Language and the Primate Brain
Martin I. Sereno
Cognitive Science Department, UCSD
[Diagrams for the following paper have been omitted
here. Explanations of the diagrams, however, follow the
bibliography. Hard copies, which include the diagrams,
can be obtained from: crl@amos.ucsd.edu. Comments that
pertain to the content of this paper should be directed
to the author at: sereno@cogsci.ucsd.edu.]
LANGUAGE AND THE PRIMATE BRAIN
Martin I. Sereno
Cognitive Science D-015
University of California, San Diego
La Jolla, CA 92093
Abstract
Psychologists, neuropsychologists, and primate neurobiolo-
gists have studied human language comprehension and its
relation to the primate brain in almost complete isolation
from each other. Recent developments provide grounds for
a new attempt at drawing some preliminary connections
across the levels of organization spanned by these fields.
New data on the large number of modality-specific areas in
the post-central cortex of several non-human primates, and
recent anatomical and functional studies of the human
brain suggest that very little of the cortex consists of
poly-modal 'association' areas. These observations are
used to reinterpret psychological and neuropsychological
data on language comprehension in normal and brain-damaged
humans. I argue that language comprehension in sighted
people might best be thought of as a kind of code-directed
scene comprehension that draws heavily upon specifically
visual, and probably largely prelinguistic processing con-
straints. The key processes of word-recognition and the
assembly of visual word meaning patterns into interacting
chains, however, may be mediated in part by species-
specific activity patterns in secondary auditory cortex
similar to those generated by uninterpreted speech-sound
sequences.
One obvious reason to study non-human primate brains is
that they resemble the human primate brain in many ways. Yet
humans exhibit behaviors--especially the comprehension of
linguistic discourse--that are qualitatively very different
from behaviors of primates and other animals. Because of
this, some have concluded that animal brains may be poor
models for the human brain. There are presently quite sub-
stantial rifts between psychological, neuropsychological,
and neurobiological approaches to language. Recent develop-
ments in studying human and animal brains, however, provide
a strong impetus to re-open discourse among these discip-
lines.
The neocortex of all mammals is now known to consist
primarily of a mosaic of visual, auditory, somatosensory,
motor, and limbic areas. Primitive mammals have a small
number of areas in each of these modalities, while car-
nivores and primates have many. In monkeys, for example, a
mosaic of 25 visual areas occupies more than half of the
entire neocortex (Merzenich and Kaas, 1980; Kaas, 1987;
Sereno, 1988; Felleman and Van Essen, 1990; Sereno and All-
man, 1990). The traditional site for higher-level
functions--"polymodal association cortex"--has been reduced
to a few diminutive strips in between large expanses of uni-
modal visual, auditory, and somatosensory areas. The poten-
tial significance of this reparcellation of cortex for the
study of language and the brain has hardly been explored.
The aim of this paper is to re-introduce a thoroughly com-
parative perspective into the evolutionary acquisition of
the capacity for language, but one that does not back away
from the obvious cognitive differences between humans and
other animals. The anatomical and physiological organiza-
tion of cortical areas in primates, including recent work on
human cortex, is reviewed first. The implications of this
work for theories of human language comprehension are then
explored.
Cortical Sensory Areas in Primates
Definition of a Visual Area. Cortical sensory areas are
best defined by multiple converging criteria (Van Essen,
1985; Sereno and Allman, 1990). I begin here with visual
areas, since they constitute the largest of the primary sub-
divisions of the cortex. Criteria for the definition of a
visual area presently include architectonic features (e.g.,
degree of myelination, cell size, cell morphology, and cell
packing density in cortical layers, histochemical features),
connection patterns (e.g., input and output areas, laminar
origins and targets of connections), visuotopic organization
(e.g., mirror-image or non-mirror-image map of hemifield,
bounding areas, pattern of map discontinuities, degree of
retinotopy), and physiological properties (e.g., excitatory
receptive field size, direction selectivity, attention-
related modulation). Areas differ in the degree to which
these criteria have been explored. V1 (primary visual cor-
tex) and MT (middle temporal area) are distinct, well-
studied areas in primates that are convergently identified
by many of these criteria. Other areas--e.g., in inferotem-
poral cortex--are less well studied. There is no evidence to
suggest that they are any less distinct.
Visual Areas in Prosimians and Monkeys. The first primates
were probably nocturnal, judging from the large size of
their orbits (Szalay and Delson, 1979). The primates living
today most closely related to these early primates are also
nocturnal or crepuscular. The bush baby or galago, the only
prosimian primate studied in detail (Allman and McGuinness,
1983; Sereno et al., unpublished studies), has on the order
of 16 distinct visual areas. Almost all visual areas in
galagos exhibit a substantial degree of retinotopic organi-
zation, including areas in the inferotemporal cortex. In
these studies, the entire extent of visual cortex was
physiologically mapped in detail for the first time. In a
passive animal, visual areas only respond to visual stimuli,
auditory areas only to auditory stimuli, and somatosensory
areas only to somatosensory stimuli. Visual cortical areas
border almost directly upon somatosensory areas (dorsally)
and auditory areas (ventrally). The transitional strip
between, for example, auditory and visual areas (in which
neurons have both a visual and an auditory receptive field)
is less than one millimeter wide.
Monkeys (anthropoids) are thought to have diverged from
the ancestors of galagos at least 40 million years ago
(Szalay and Delson, 1979). All but one of the anthropoids
are diurnal (day-living), suggesting strongly that day-
living habits evolved early in the monkey lineage. The one
nocturnal monkey, the New World owl monkey, lacks a tapetum,
suggesting that its ancestors had diurnal habits. The
organization of visual cortex has been studied in detail in
two different monkeys--the owl monkey and the macaque mon-
key. Figure 1A (hard copy only) shows a flattened summary
map of visual areas in the owl monkey (Allman and Kaas,
1976; Weller and Kaas, 1985; 1987; Sereno and Allman, 1990).
As in galagos, V1 is the largest area, followed by V2.
There appear to be at least three somewhat separate
'streams' of information passing through V1 and V2--the mag-
nocellular, parvocellular interblob, and parvocellular blob
streams (named after their relay structures in the dorsal
lateral geniculate nucleus and area V1)--that remain some-
what separated as one moves on to higher areas (Ungerleider
and Mishkin, 1982; Livingstone and Hubel, 1984; DeYoe and
Van Essen, 1988; Zeki and Shipp, 1988). These pathways pro-
cess different aspects of the visual signal in parallel--
roughly, motion, location, and depth in the magnocellular
pathway, and color, shape, and shading in the parvocellular
pathways. The pathways pass through layer 4B, layer 2-3
interblobs, and layer 2-3 blobs in V1, and the thick
stripes, interstripes, and thin stripes in V2, respectively.
There is a broad subdivision of the more rostral visual
areas into parietal (e.g., TP, ST--receiving primarily mag-
nocellular stream input) and inferotemporal (e.g., ITcd,
ITr-- receiving primarily parvocellular interblob and parvo-
cellular blob input). Retinotopy is only lost in the most
anterior members of these two streams. One can define a
hierarchy of visual areas based on the laminar targets of
corticocortical projections; feedforward projections synapse
mainly in layer 4 of the target area, while feedback projec-
tions avoid layer 4 (Rockland and Pandya, 1979; Maunsell and
Van Essen, 1983; Felleman and Van Essen, 1990). The border
between different modalities appears to be as sharp as in
galagos; detailed mapping experiments at the anterior border
of visual cortex reveal that the transitional strip between
visual and somatosensory areas in parietal cortex as well as
the strip between visual and auditory areas in temporal
cortex is less than one millimeter wide (Sereno and Allman,
1990; unpublished studies).
Figure 1B (hard copy only) shows a similar summary map
for the macaque monkey (an Old World monkey) (based on Van
Essen, 1985; Desimone and Ungerleider, 1986; Felleman et
al., 1986; 1987; and personal communication; Colby et al.,
1988). Although many of the areal names are not the same,
and though the relative sizes of similar areas differ, the
overall configuration of the map, the retinotopic and func-
tional organization of individual areas, and the interareal
connection pattern is remarkably similar to our results in
the owl monkey. New and Old World monkeys diverged over 30
million years ago. The main difference between the maps is
the reduced size of the areas between V2 and MT in owl mon-
keys, the shape of V3 (owl monkey DM, its probably homolo-
gue, is much less elongated than the macaque area), and the
somewhat larger size of several inferotemporal areas. Most
of these differences reflect the reduced emphasis on the
center of gaze in the retina of the secondarily nocturnal
owl monkey. An important point is that there does not
appear to be any substantial increase in the area of overlap
between modalities. The zone in the dorsal bank of the
superior temporal sulcus that responds to more than one
modality is several millimeters wide (Seltzer and Pandya,
1989); this is in line with the greater overall area of the
primary cortical areas in the macaque compared to the owl
monkey.
Auditory and Somatosensory Areas in Monkeys. Auditory and
somatosensory areas have been studied in parallel with
visual areas. The main differences are the basis for topog-
raphy (tonotopy and somatotopy vs. retinotopy), the one-
dimensional nature of tonotopy (in contrast to two-
dimensional retinotopy and somatotopy), the smaller overall
size of auditory and somatosensory cortex, and the greater
diversity of types of information collected by somatosensory
receptor types (light touch, pain and temperature, muscle
length changes, force on tendons, joint position). In both
New and Old World monkeys, there are about 9 auditory corti-
cal areas (Merzenich and Brugge, 1973; Pandya and Yeterian,
1985) and about 9 somatosensory cortical areas (Merzenich et
al., 1978; Burton, 1986; Cusick et al, 1989). As in visual
cortex, one can define a hierarchy of areas based on the
laminar targets of between-area projections, and, as in
vision, there is a successive loss of receptotopy as one
progresses to higher levels in the two systems. Most of the
somatosensory maps are based on responses to cutaneous
stimulation (it is difficult to stimulate muscle and tendon
receptors without also stimulating the skin).
These maps (and more fragmentary data from other
species) suggest that the parcellation of most of the cortex
has not changed radically during the evolution of the pri-
mate order (Sereno and Allman, 1990). Notably, there does
not seem to be any significant increase in the areas where
several modalities overlap; rather, modality-specific areas
have increased in size, and quite moderately in number; the
number of cortical areas has probably not changed in New and
Old World monkeys, which have evolved independently for over
30 million years.
Visual Areas in Apes and Humans. The organization of the
cortex in a variety of mammals including humans was studied
extensively by Brodmann and others at the beginning of the
century using stains for cell bodies and myelin (Brodmann,
1909). Since then, anatomical and physiological studies
have revised many of Brodmann's conclusions with respect to
non-human primate brains (e.g., Brodmann's area 18 in Old
World monkeys is twice as wide as it should have been;
Brodmann's area 19 actually contains many distinct cortical
areas). But it is only very recently that human cortex has
been approached from a modern perspective. Preliminary
results suggest that human visual cortical areas are organ-
ized quite similarly to those of other primates.
The human visual area whose borders are best known is
V1--by far the most distinct visual area on architectonic
grounds. Fixed- tissue injections of membrane-intercalating
dyes suggest that local circuit connections within, and long
range connections between, human areas V1 and V2 are very
similar to those of other primates (Burkhalter and Bernardo,
1989). There is a densely myelinated, ellipsoidal area in a
dorsolateral occipital sulcus that may correspond to human
visual area MT, an area found in all primates (Sereno et
al., 1988; Sereno and Allman, 1990) (see Figure 2). Studies
using PET to monitor blood flow and a stimulus designed to
selectively activate MT (based on animal studies) have
uncovered an active locus near the densely myelinated region
(Miezin et al., 1987).
Now clearly, there is a great deal of 'additional'
non-primary cortex in humans. Despite the fact that mon-
keys, apes and humans all have about the same number of
cells in the retina, the dorsal lateral geniculate nucleus,
and in V1 (Frahm et al., 1984; Tolhurst and Ling, 1988), V1
comes to occupy a smaller and smaller proportion of the
total neocortex--about 10-12% or the neocortex in monkeys,
about 6% of the neocortex in apes, but only about 2.5% of
the total neocortex in humans. The preliminary studies
cited above suggest a new answer to the problem of this
'extra' cortex in humans--it may be occupied mostly by
larger versions of areas already familiar from work in mon-
keys (as opposed, for example, to an evolutionarily unpre-
cedented 'language organ'). V2 in humans, for example, is
much wider than would be expected when normalized with
respect to the area of V1. Similarly, there is much more
area between V1 and the putative human MT than would be
expected (this region is mostly occupied by area V4 in Old
World monkeys). Finally, the area of the putative human MT
is about 3 to 4 times as big as would be predicted on a
macaque model. If the other 25 or so extrastriate areas in
human visual cortex increased in size (relative to V1) as
much as this preliminary data suggests that V2, V4, and MT
have, we could almost completely account for the 'extra'
non-primary cortex in humans relative to monkeys. These
observations, combined with the lack of any trend toward
increased polymodal cortex in neocortical evolution, suggest
a radical revision of current neuropsychological theories of
human cognitive processing.
Language Processing in the Context of the Primate Brain.
Modularity and Levels of Explanation. The question of what
language processing looks like in the brain is a contentious
one, especially given the preliminary state of our current
knowledge in this area. A certain tradition in cognitive
science and neuropsychology seems to have taken as its goal,
the isolation of higher levels of explanation from their
lower level implementation. Such a so-called 'functional'
approach is quite curious from a biological perspective.
Surely, biologists are interested in function (e.g., the
heart serves as a pump for blood). But the goal there is to
try to explain how it is that the structure of the heart
gives rise to its function--not to ignore that structure and
build an independently motivated theory in a different
language (a language of 'heart'?!). The fact that the same
program can run on somewhat differently designed von Neumann
machines (e.g., Fodor and Pylyshyn, 1988) seems an insuffi-
cient reason to abandon a biological and evolutionary
approach to the functional organization of the human brain.
This tendency to ignore the structure of the brain is
quite unfortunate in light of the recent progress made in
primate neurobiology. Most current texts of physiological
psychology, neuropsychology, and cognitive neuroscience
(e.g., Damasio and Geschwind, 1984; Caplan, 1987; Ellis and
Young, 1988) still implicitly employ a model of the organi-
zation and evolution of the cortex that dates to the associ-
ationists of the late nineteenth century. In this way of
thinking, 'primitive' mammals like rats start out with pri-
mary visual, auditory, and somatosensory areas almost touch-
ing. Next up the rung of an essentially pre-evolutionary
scala natura come animals like cats, which have a small
amount of 'uncommitted' space in between. Finally, at the
top, are primates and especially humans, where we find a
great deal of uncommitted 'association' cortex, properly
situated to integrate and associate the modality-specific
information presented to it by visual, auditory and
somatosensory cortices (see e.g., Fodor, 1983; Ellis and
Young, 1988, on the 'semantic system' postulated in most
models of word processing; Damasio, 1989).
Fine-grained mapping experiments in hedgehogs, rodents,
cats, and primates, during the past decade have shown this
picture of the evolution of the cortex to be incorrect.
Cats and primates do have more cortex in between the primary
sensory areas; but that cortex consists not of poly-modal
association areas, but rather larger and more numerous
modality-specific (i.e., visual, auditory, and somatosen-
sory) areas. The studies discussed above provide no indica-
tion that humans are any different in this regard. The prob-
lem is, then, in the spirit of biological studies of func-
tional organization, to try to describe how the basic ana-
tomical modules of primate cortex--namely visual, auditory,
somatosensory, motor, and limbic areas--support a new, pecu-
liarly human function.
Language as Code-directed Scene Perception. Vision is very
important to primates; in fact, over 50% of the cortex in
primates, probably including humans, consists of areas
devoted to specifically visual processing. This is not to
deny that information about an object perceived via another
modality--say the somatosensory system--might be able to
enter visual areas in the form of a visual copy of the soma-
tosensory areas' activity pattern (see e.g., experiments by
Haenny et al. (1988) in macaque visual area V4 using a
somatosensory-visual matching task). But it does suggest
that we carefully distinguish a visual copy of a somatosen-
sory stimulus (in a visual area with a visual map) from a
somatosensory copy of a visual stimulus (in a somatosensory
area with a somatosensory map).
Some linguists have independently suggested that visual
representations may be very important in the semantics of
natural language (Jackendoff, 1983; 1987; Fauconnier, 1985;
Lakoff, 1987; Langacker, 1987). An idea common to several
different approaches is that more concrete visual meanings
may have been extended by analogical processes to deal with
more abstract objects and relations. The present proposal
goes further in suggesting a particularly direct relation-
ship between the mechanisms of scene and discourse
comprehension.
The integration of successive glances in the comprehen-
sion of a visual scene requires a kind of serial assembly
operation similar in some respects to the integration of
word meanings in discourse comprehension. Primates (but
also many other animals) make long series of fixations at
the rate of several new views per second during scene
comprehension. Each fixation brings the retina to a new
part of the visual scene and generates a burst of activity
in V1, which largely replaces the burst caused by the previ-
ous fixation. Higher visual areas with less precise retino-
topy somehow integrate information from these disconnected
activity sequences to generate an internal representation of
the location and identity of the relevant objects in the
current scene (e.g., predators, food items, particular con-
specifics, escape routes, suitable sleeping trees, etc.)
that can serve as a basis for action. Many aspects of this
process are redolent of linguistic integration--e.g., the
underspecified, context-free information in an isolated
glance is sharpened and focused by context (cf. polysemy);
information from temporally distant glances must be tied
together (cf. anaphora). None of this implies that scene
representations (or their presumed linguistic fellows) need
look anything like pictures; the patterns in question would
be distributed across many areas, some of which show little
retinotopy.
One main difference between scene and discourse
comprehension is, of course, that scene comprehension is
tied closely to the current scene. Discourse comprehension
might best be thought of as a kind of fictive visual scene
comprehension directed, in the case of spoken language
comprehension, by sequences of phoneme representations in
secondary auditory cortex. The advantage of linguistic
discourse comprehension is that we are no longer tied to the
current scene. However, once the appropriate visual word
meaning patterns have been called up and bound together, the
nature and interactions of the composite pattern may be con-
ditioned mainly by the prelinguistic rules of interaction of
scene representations in primate visual areas networks. In
this sense, a large part of what has been called linguistic
syntax and semantics might not be modular with respect to
the neurobiology of vision.
There is in fact substantial evidence that visual areas
in humans are involved in specifically linguistic functions.
There is a kind of aphasia confusingly called 'transcortical
sensory' aphasia (i.e., 'across-from-the-language-cortex'
aphasia!) that is generated by a lesion in left human
inferotemporal cortex (Rubens and Kertesz, 1983). Many of
these lesions are so posterior and ventral that they are
associated with overt visual field defects. Transcortical
sensory aphasics have poor, "Wernicke's-like" comprehension,
yet paradoxically (at least in the context of traditional
models of language comprehension), can repeat words effort-
lessly. Far from being 'across from the language cortex',
the visual areas in posterior inferotemporal cortex damaged
in these patients may be the primary site of semantic pro-
cessing in sighted humans. Transcortical sensory aphasics
recover more quickly than patients with more dorsal lesions;
this may only be an indication that the functions performed
by visual cortex in language comprehension are less
lateralized than those performed by auditory cortex. This
is consistent with what we know about primate visual areas;
permanent deficits in visual pattern recognition in monkeys
require bilateral inferotemporal cortex lesions (Gross,
1973). There is no need to assume that all the cortical
areas involved in language comprehension are equally
lateralized; for example, the functions performed by the
superior temporal gyrus (see below) may be more lateralized
than the functions performed by the inferotemporal cortex.
Psycholinguistic experiments using pictures inserted
into sentences and picture-word priming (Potter et al, 1986;
Vanderwart, 1984) suggest that it is surprisingly easy for
visually represented concepts to be integrated into ongoing
linguistic discourse comprehension. This may be another
indicator of the closeness of visual category representa-
tions to linguistic meanings.
Some PET Experiments. Recently, it was suggested on the
basis of PET experiments that semantic processing may be
localized instead in the frontal lobe, just in front of
"Broca's area" (Petersen et al., 1988; Posner et al., 1988).
In the key experiment, subjects performed two tasks--1)
repeating visually presented nouns, and 2) generating "uses"
(related verbs) upon viewing an otherwise comparable series
nouns. Upon subtracting these two conditions, an activated
locus was uncovered in frontal cortex, just anterior to the
representation of face, tongue, and throat muscles in pri-
mary motor cortex. Given the ease with which preparation
for movement elicits strong activation in premotor areas
(see e.g., Roland et al., 1980), however, it seems likely
that the activity uncovered in this experiment actually
represents the different motor programming demands of the
two tasks. In the first case, a motor pattern is called up
directly via overlearned connections between visual word
shape and articulatory movements. In the second case, by
contrast, the subject must make a new motor plan to say a
word that is different from that which was viewed. In fact,
the subject must also suppress an output that would normally
be generated by looking at the first word (in the context of
reading words aloud). Frontal cortex lesions in monkeys and
man are known to especially impair the ability to make
delayed responses. Given that posterior inferotemporal cor-
tex has rarely if ever been selectively activated in a blood
flow experiment, and that the PET technique has limited
resolution, the activation underlying semantic processing
may not yet have been seen. A posterior locus for semantics
is more in line with the observation made long ago (and
hardly overturned by more recent studies) that patients with
large posterior lesions are generally much more impaired in
extracting meaning from linguistic discourse--and surely
seem to have a much more severe derangement of thought
processes--than patients with large anterior lesions.
What's in Wernicke's Area? Wernicke's area has occupied
several different gyri over the years. Sometimes it is
placed on the angular gyrus; sometimes it sits more anteri-
orly on the superior temporal gyrus; and often it sneaks
across the superior temporal sulcus (the boundary between
auditory cortical areas dorsally and visual cortical areas
ventrally in primates) to sit partly in inferotemporal cor-
tex. The left-right asymmetry originally demonstrated by
Geschwind and Levitsky (1968) was in yet a different place-
-on the planum temporale (not even clearly visible in a
lateral view). Several architectonic studies (Braak, 1978;
Galaburda and Sanides, 1980) have identified a distinct area
that shows a considerable left-right asymmetry (Braak's tem-
poral magnopyramidal zone; Galaburda and Sanides' area Tpt)
confined entirely to the posterior part of the lateral supe-
rior temporal gyrus. By comparison with other primates,
this area is very likely to be a unimodal, secondary or ter-
tiary auditory cortical area. Merzenich and Brugge (1973)
recorded diffuse auditory responses from a geographically
similar area in macaques.
If Wernicke's area proper (e.g., of Braak) is in fact a
secondary or tertiary auditory area, we are left with some-
thing of a conundrum. Why should a lesion in an auditory
area cause deficits in the assembly of the meaningful units
of language? The deficits exhibited by many patients with a
lesion in this area seem to extend beyond mere problems with
auditory representations of words--their thoughts seem
disarranged; often they are unable to manipulate even words
with concrete visual meanings. The traditional conclusion
has thus been that Wernicke's area must be an evolutionarily
new 'language organ' not tied to one modality. A new
interpretation more in line with the animal literature, is
that the internal representations of speech sound sequences
that a primate neurobiologist would expect to find in
Wernicke's area proper must have some other function besides
merely serving as internal copies of the speech stream;
these uninterpreted speech sound representations must also
be involved in word recognition and assembly of (primarily
visual) meanings into coherent discourse structures. By
this account, what distinguishes humans is the ability to
use a sequence of symbol patterns from another modality to
cause the assembly of meaning patterns in tertiary visual
cortex. But the product of that assembly may be very simi-
lar to patterns assembled from direct visual inputs arriving
via V1 during scene comprehension. The implication is that
the trick of language was not to have invented the basic
meaningful units but to have found a way of making
standardized connections between them (see Sereno, 1986;
1990a; 1990b, for an extended discussion).
In monkeys, the superior temporal sulcus forms, as
noted, the border between auditory and visual cortices.
Since clinically defined Wernicke's-like aphasics often have
lesions that extend into the inferotemporal region on the
middle and inferior temporal gyri, a typical 'Wernicke's
aphasia' may require damage to both the auditory cortex
meaning assemblers and the visual cortex meanings they
assemble.
New Routes Between Modalities. In monkeys, one pathway
responsible for cross-modal matching performance has been
well-defined. Performance on somatosensory-visual matching
tasks is catastrophically impaired by lesions to the basola-
teral amygdala (Murray and Mishkin, 1985). This part of the
amygdala receives projections from secondary and tertiary
visual, somatosensory, and auditory areas, and projects back
to them. There is also a small polymodal strip on part of
the upper bank of the superior temporal sulcus (e.g.,
Seltzer and Pandya, 1989). But this strip cannot by itself
support cross-modal matching in monkeys.
The situation in humans must be somewhat different, at
least with regard to the relative importance of the amygdala
in one particular kind of cross-modal mapping that charac-
terizes human language--the mapping between speech sounds
and visual word meanings. The patient H.M. who had his
amygdala removed bilaterally is quite unimpaired in recog-
nizing visual objects named for him (or in naming visual
objects himself). This suggests that humans must have a
more robust connection between areas on either side of the
superior temporal sulcus than monkeys do. Cross-modal
matching experiments of the kind that amygdala-lesioned mon-
keys fail to perform have not yet been tried with H.M., and
so the cross-modal pathway through the amygdala could very
well still be important for some tasks in humans.
Conclusion
Language is recently derived; based on the evidence of stone
tools and other more spectacular artifacts like cave paint-
ings, it seems likely that peculiarly human cognition and
presumably language use originated rather suddenly less than
50,000 to 100,000 years ago. In view of our knowledge of the
strong similarities between the brains of various non-human
primates, it seems unlikely that the cortex could have been
completely reorganized in so short a time. Surely, there is
no positive evidence for such a major reorganization.
Recent evidence instead suggests that human and non-human
primate brains are organized quite similarly. We need more
attempts to explain the large qualitative differences
between animal cognition and human language-based cognition
as the result of relatively minor modifications and re-use
of pre-existing primate neural circuitry (cf. Bates et al.,
1989).
This paper suggests that it might be profitable to view
language comprehension in sighted people as a kind of code-
directed scene comprehension taking place primarily in uni-
modal visual areas in posterior inferotemporal cortex. A
second suggestion is that internal representation of speech
sound chains in secondary auditory cortical areas
(Wernicke's area proper) may have other functions besides
merely serving as internal copies of the speech code chain;
they may be intimately involved in word recognition and the
binding together of visual cortex meaning patterns. Code-
directed pattern binding is clearly a specifically human
faculty; but many of the constraints on the resulting
bound-together patterns may reflect prelinguistic (non-
modular) constraints on interactions between activity pat-
terns in tertiary visual areas. Studies of the connections
of superior temporal sulcus region in humans--just now
becoming possible--may throw more light on the presently
obscure neural substrate of language and human thought.
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Captions for Figures in hard copy
Figure 1. Cortical visual areas in the owl monkey (A)
and the macaque monkey (B). A cut was made in V1 medially to
allow the cortex to lie flat. The insets illustrate the
location these areas in occipital, parietal, and temporal
cortex (after Sereno and Allman, 1990). All areas shown are
visual except for area PM (owl monkey) and area STP
(macaque), which border on somatosensory and auditory
cortices (not shown).
Figure 2. Cortical visual areas in the human (prelim-
inary). A left occipital lobe (reversed here to aid com-
parison with previous figures) was physically flattened,
sectioned, and stained for myelin. The exposed crowns of
the gyri are colored black. A cut was made in V1 medially
to allow the cortex to lie flat. The insets illustrate the
location these areas in the intact brain (after Sereno and
Allman, 1990). Note that the scale is now in centimeters.
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