i.e., right-hemisphere “dominance”) takes
over in a minority of humans. In approximately 8-9% of the population, right
hemisphere functions predominate to the degree that even skilled manipulations
are performed with left rather than right hands. Thus, left-handedness may be
viewed as one manifestation of more general right-hemisphere dominance for a
range of activities. Such a construct is in keeping with the fact that right-handed
people with left-handed relatives are more likely to use their right hemispheres for
recognition of faces or shape unification tests than right-handed people without lefthanded relatives. That is, left-handedness may be viewed as a literal “breakthrough” of a right hemisphere activity represented by one particular area (hand) of
a relatively continuous body map represented along the primary motor cortex in the
right hemisphere. This concept is concordant with an earlier proposed “field effect”
to account for the high frequency of hemispheric coincidence of right-handedness
and language functions in humans (Falk, 1980a).
Most studies on lateralization have failed to control for right-handed individuals
who have left-handed relatives (Glass et al., 1984),which probably accounts for much
of the confusion in the literature. The literature suggests that sexual dimorphism in
handedness exists for some functions under some circumstances, but that it is hard
to demonstrate. Evidence for sexual dimorphism appears in studies of left-handers
(with females being especially unusual as compared to right-handers of both sexes)
and may show up especially for tasks that entail visualhpatial skills (see below).
Hand preferences appear very early in life and it is interesting that “consistency in
hand preference across time is indicative of precocious intellectual development for
females, but not for males, during infancy and the preschool years” (Gottfried and
Bathurst, 1983).
Finally, recent evidence based on analyses of the morphology of stone flakes
produced from knapping stone tools suggests that hominids had become righthanded by 1.5-2.0 million years BP (Toth, 1985). This finding is perfectly in keeping
with analyses of endocranial casts of early hominids that show that the earliest
evidence for Broca’s speech area in left hemispheres is seen in KNM-ER 1470, a
Homo habilis specimen dated to 2 million years BP (Tobias, 1981; Falk, 1983). In
sum, handedness is hardly a simple phenomenon, and it should not be viewed in
isolation from other asymmetrical cognitive functions.
We turn now to functions which are less obviously lateralized in the majority of
the population than is handedness - namely, verbal (language) skills that are
[Vol. 30, 1987
primarily associated with the left hemisphere, as opposed to visuospatial skills that
depend largely on the right hemisphere. Bradshaw and Nettleton (1982) are correct
in stating that a more fundamental dichotomy might be described as analytical
processing vs. global or holistic processing since sensory and motor verbal processing
is based on left-hemisphere dominance for analytical, timedependent, sequential
mechanisms (e.g., Schwartz and Tallal, 1980) whereas visuospatial processing is
apparently dependent upon right-hemisphere gestalt analysis and overall pattern
perception. Although it is almost a cliche that females are more verbal than males
and males are better at spatial analyses than females, the literature on sexual
dimorphism in lateralization of these functions is far from clear. In fact, the only
generalization that emerges with even an approximate consensus is that functional
brain asymmetry may be less marked in the female than the male population, i.e.,
that males may be “more lateralized” than females (McGlone, 1980). However, as
McGlone points out (1980:250):
For perceptual measures (dichotic listening or tachistoscopic viewing),
the results indicate generally that where differences can be detected,
males show the greater degree of asymmetry. Yet, for the motor system
it is females who tend to show the greater degree of asymmetry. Thus,
the putative sex difference is hardly robust.
Females tend to outperform males on tests of verbal ability including reading
comprehension, analogies, creative writing, word memory, Wechsler similarities,
word fluency, and recall of digits (reviewed in Hirst, 1982). Women are also characterized by shorter reaction times in recognizing stimuli, shorter brain reaction time
to evoked-potential studies, and higher cerebral blood flow rates than are males
(summarized in Hanske-Petitpierre and Chen, 1985). Apparently, females show
greater asymmetry for melodic patterns and environmental sounds than do males
(Kimura and Harshman, 1984). Healey et al. (1985) review studies that show that
females tend to be more dextral than males, that they have a greater rightward bias
in fine motor skills such as finger-tapping and graphomotor coding, and that they
are more lateralized for tasks involving speech and whistling. These authors therefore conclude that females may be more left-hemisphere biased for general motor
expressions than are males.
Males, on the other hand, test better than females for perception and manipulation
of spatial relationships such as mental rotation of figures, maze tracing, map reading, a rod-and-frame test, and remembering positions of digits (Hirst, 1982). They
also are better at left-right discriminations, disembedding figures, and localizing
points (reviewed in McGlone, 1980). In short, females are associated with at least as
many verbal specializations as men are with visual skills. Why then are males
believed to be “more lateralized” than females?
Although women appear to be relatively verbal while men seem to be especially
skilled at certain kinds of visual processing, these patterns can be misleading if
applied too literally to speculation about how male and female brains actually
function. McGlone’s (1980) survey (confined to right-handers) of the clinical literature shows that males demonstrate significant verbal deficits subsequent to lefthemisphere lesions, whereas females do not. The incidence of aphasia after lefthemisphere lesions is at least three times higher in men than in women (McGlone,
1980). There is less clinical evidence for sexual dimorphism in the degree to which
visuospatial skills are lateralized. However, McGlone does point out a small number
of studies that show males to be more dependent on the right hemisphere on certain
visuospatial tasks than are females. She therefore concludes that the adult clinical
literature shows that functional brain asymmetry for nonverbal and verbal functions is less marked in females than in males.
According to the above model, females tend to process information with both
hemispheres whereas males tend more to rely on one hemisphere or the other. This
generalization finds limited support from McGlone’s (1980) survey of dichotic and
tachistoscopic studies, but is not without controversy (Kimura, 1983; Kimura and
Harshman, 1984; Healey et al., 1985; Snow and Sheese, 1985; and see below).
Nevertheless, the notion that brains of females are functionally more bilaterized
than those of males seems to have gained fairly wide acceptance (Hirst, 1982;
Hanske-Petitpierre and Chen, 1985). Interestingly, a dichotic listening study of
children (Gordon, 1983)reveals that young boys and girls
are both left-hemisphere specialized for “speech,” but that the adult pattern is
established by late childhood (i.e., older girls exhibited no significant ear advantage).
Within- us. between-hemispheresexual dimorphism
Two important studies demonstrate sexual dimorphism in the anterioriposterior
organization within left hemispheres. Stimulation mapping studies (Ojemann, 1983)
revealed that naming functions are based on larger areas of frontal (and to a lesser
extent parietal) lobes in males than in females. Furthermore (Ojemann, 1983:200):
Conceivably this difference in intracortical localization could reflect the
somewhat stronger functional lateralization in the male than the female
brain (McGlone 1980).The issue of sex differences in brain organization,
then, probably extends beyond lateralization, into the largely unexplored
area of intracortical localization.
Kimura’s (1983;Kimura and Harshman, 1984)retrospective study of the incidence
of aphasia and apraxia showed that speech disorders and manual apraxia occurred
significantly more often in women due to damage in the left frontal hemisphere,
whereas these conditions occurred significantly more often in men due to posterior
parietalhemporal lobe damage. Kimura therefore suggests that functions vested in
posterior regions in males are subserved by anterior regions in females and, like
Ojemann, she suggests that the appearance of more bilaterality in female brains
might be largely an artifact due to sexual dimorphism in intrahemispheric
It should be noted that the results of these two studies are not necessarily contradictory. Results of cortical mapping in bilingual patients suggest that the area of
cortex used for naming may be greater in the more difficult (i.e., secondary)language
(Ojemann, 1983). Thus, greater areas subserving naming in left frontal lobes of
males does not conflict with Kimura’s conclusion that general language functions
are based more profoundly on the left frontal lobe in females than in males. That is,
diffuse naming representation in the left frontal lobes of males could be indicative
of a relative lack of refinement in frontal-lobe language skills.
The findings that females appear to be more dextral than males and have a greater
rightward bias for refined motor skills (discussed above) are also corroborated by
Kimura’s study of patients with left-hemisphere lesions. In fact, Kimura concludes
that, in women, manual praxias and constructional ability are at least as dependent
on the left frontal lobe as are speech-related skills. In sum, these two studies make
an important contribution because they illustrate the need for further investigations
of sexual dimorphism in intrahemispheric organization.
Recognizing faces is an important ability for primates including humans, in whom
this process is impaired by lesions in certain areas of the occipital and temporal
lobes. Nevertheless the literature on sexual dimorphism in lateralization for perceiving faces is contradictory. On the one hand, the prevailing perspective is that males
rely more heavily on right hemispheres (left visual field) for perceiving faces than do
females (McGlone, 1980). On the other hand, several studies dispute this contention.
For instance, a study that required 3- and 4-year-old boys and girls to identify the
sex of male and female faces presented to right and left visual fields claimed that
girls show no field advantage whereas boys are characterized by a strong right
visual field (left hemisphere) advantage (Jones and Anuza, 1982). It would be more
[vol. 30,1987
in keeping with Figure 1 of the latter study to conclude that boys and girls are
equally good at the task when carried out by the left hemisphere, whereas boys, but
not girls, are terrible at describing faces perceived by their right hemispheres.
Other studies also contradict the notion that recognition of faces is a righthemisphere function. Emotional faces (especially if they are “positive”) are reported
to be perceived faster in the right than in the left visual field, and males respond
faster than females do to these tests (Stalans and Wedding, 1985).Such lateralization
for afTective processes appears to be established by 10 months of age (Davidson and
Fox, 1982). Along these lines, “facedness for pleasant expressions” is positively
correlated with handedness for males but not for females (Borod et al., 1981); i.e.,
right-handed males would also produce pleasant expressions more easily with the
right than the left sides of their faces. What accounts for these apparent contradictions in the literature on recognition of faces?
Much of the confusion is likely due to poor research designs that do not control
adequately for confounding factors. For example, the Jones and Anuza (1982) investigation of children failed to take into account that the gender of a face perceived by
the right hemisphere must be labeled by the left hemisphere. The greater inability
of boys to attribute sex to faces perceived by the right hemisphere may have more
to do with maturation of connectivity between the hemispheres than with righthemisphere disadvantage in face perception. Failure to control for right-handed
individuals with left-handed relatives can also affect test outcomes. For example, an
elegant EEG study (Glass et al., 1984) showed that right-handed males and females
without left-handed relatives utilize their left hemispheres more than their right
when recognizing faces (however, one should not lose sight of the fact that both
hemispheres are “engaged” during this task). On the other hand, right-handed
individuals of both sexes with left-handed relatives %witch” dramatically to greater
use of right than left hemisphere during these tests. The same pattern holds for the
figure unification test. Still other contradictory results can occur from studies that
fail to use identical methods when testing for hemispheric involvement in face
recognition. Levine and Koch-Weser (1982),for example, report a right-hemisphere
advantage for recognition of famous faces in right-handed individuals who have
right-handed parents. These authors note that a right hemisphere advantage has
also been found for recognition of unfamiliar and familiar faces by other workers
using experimental procedures similar to their own. Levine and Koch-Weser attribute occasional findings of a left-hemisphere advantage in recognizing faces to differing methodologies, some of which “may involve the activation of a series of verbal
associations, thereby increasing left hemisphere involvement in the task.” Levine
and Koch-Weser’s arguments are convincing. Carefully controlled experimental
procedures suggest a basic right-hemisphere advantage for recognition of faces in
humans. It is interesting that Hamilton and Vermeire (1985) report a right-hemisphere superiority for differentiating photographs of monkeys’ faces in split-brain
rhesus monkeys. Similarly (Ifune et al., 19841, the number of facial expressions
elicited from the right hemispheres of split-brain rhesus monkeys is greater than
the number of faces made with left hemispheres.
Males are better at visuospatial imagery
In addition to the recognition of faces by both sexes, the right hemisphere is
implicated in numerous visuospatial functions at which males excel. For example, a
study of tactile perception of ambiguous figures (Lenhart and Schwartz, 1983)found
that males performed much better with right and especially with left hands (right
hemisphere) than did females, but only under conditions where participants were
instructed to rely exclusively on mental imagery. When instructions were to rely on
verbal strategies, females outperformed males but the differences were not as dramatic as for imagery strategies. The authors therefore concluded that males have
“privileged access to right-hemisphere imagery codes.” The results from control
groups who were given no specific coding instructions were particularly striking
because males performed as if they had been given verbal rather than imagery
coding instructions even though they perform more successfully using imagery
strategies! Perhaps these results have implications for the primacy of language
functions in Homo sapiens?
An earlier study of sexual dimorphism in performance on spatial aptitude tests
(Guay and McDaniel, 1978)shows that males are significantly better than females
at four of the five types of visual tasks that were investigated. These four tasks
involved three-dimensional figures, whereas the one test that did not separate the
sexes entailed flat two-dimensionalfigures.
Guay and McDaniel found that, despite their relatively poor performance, females
report that they enjoy spatial thinking to a greater extent than reported by males,
and the authors conclude that cultural variables may account for much of the
discrepancy in spatial aptitude between the sexes. As with many earlier studies,
this one did not control for right-handed individuals with left-handed relatives, so a
lack of clear-cut findings regarding neurophysiological factors is not suprising.
Nevertheless, the findings regarding sexual dimorphism in performance on certain
visuospatial tasks are significant and examples of these problems are provided in
Figures 1-4.(Solutions to the tests are given in Fig. 4.) Although cultural factors
may partially explain sexual dimorphism in spatial aptitude, the fact that males
IS R O T f l T E O T O
Fig. 1. Mental rotation test. Study how the object in the top line is rotated and select the object from the
bottom line that looks as the figure in the second line would appear if it were rotated in exactly the same
way. Example provided by Roland Guay.
\L '
Fig. 2. The example shows an object positioned in the middle of a glass box, and drawings A-E show the
same object as seen from different views. Select the view that would be seen if the black dot were located
between the object and the viewer's eyes. Courtesy of Roland Guay.
[Vol. 30, 1987
Fig. 3. The upper diagram shows a three-dimensional figure that has been flattened; the shaded portion
indicates the bottom surface. Select the appropriate figure that represents what the upper figure would
look like when it is folded into a three-dimensional object. Provided by Roland Guay.
Fig. 4. The instructions for this problem are the same as for Figure 3. While Figures 1-3 provide very
simple examples of mental imagery tests, this example provides a more complicated example. Courtesy of
Roland Guay. As a population, males perform better than females on the kinds of visual imagery tests
represented in Figures 1-4. See text for discussion. Solutions to the tests are the following: Fig. l=D,
2=E, 3=E, 4=B.
outperform females on these tasks raises fascinating questions about the possible
adaptive significance, if any (see below), of these skills.
According to Flor-Henry (1983), lateralization and sexual dimorphism of the cerebral cortex are both determined in the third month of intrauterine life by testosterone-mediated neurohumoral interactions. The brain also appears to be lateralized
for immune recognition with an intact left neocortex being essential for T-cell
numbers and activities (Renoux and Biziere, 1986). The relationship between the
immune system and testosterone has recently been explored by Geschwind and
Behan (1982) and Geschwind and Galaburda (1985a-c, 1987) who showed that lefthanders are more susceptible to autoimmune diseases and certain learning disabilities. The authors suggested that these relationships are mediated by an excess of
testosterone in the fetus,
The topographic distribution of neurotransmitter systems appears to be asymmetrical with dopaminergic and cholinergic systems biased toward the left hemisphere
whereas serotoninergic and noradrenergic systems seem biased toward the right
hemisphere @'lor-Henry, 1983,1985).The development of cholinergic neurons in the
right hemisphere is apparently accomplished during fetal life whereas those on the
left side are developed later in postnatal life (Amaducci et al., 1985). This finding
agrees with the concept of a more slowly maturing left than right hemisphere, an
effect which is less marked in girls than in boys (Sherwin, 1985; Geschwind and
Galaburda, 1987).
Studies of temporal lobe epilepsy have revealed statistical relationships between
schizophrenia and left temporal lobe epilepsy on the one hand, and manic-depressive
psychoses and right temporal lobe epilepsy on the other @lor-Henry, 1983, 1985).
Furthermore @lor-Henry, 1983))cerebral mood systems are believed to be asymmetrical (Serafetinides, 1985; Leventhal and Tomarken, 1986))with a left-hemisphere
association for euphoria, anger, and paranoia and a right-hemisphere basis for
sadness, fear, and dysphoric mood. However @lor-Henry, 1983:48):
The neural substrate for emotion, normal and abnormal, is predominantly nondominant but its regulation is a function of both the dominant
and nondominant regions-for different emotions. The right and left
controlling systems are themselves under active reciprocal interaction
through transcallosal neural inhibition. In this manner anger, euphoria,
paranoid mood are evoked when the nondominant hemisphere no longer
controls the dominant systems.
Levy (1983) questions the above and suggests that emergence of euphoria after
right hemisphere inactivation and of depression after inactivation of the left hemisphere might reflect ipsilateral limbic release. She aftkms the role of the right
hemisphere for emotional function, stating that mood is positive when the arousal
level of the right hemisphere is high and is negative when its arousal level is low.
Whatever the mechanisms for facilitating the expression of emotions, a recent
survey of the literature on emotional expressiveness (Hanske-Petitpierre and Chen,
1985) reveals a general pattern of higher emotional expressiveness in women than
in men, as well as a higher female advantage in decoding emotional stimuli.
The psychiatric literature related to lateralization is at least as controversial as
that pertaining to other areas discussed in this review (see for instance MeyerBahlburg, 1983). Nevertheless, statistics concerning specific populations that suffer
differentially from certain psychiatric disorders are suggestive. As populations, men
and women suffer from a number of different psychiatric disorders which appear to
be related to sexual dimorphism in cerebral organization. Females are aMicted more
often than males with neurotic and psychotic forms of depression, phobias, hysteria,
and anxiety (Flor-Henry, 1983). Males, on the other hand, are more susceptible to
aggressive psychopathy, sexual deviations, and early onset, poor-prognosis schizophrenia @lor-Henry, 1983). Furthermore, all of the major developmental language
disorders including aphasia, dyslexia, stuttering, and infantile autism are approximately three times more prevalent in boys than in girls (Hier and Kaplan, 1980;
Geschwind and Galaburda, 1985a-c; 1987). It is also interesting that the mentally
retarded, including those suffering from infantile autism, are characterized by
significantly higher rates of left-handedness than the general population (Kimbourne, 1985).
According to West et al. (1985))our comprehension and response to music depends
on our ability to perceive patterns. As listeners, we share common perceptual
processes which composers take into account to cause us to perceive a particular set
of patterns. The authors point out that music and natural languages are analogous
in that both are temporally patterned and both are differentiable from nonlinguistic
or nonmusical noise. They further suggest that transformational rules of linguistics
are applicable to music, i.e., that the concepts of deep and surface structures, rewrite
rules, generative grammars, and well-formedness may be applied to music as well
as language. However (West et al., 1985: 33), “Music does not exist to convey
meaning in the same way (as language). It exists to provide listening satisfaction, to
accompany rituals, and so on. . . . In the case of music, we are in a similar position
to someone who is attempting to judge the grammatic correctness of a language he
or she does not understand.”
[vol. 30,1987
West et al.’s analysis makes sense because music is believed to be associated
largely with the right hemisphere. Thus, music may be viewed as a kind of “language” of the right hemisphere and one which is characterized by the same attributes that are used to describe that hemisphere, i.e., “emotional,” “nonverbal,” and
“holistic.” Interestingly, human song synthesizes components of both music and
language and is believed to be represented in comparable regions of the frontal
cortex in both hemispheres (Crosby et al., 1962514).Human song then, may approximate a symmetrical neurological phenomenon.
The right hemisphere is believed t o be the visuospatial as well as the musical
hemisphere, and gestalt principles of perceptual organization are frequently used to
draw analogies between sound (music) and visual-form perception (reviewed in
Watkins and Dyson, 1985). Thus, rules of proximity, similarity, and good continuation apply to both auditory and visual perception. Other properties that are said to
apply to both domains include translation, distortion, figure-ground relationships,
and closure (Crosby et al., 1962).In particular, visual and auditory contours may be
perceived by similar mechanisms in humans.
The term “contour” refers to the general shape of a melody, i.e., whether adjacent
notes are higher or lower than each other. In visual shape perception, some elements
of overall contour, such as corners, are more salient than others. Similarly, melodic
contour may be defined by reversals in pitch which Watkins and Dyson (1985) refer
to as “auditory corners.” Contour is an important aspect for remembering music as
well as for communicating its structure, and it may be that “shaping” or composing
music draws on right hemisphere skills similar to those used in visual mental
rotation tasks (see above and Figs. 1-3).
There are hints in the literature that suggest that the ability to compose music
depends on the right hemisphere (Waldrop, 1985) and that a high frequency of
musicians may be left-handed (Deutsch, 1980; Byme, 1974). One, of course, cannot
delineate precisely the cultural vs. biological variables that have contributed to
traditional sexual divisions in productivity. Nevertheless, it is fascinating that the
geniuses at musical composition have usually been represented by the sex that
excels differentially at another right-hemisphere activity-namely, mental manipulations of three-dimensional visual figures. Not much is known about genius female
composers and, tragically, Lili Boulanger, who is reputed to have been one of the
world‘s most gifted female composers, died in 1918 at the age of 24 (Rosenstiel, 1978).
A number of studies report different lateralization patterns for musicians and
nonmusicians (Shanon, 1984). Bever and Chiarello (1974)found that musically naive
listeners recognize simple melodies better with the right hemisphere (left ear) than
with the left but that musically sophisticated listeners utilize the left hemisphere to
recognize melody. These findings have been interpreted as consistent with the view
that the left hemisphere is dominant for analytical processing while the right
hemisphere engages in holistic processing of music. This finding was confirmed by
Gordon (1975), who also reported a right-hemisphere superiority in musicians for
recognizing chords (Gordon,1970).Using dichotic techniques combined with analysis
of eye movements, Rainbow (1982) confirms that nonmusicians utilize the right
hemisphere to process music but reports a bihemispheric strategy for musicians.
Experiments by Selby et al. (1982) also contradict the findings of Bever and
Chiarello (1974). These authors find that musically untrained people recognize tone
sequences better with their left than their right hemispheres, while the musically
sophisticated recognize sequences equally well with either ear. They conclude that
the analytic strategies of the left hemisphere are developed spontaneouslyby “everyday listening” and that it is primarily the right rather than the left hemisphere
that benefits from musical training. Interestingly, the experiments of Selby et al.
revealed sexual dimorphism in the response to musical training, a finding which the
authors believe to be consistent with McGlone’s (1980)hypothesis that women show
less hemispheric specialization than do men. Shanon (1984) also reports sexual
dimorphism in which male but not female musicians show a significant preference
TABLE 1. Hemispheric dimorphism’
Associated with left hemisphere
Associated with right hemisphere
1. Analytical, time-sequencing
2. Verbal, language skills
3. Skilled motor function, right hand
4. Immune system processes
5. Relatively slow maturation
6. Dopaminergic, cholinergic systems
7. If damaged sadness, fear;
temporal lobe epilepsy:
1. Global, holistic processing
2. Visuospatial, mental imagery
3. Musical abilities
4. Emotional processes
5. Relatively fast maturation
6. Serotoninergic, noradrenergic systems
7. If damaged euphoria, anger, paranoia;
temporal lobe epilepsy: manic-depression
‘Entries represent gross generalizations based on the literature cited in this paper. Scientific experiments are usually
required to determine functional differences between the hemispheres, which are often subtle but statistically significant.
See text for further discussion and exceptions to these generalizations.
TABLE 2. Behavioral sexual dimorphism‘
Females excel at
Males excel at
1. Verbal, language skills
2. Rightward bias for fine motor skills
3. Emotional decoding and expression
Suffer from:
depressions,phobias, hysteria
1. Visuospatial skills
2. Mathematics
3. Musical composition
Suffer from:
developmental language disorders,psychopathy,
schizophrenia, sexual deviations
‘Entries represent gross generalizationsbased on the literature cited in this paper. Scientific experiments are usually
required to determine male/female differences in these behaviors, which are often subtle but statistically significant.
See text for further discussion and exceptions to these generalizations.
for arrangements of instruments in which the leading (usually high) voice is administered to the left ear (right hemisphere).
Despite the complexity of the topic under review and the confusion that abounds
in the literature, certain generalizations concerning (1)the right hemisphereAeft
hemisphere dichotomy and (2) sexual dimorphism in neurological processing “float
to the top.” These are listed in Tables 1 and 2. It should be noted, however, that
these generalizations are indeed gross, for many exceptions have been noted above.
Fewer exceptions would exist if workers would control for right-handed individuals
with left-handed relatives (Glass et al., 1984)as well as for sexual dimorphism in
intrahemispheric organization (Ojemann, 1983;Kimura, 1983).
Unfortunately, the literature on lateralization tends to reify separate identities
for the hemispheres, i.e., to emphasize differences and to ignore the fact that in
normal individuals both hemispheres engage in most activities. Furthermore, numerous workers (Bleier, 1984;Meyer-Bahlburg, 1983)have questioned the utility of
investigating sexual dimorphism in lateralization because there is massive overlap
in the distributions for both sexes of the traits under consideration (Meyer-Bahlburg,
If one uses relatively pure ability measures, the sex difference favoring
females on specific verbal abilities amounts to about a quarter of a
standard deviation, and the one favoring males in visual-spatial perception to about 0.4 standard deviations . . . corresponding to about 1% and
4% of the total interindividual variance. . . . These findings imply massive overlap of the distributions of both sexes. . . .I find it hard to imagine
that such a fine sex difference in cognitive functioning will easily be
traced back to clearly definable functional andor structural sex differences in the brain.
[vol. 30, 1987
One cannot help but sympathize with the above view when confronted with
“creeping Jensenism” (Brace and Livingston, 1975) such as the following (Gowan,
It appears to this writer that recent medical advance has conclusively
settled a question which has perplexed educators for some time. Let us
hope that educators can teach themselves by this advance and avoid the
lunacies of the Reavis animal school where great efforts were expended
teaching the squirrel to swim and the tortoise to fly. Let us honor each
subgroup of our society for the talents it possesses differentially (as we
now do in athletics), and use the talents of each for a better life for all.
Despite these caveats, numerous studies across a diverse spectrum of human
activities (including psychiatric, musical, visuospatial, auditory, motor, emotional,
and linguistic) suggest that finely shaded but significant sexual dimorphism characterizes cortical organization in Homo sapiens. In particular, males appear to be
subtly biased toward specialization in the right hemisphere. As discussed above,
manipulation of auditory space (i.e., composition of music) and mental rotation of
visual figures may be manifestations of similar cognitive processes in different
modalities. In other words, males seem to be good at “getting around,” i.e., reading
maps, tracing mazes, and mentally manipulating spatial arrangements in visual
and auditory modes. Although a review of the controversy surrounding mathematical abilities (Bleier, 1984; Gowan, 1984) is beyond the scope of this paper, it should
be noted that better performance of males on math tests may be due in part t o the
applicability of visuospatial processing to geometrical tasks. Females, on the other
hand, are subtly biased in certain left-hemisphere (verbal, motor) and right-hemisphere (emotional) skills. Furthermore, females are particularly good at decoding
and production of verbal and nonverbal communications (Hanske-Petitpierre and
Chen, 1985).
These differences between the sexes are small, real, and fascinating. Delineation
of the cultural vs. genetic components that contribute to these differences is beyond
the scope of the current biological sciences (but see Geschwind and Galaburda,
1985a-c, 1987). Furthermore, tests that purport to demonstrate higher “intelligence” of one sex over the other (Gowan, 1984)reveal more about the composition of
the test and biases of their designers than they do about sex and intelligence. One
could design a test to produce whatever results one desired.
Evolutionary scenarios
As discussed in this paper, a recent review of studies on handedness in nonhuman
primates (MacNeilage et al., 1986)suggests that nonhuman primates are lateralized
for differential visual processing in the right hemisphere (left-hand bug snatching)
and fine somatic sensorimotor control in the left hemisphere (right-hand use for
more skilled manipulations). This dichotomy is in keeping with the finding that
split-brain rhesus monkeys show right-hemisphere superiority for another skill that
requires visual processing-differentiating photographs of monkeys’ faces (Hamilton
and Vermiere, 1985). Other studies of the same genus (Macaca) report left-hemisphere dominance for processing species-specificvocalizations (Petersen et al., 1978;
Heffner and Heffner, 1984). Thus, at least one genus of Old World monkey exhibits
left-hemisphere dominance for communication and fine motor skills and right-hemisphere dominance for visual processing. This implies that the neurological substrate
for the basic verbaUvisua1 dichotomy that characterizes Homo sapiens may indeed
have been present during early anthropoid evolution (MacNeilage et al., 1987; Falk,
1980a; Steklis, 1985).
The hominid brain has nearly quadrupled during the last 4 million years (Falk,
1985, 19871, and anthropologists enjoy speculating about hypothetical “prime movers” such as warfare, language, tool production, and hunting that may have been
responsible for this increase. Prime-mover theories are fun but impossible to test. It
is also noteworthy that these theories have usually been biased in favor of males
(see Falk, 1980b, for a review).
Presumably, neurological lateralization similar to that seen in extant Macaca was
refined and elaborated during human evolution in association with the emergence
of language and right-handedness. However, efforts to establish scenarios that specify the exact human behaviors selected upon are as speculative as those listed above.
Two interesting scenarios have recently been suggested: one that emphasizes selection for left-hemisphere skills (Calvin, 1983) and another that emphasizes abilities
associated with the right hemisphere (Flor-Henry, 1980).
Calvin (1983) suggests that brains became bigger because of selection for precise
throwing in conjunction with action-at-a distance predation. In this scenario, increased numbers of timing neurons were selected for and Calvin postulates that
eventually the resulting enlarged left-hemisphere timing circuitry was secondarily
used for language abilities (1983132-133): “The brain may have begun precisely
uncocking the elbow while hammering nuts in the tropics. . . . In basketball to
tennis, this mosaic brain expresses its ancient pleasure in precisely timing a sequence. Transcending its origins, ow brain can now create novel sequences using
grammar and music.” Calvin’s emphasis on sequential timing is intriguing, but the
relatively late emergence of language is inconsistent with recently discovered lefthemisphere dominance for processing vocal communications in monkeys.
Flor-Henry (1980), on the other hand, suggests that lateralization in Homo sapiens
may be viewed as a manifestation of a general rule that emerges from observations
of animals as diverse as rats and birds (Glick, 1985). In rodents, the direction of
circling behavior is contralateral to the side containing higher levels of dopamine
and is associated with fighting and sexual display (Glick et al., 1977).Left-lateralized
control of male bird song is associated with territoriality and mate attraction (Nottebohm, 1977). In keeping with Webster (1977), Flor-Henry suggests that neural
asymmetry increases the efficiency of spatial analysis involved in mate attraction,
and “thus it would follow that in those species where the male actively seeks the
female, the former would exhibit a greater degree of lateralization than the latter”
Were there more specific adaptive results of the right hemisphere’s visuospatial
skills that, according to Flor-Henry’s model, were pivotal for the evolution of asymmetrical cortical organization in humans? Or, put another way, what good is it for
males to be able to perform better than females at mental rotations such as those
presented in Figures 1-4? When asked this question, a colleague suggested that
selection has operated to produce good practitioners of origami. When that suggestion was rejected, he proposed that such visualization skills might have been useful
in the production of multifaceted stone tools. Selection for tool producing is a
classical prime-mover theory and an interesting idea, but one that places too much
responsibility for brain evolution on one human activity.
Field effects
What alternative can be offered to the above scenarios? Several authors have
proposed that testosterone is a primary factor that determines sexual dimorphism
and cerebral lateralization in intrauterine life (Flor-Henry, 1983; Greschwind and
Behan, 1982; Gowan, 1984).If so, rather than being the result of selection for certain
skills associated with specific sexes or hemispheres, cerebral lateralization might
simply be a serendipitous by-product of the intrauterine hormonal processes that
cause gender differentiation. Furthermore, evidence reviewed above hints that such
“priming” may effect the organization of entire hemispheres rather than discrete
areas such as hand representations or visuospatial association areas. (For example,
see Binnie-Dawson and Cheung, 1982, for a discussion of feminized males with
“reversed” spatialherbal cognitive skills.)
Earlier, I proposed a field effect model as a possible explanation for the relationship
between left hemisphere dominance for language and for right-handedness in Homo
sapiens (Falk, 1980a). According to this model (Fig. 5), left-hemisphere dominance
[vol. 30, 1987
Fig. 5. Illustration of the field effect discussed in text. Reproduced from Falk (1980a)and modified after
Penfield and Rasmussen (1950).During human evolution, selection for increasingly complex communication systems correlated with increased asymmetry in the neurological substrates underlying symbolic
vocal and manual output. Left-hemisphere dominance spread to include association areas influencing
adjacent hand regions as bipedalism was achieved.
was initially confined to association areas influencing vocal apparatus-an idea that
finds recent support from comparative neurological and psychophysical evidence
(Steklis, 1985; Falk et al., 1987). Eventually, the area of cortex selected in the left
hemisphere in conjunction with vocal communication ke., cortex with properties
that facilitate “dominance” for speech) widened to include nearby association areas
influencing hand representation, as hands were freed during the achievement of
bipedalism. In this context, it is interesting to note the existence of a right-hand
bias for gesturing during speech in Homo sapiens (Kimura and Harshman, 1984).
The finding that right-handed individuals with left-handedrelatives are biased more
than other right-handers toward use of the right hemisphere for certain tasks such
as recognizing faces or unifying figures (Glass et al., 1984) suggests that lefthandedness may result from an increased “dominant” field in the right hemisphere.
That is, dominance of the right hemisphere extends to include hand representation
in left-handers, but not in their right-handed relatives, who nevertheless exhibit
right-hemisphere dominance for certain other tasks.
It has been proposed above that skills in mental rotation of three-dimensional
figures and composition of music may both be manifestations of the right hemisphere’s “priming” for manipulation of spatial relationships. It would be interesting
to determine if individuals gifted at composing music are also particularly skilled at
mental visual imagery. If so, this phenomenon would perhaps be explained by
intrauterine hormonal influences on a field that includes the entire right hemisphere.
This review has attempted to ferret out some understanding of cortical lateralization and its evolution in Homo sapiens by examining an often-conflictingliterature
spanning the topics of handedness, verballvisual skills, psychiatry, and musical
abilities. The little black box of brain lateralization has an extremely complex and
frequently controversial surface. This is especially true concerning the topic of
sexual dimorphism in cognitive processing. It may well be that prenatal hormonal
priming leads to sexual dimorphism in cerebral lateralization and, further, that the
resulting lateralization is serendipitously responsible for the occasional birth of
geniuses who are compelled to create beautiful symphonies, or write exquisite
poetry. . . . Perhaps it’s not such a black box after all?
I thank Roland Guay for providing Figures 14;Harry Potter and Criss Helmkamp
for helpful banter; and Bill Kisinger and Frank Stubbs for taking time to discuss
music with me. This research was supported by Public Health Service grant 1ROl
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