Distributed Hierarchical Processing in the Primate Cerebral Cortex

TL;DR: A summary of the layout of cortical areas associated with vision and with other modalities, a computerized database for storing and representing large amounts of information on connectivity patterns, and the application of these data to the analysis of hierarchical organization of the cerebral cortex are reported on.

Abstract: In recent years, many new cortical areas have been identified in the macaque monkey. The number of identified connections between areas has increased even more dramatically. We report here on (1) a summary of the layout of cortical areas associated with vision and with other modalities, (2) a computerized database for storing and representing large amounts of information on connectivity patterns, and (3) the application of these data to the analysis of hierarchical organization of the cerebral cortex. Our analysis concentrates on the visual system, which includes 25 neocortical areas that are predominantly or exclusively visual in function, plus an additional 7 areas that we regard as visual-association areas on the basis of their extensive visual inputs. A total of 305 connections among these 32 visual and visual-association areas have been reported. This represents 31% of the possible number of pathways if each area were connected with all others. The actual degree of connectivity is likely to be closer to 40%. The great majority of pathways involve reciprocal connections between areas. There are also extensive connections with cortical areas outside the visual system proper, including the somatosensory cortex, as well as neocortical, transitional, and archicortical regions in the temporal and frontal lobes. In the somatosensory/motor system, there are 62 identified pathways linking 13 cortical areas, suggesting an overall connectivity of about 40%. Based on the laminar patterns of connections between areas, we propose a hierarchy of visual areas and of somatosensory/motor areas that is more comprehensive than those suggested in other recent studies. The current version of the visual hierarchy includes 10 levels of cortical processing. Altogether, it contains 14 levels if one includes the retina and lateral geniculate nucleus at the bottom as well as the entorhinal cortex and hippocampus at the top. Within this hierarchy, there are multiple, intertwined processing streams, which, at a low level, are related to the compartmental organization of areas V1 and V2 and, at a high level, are related to the distinction between processing centers in the temporal and parietal lobes. However, there are some pathways and relationships (about 10% of the total) whose descriptions do not fit cleanly into this hierarchical scheme for one reason or another. In most instances, though, it is unclear whether these represent genuine exceptions to a strict hierarchy rather than inaccuracies or uncertainities in the reported assignment.

Summary

A Cortical Map

• The authors primary format for illustrating the location of different visual areas involves the use of 2-D cortical maps that are generated from contours of layer 4 in a series of regularly spaced histological sections (Van Essen and Zeki, 1978; Van Essen and Maunsell, 1980) .
• That map was not especially accurate, however, because of the large and somewhat nonuniform spacing between sections, and no scale was provided.
• In addition to the obvious cut that surrounds area VI (the elliptical region on the left), there are 2 smaller discontinuities, one along the ventrolateral side of the frontal lobe (upper right), and the other at the temporal pole (lower right).
• The remainder of the perimeter of the map represents intrinsic borders between the cortex and various noncortical structures (e.g., the dentate gyrus, amygdalar nuclei, and corpus callosum).

Visual Areas

• Altogether, there are 32 separate neocortical areas that are implicated in visual processing, based on the occurrence of visually responsive neurons and/or the presence of major inputs from known visual areas.
• The authors have drawn a distinction between 25 areas that appear to be predominantly or exclusively visual and another 7 neocortical areas that are less intimately linked to vision and will be considered visual-association areas.
• The criteria used in identifying these areas are discussed in detail below.
• A key that links these abbreviations to the standard text citations is given in the table notes.
• In other cases, the alternative scheme is even more fine grained (e.g., POa-i and POa-e vs. LIP).

Surface Area

• Measurements of the surface area of different regions of the cortical map (Table 2 ) provide useful information about the absolute and relative amounts of cortical machinery devoted to different types of processing.
• Besides the neocortex, there are 245 mm 2 of the hippocampus proper (fields CA1 and CA3, the subiculum and the prosubiculum), 120 mm 2 of paleocortex (pyriform and periamygdaloid cortex), and 270 mm 2 of transitional cortex [entorhinal cortex (ER), periallocortex, parasubiculum, presubiculum, and prostriate cortex].
• There are also inaccuracies in their transposition of areal boundaries defined in other studies onto the particular hemisphere used for this map (see above).
• These are hard to quantify, but they probably reflect errors of 50% or more for some areas.
• Areas with sharply defined borders such as VI and MT show roughly 2-fold individual variability in surface area (Van Essen et al., 1981 ,1984) , and it seems likely that this range will be applicable to most, if not all, cortical areas.

Connectivity

• Nearly all of the areas included in this scheme can be distinguished on the basis of their overall pattern of connectivity, and for many, this is the primary basis for identification.
• The authors have included entries for both coarser and finer subdivisions when appropriate in the table.
• Many areas, particularly the recently defined ones, have yet to be studied in detail; hence, their description of the connectional pattern is surely far from complete.
• Each row shows whether the area listed on the left sends outputs to the areas listed along the top.

Specific Visual Areas

• In order to put the current map into perspective, it is useful to comment on the layout of specific visual areas, with emphasis on recently identified areas and areas for which uncertainties in identification persist.
• These are surrounded anteriorly by a collection of smaller areas, 3 of which have been mapped in some detail (MT, V3, and VP), and the remainder of which are less well characterized (V3A, V4t, and VOT).
• This region includes 3 areas (PO, PIP, and DP) situated posteriorly, 5 areas (7a, LIP, VIP, MIP, and MDP) situated more anteriorly and arranged in a lateral-to-medial swath that adjoins the somatosensory cortex, and 2 areas (MSTd and MST1) within the dorsal part of the superior temporal sulcus (STS).
• Overall, it remains unclear whether this heavily myelinated strip should be considered part of VIP or LIP or as a distinct area unto itself.
• Based on the heterogeneous pattern of connectivity with parietal and temporal areas, there are probably distinct subdivisions within area 46 (Goldman-Rakic, 1988; Barbas and Pandya, 1989; Cavada and Goldman-Rakic, 1989b; Seltzer and Pandya, 1989a) , but a coherent scheme for subdividing it has yet to emerge.

Reciprocity and Distributed Connectivity

• This tabulation also provides a useful framework for discussing other important principles concerning the numbers and patterns of connections among different areas.
• The degree to which this relationship holds is reflected in the symmetry of Table 3 about the diagonal axis (shaded boxes).
• A lower bound on the overall degree of connectivity can be set from the overall number of 305 identified pathways linking 32 visually related neocortical areas.
• If each area has an average of 27 connections, as found for well-studied areas, the connectivity level would exceed 40% of the theoretical limit (432/992).
• The fraction of pathways that are "robust," in the sense of showing heavy labeling when analyzed with conventional tracers, may be only 30%-50% of the total number of identified connections.

Hierarchical Relationships in the Visual Cortex

• The possibility that the visual cortex might operate by a strictly serial processing scheme can be ruled out just from knowing the multiplicity of connections per area and the near ubiquity of reciprocal connections.
• One hypothesis is that cortical areas are hierarchically organized in some very well-defined sense, with each area occupying a specific position in relationship to all other areas, but with more than 1 area allowed to occupy a given hierarchical level.
• Others are less well defined, and there may be basic uncertainties as to who ranks above whom in various interactions.
• It is worth noting in general terms that information flow in a hierarchical system (1) can go in both directions (upwards and downwards), (2) can skip over intermediate levels to go directly from a low to a high level, and (3) can travel in parallel through multiple, functionally distinct channels.
• The number of identified pathways for which useful laminar information is available has more than tripled in the past 5 years.

Criteria

• The authors revised criteria for identifying hierarchical relationships are illustrated schematically in Figure 3 .
• The different patterns are arranged to show the laminar distributions of cells of origin and axonal terminations that the authors consider to be indicative of ascending (A, upper row), lateral (L, central row), and descending (D, bottom row) pathways.
• In one pattern (F), terminations are densest in layer 4, though they may also be prominent in layer 3 and other layers, as well.
• Occasionally, patterns are encountered that involve primarily superficial layers (e.g., layers 1 and 2 in the projection from V4 to VI; predominantly layer 3 in the projection from AITd to FEF).
• Such B-F combinations invalidate one of the initial assumptions about feedforward pathways, but they do not necessarily invalidate the notion of hierarchical organization.

A Database for Anatyxtng Hierarchical Relationships

• The authors goal in this section is to apply the scheme illustrated in Figure 3 as objectively and rigorously as possible to the analysis of hierarchical relationships in the visual cortex, while taking into account the uncertainties and qualifications that are associated with some of the experimental data.
• The ease and reliability with which such data could be related to their partitioning scheme varied widely and depended to a large extent on how much detailed information was given about the pathways under consideration.
• As with the areal assignments, the determination of laminar patterns associated with each pathway was often difficult, depending on the nature and extent of published information available.
• For this reason, their computerized database included, in addition to the relevant publications, a listing of their specific page numbers and figure numbers that are particularly informative about laminar patterns.
• With respect to determining hierarchical relationships, however, the presence of a mixed result (S/B or I/B) in a single pathway does not represent an inherent conflict, because a bilaminar pattern is consistent with all possibilities, ascending, descending, or lateral.

Levels crossed

• This table shows connections among visual conical areas listed in Table 1 .
• The authors suspect that this bias for C/F and C/M patterns is not a coincidence and that it may be important for understanding the significance of mixed or intermediate termination patterns (see below).
• To avoid logical inconsistencies, each area must be placed above all areas from which it receives ascending connections and/or sends descending connections.
• Areas MIP and MDP have been placed at the fifth hierarchical level, even though the connections known for both areas are ambiguous (bilaminar retrograde labeling) and would technically be consistent with placement at any lower level.
• It is notable that all 3 of these inconsistencies involve relationships that were already questionable from an earlier stage of the analysis.

Significance of Hierarchical Irregularities

• Their presence raises the issue of whether the cortex is inherently only a' 'quasi-hierarchical" structure that contains a significant number (perhaps 10%) of bona fide irregularities and exceptions to any set of criteria that can be devised.
• The anatomical data on which their analysis is based are often fuzzy and replete with uncertainties of one or another type.
• Thus, it would have defied the odds if every single one of the 305 pathways had fit precisely into an orderly hierarchy.
• If one suspects that the underlying biology is extremely orderly, one would predia that the apparent discrepancies listed in Table 6 will largely disappear upon careful reexamination, thereby improving the overall fit to the hierarchy.
• The authors found that resolution limits made it impractical to flag these special cases by distinctive colors in the figure, but they can nonetheless be readily tracked down with reference to Tables 3 and 5 .

Number of Levels Traversed

• While some pathways link areas at the same or immediately adjacent hierarchical levels, the majority of pathways traverse more than 1 level.
• Figure 6 shows that there is an interesting difference along these lines.
• Nonetheless, it is apparent that the more specific unilaminar projections, on average, traverse more hierarchical levels than do the bilaminar projections: 2.68 levels for I patterns, 2.76 levels for S patterns, and 1.71 levels for B patterns, excluding all of the lateral pathways.
• A related set of questions arises when considering connectivity patterns and hierarchical relationships among adjacent visual areas, that is, ones that share a common boundary in the intact cortex.
• There are numerous examples of neighboring areas separated by 2 or 3 levels (e.g., V2/V4, VP/V4, and PIP/VIP).

Hierarchical Relationships in Other Regions and in Other Species

• The visual cortex has extensive connections with a variety of nonvisual areas, both cortical and subcortical.
• This allows us to link the visual hierarchy with a somatosensory hierarchy that will be discussed below.
• The analysis is less straightforward for entorhinal cortex, a complex of several small areas (Amaral et al., 1987) all having a transitional architecture that lacks the cell-dense layer 4 characteristic of most neocortical areas.
• The architecture and connectivity of the hippocampal complex is radically different from the neocortical areas discussed above (cf. Swanson et al., 1987) .
• Hence, it should not be surprising that a modified set of criteria would be necessary for making any hierarchical assignments.

Somatosensory and Motor Cortex

• The notion that forward and feedback connections can be used to delineate hierarchical relationships is nearly as old for the somatosensory cortex as it is for the visual cortex.
• As in the visual system, reciprocity of connections between areas appears to be a general rule, but there are several possible exceptions, including pathways from 7b to 1, SII to 4, and granular insular (Ig) to dysgranular insular (Id) that apparently lack connections in the reverse direction.
• By this point, it should not be surprising to find that there are a few irregularities that must be addressed.
• Figure 7 shows the somatosensory-motor hierarchy that results from the systematic application of the pairwise hierarchical assignments contained in Table 8 .
• In brief, this hierarchy starts with areas 3a and 3b at the bottom and extends in successive stages through areas 1, 2, 5, retroinsular (Ri), SII, 7b, Ig, and Id.

Auditory Cortex

• In the auditory system, Galaburda and Pandya (1983) analyzed connections among 12 cytoarchitectonic areas that they identified within the superior temporal gyrus and supratemporal plane of the lateral sulcus.
• These areas were grouped into 4 rostrocaudally aligned triplets of "root," "core," and "belt" areas.
• With anterograde labeling, they found that the feedbacktype pattern was generally strongest in layer 1, but otherwise conformed to the F, C, and M description that the authors have used.
• They reported that rostral-to-caudal projections tended to be of the descending pattern, and that caudal-to-rostral projections tended to be ascending in some cases but columnar in others.
• One small piece of evidence in further support of an auditory hierarchy comes from a single tracer injection in the postauditory area (Pa), which demonstrated descending projections to Al and ascending connections to a different auditory area (Friedman et al., 1986) .

Other Cortical Regions

• The remaining regions of the neocortex yet to be incorporated into their analysis include much of the frontal lobe (orbitofrontal, lateral prefrontal, dorsal prefrontal, and medial prefrontal), as well as cingulate, retrosplenial, and insular regions.
• There is not a great deal of information about the specific laminar patterns for pathways to and from precisely defined areas in these regions.
• One striking finding is that large paired injections centered in areas 7a and 46 led to interdigitating columnar patterns of terminations in some regions (e.g., cingulate cortex and orbitofrontal cortex), even though the same injections contributed to complementary (ascending and descending) patterns in other regions, such as the STS (Selemon and Goldman-Rakic, 1988) .
• This trend may instead simply represent the greater uncertainty and ambiguity about many of the high-level assignments.
• Each of these regions receives direct inputs from the olfactory bulb that, as already noted, terminate preferentially in superficial layers of cortex (Turner et al., 1978) .

Subcortical Projections

• All visual areas that have been appropriately examined have extensive connections with a variety of subcortical structures.
• Indeed, it would not be surprising if the sheer number of corticosubcortical pathways exceeds that of the corticocortical pathways analyzed in this article.
• The projections from cortex to different pulvinar subdivisions originate predominantly from layer 5, and the reciprocal projections from the pulvinar terminate most heavily in layers 4 and 3 of the extrastriate cortex (Lund et al., 1975; Benevento and Rezak, 1976; Ogren and Hendrickson, 1977) .
• Interestingly, however, the pulvinar projection to VI terminates mainly in superficial layers, even though the reciprocal pathway originates from layer 5, just as for extrastriate areas (Rezak and Benevento, 1979) .
• This is consistent with the amygdala being at a well-defined level just below TF and TH.

Other Species

• There is also a considerable body of information about laminar connectivity patterns in other species.
• The authors have already discussed the need in the primate cortex to treat bilaminar retrograde labeling patterns as completely ambiguous with regard to hierarchical assignments.
• By applying their revised criteria to connectivity patterns described in Symonds and Rosenquist (1984a,b) for visual cortex in the cat, the authors have constructed an orderly hierarchy that involves 62 connections among 16 areas organized into 8 levels (Fig. 8 ).
• They are followed by 2 levels, each containing numerous entries (areas PLLS, PMLS, SVA, and ALG at the fourth level and areas AMLS, ALLS, DLS, VLS, 21a, and 20b at the fifth level).
• Much remains to be done in order to resolve the modest number of apparent discrepancies and to ascertain just how generally this hypothesis applies across systems and species.

Intertwined Processing Streams in the Visual Cortex

• The notion of parallel processing streams in the visual system has received considerable attention during the past decade and is the topic of several recent reviews (e.g., Livingstone and Hubel, 1987b; Maunsell and Newsome, 1987; DeYoe and Van Essen, 1988; Lennie et al., 1990) .
• The central issue the authors wish to address in the remainder of this article is the relationship between the low-level M and P streams that originate in the retina and the high-level streams associated with areas in the temporal and parietal lobes (Ungerleider and Mishkin, 1982; Desimone and Ungerleider, 1989) .
• A second form of cross talk occurs in the ascending connections between areas.
• Likewise, MT projects heavily to the parietal cortex (directly to VIP and indirectly via MSTd and MST1), but it also has indirect connections with inferotemporal areas via FST and V4.

Single Neuron Connectivity

• Thus far, the authors have concentrated on the connections of entire areas or of layers and compartments within areas, without addressing the issue of heterogeneity among the individual neurons that make up a layer or an area.
• Most of what the authors know about this issue comes from a relatively small number of double-retrograde-labeling studies in cats and monkeys, in which tracers are injected into topographically corresponding portions of 2 different areas (cf. Kennedy and Bullier, 1985; Bullier and Kennedy, 1987) .
• In general, diis approach reveals a significant number of doubly labeled cells, signifying that individual neurons can indeed have collaterals projecting to more than 1 area.
• The average number of target areas per cortically projecting neuron could plausibly be well under or well over 2.
• In the cat, there is evidence that this number is greater for descending pathways than for ascending pathways, and that some cells can even contribute simultaneously to both directions, by making both an ascending and a descending connection (Bullier et al., 1984; Bullier and Kennedy, 1987) .

Functional Implications

• The authors have concentrated in this study primarily on an anatomical analysis that suggests 5 key principles of primate cortical organization: (1) a large number of visual areas, (2) highly distributed connectivity among areas, (3) reciprocity of connections, (4) hierarchical organization, and (5) distinct, yet intertwined, processing streams.
• The authors now comment on what these principles might signify for understanding the functions of different visual areas.

Distributed Hierarchical Processing

• The hierarchical scheme for visual cortex that the authors have presented is grounded explicitly on anatomical criteria.
• That situation is now changing, and a few of the more notable examples are worth explicit mention: (1) Many cells in V2, but not in VI, are responsive to patterns that elicit percepts of subjective contours in human observers (Peterhans and von der Heydt, 1989; von der Heydt and Peterhans, 1989) .
• These and other examples support the notion that higher stages of the cortical hierarchy represent more advanced levels of processing.
• The physiological properties discussed thus far (increases in classical receptive field size and more advanced receptive field selectivities) may largely reflect the contributions of ascending pathways and of circuitry intrinsic to each area.
• The physiological properties of any given cortical neuron will, in general, reflect many descending as well as ascending influences.

Functionality of Processing Streams

• The M stream contains a high incidence of cells selective for direction of motion and for binocular disparity, suggesting that it is heavily involved in the analysis of motion and depth.
• First, consider what sources of information are useful for signaling object motion.
• The effects of selectively lesioning the M and P layers of the LGN on specific behavioral tasks provide support for the notion that M and P channels each contribute to multiple aspects of perception (Schiller and Logothetis, 1990; Schiller et al. 1990; Merigan et al., 1991) .
• In a more general sense, there appears to be a complex, but orderly, relationship between low-level sensory cues (e.g., orientation, velocity, disparity, and spectral composition), high-level aspects of perception (e.g., perception of shape, surface qualities, and spatial relationships), and the processing streams that generate one from the other (DeYoe and Van Essen, 1988) .

Notes

• Two such enamel-painted, plaster-coated, styrofoam models were available, one at 3 times life size and the other at a scale of 9-fold.
• Boundaries of individual cortical areas identified in the studies indicated in the text and in Table 1 were marked onto the brain model, mainly on the basis of the relationship to various geographical landmarks.
• Once the physical model had been marked, the various areal boundaries were transposed to outlines of the sections on which the model was based.
• The next step was to transpose boundaries to sections of the brain from which the cortical map was made.
• The manually generated map, complete with areal boundaries, was optically scanned and used as a template for creating the color map with the CANVAS program on a Macintosh II computer.

Full text

Distributed Hierarchical Processing
in the Primate Cerebral Cortex
Daniel J. Felleman
1
and David C. Van Essen
2
1
Department of Neurobiology and Anatomy,
University of Texas Medical School, Houston, Texas
77030, and
2
Division of Biology, California
Institute of Technology, Pasadena, California 91125
In recent years, many new cortical areas have been
identified in the macaque monkey. The number of iden-
tified connections between areas has increased even
more dramatically. We report here on (1) a summary of
the layout of cortical areas associated with vision and
with other modalities, (2) a computerized database for
storing and representing large amounts of information
on
connectivity patterns,
and
(3) the application of these
data to the analysis of hierarchical organization of the
cerebral cortex. Our analysis concentrates on the visual
system,
which includes 25 neocortical areas that are
predominantly or exclusively visual in function, plus an
additional 7 areas that we regard as visual-association
areas on the basis of their extensive visual inputs. A
total of 305 connections among these 32 visual and
visual-association areas have been reported. This rep-
resents
31 %
of the possible number of pathways if each
area were connected with all others. The actual degree
of connectivity is likely to be closer to 40%. The great
majority of pathways involve reciprocal connections be-
tween areas. There are also extensive connections with
cortical areas outside
the
visual
system proper, including
the somatosensory cortex, as well as neocortical,
tran-
sitional,
and archicortical regions in the temporal and
frontal
lobes.
In the somatosensory/motor
system,
there
are 62 identified pathways linking 13 cortical areas,
suggesting an overall connectivity of about
40%.
Based
on the laminar patterns of connections between areas,
we propose a hierarchy of visual areas and of somato-
sensory/motor areas that is more comprehensive than
those suggested in other recent studies. The current
version of the visual hierarchy includes 10 levels of
cortical processing. Altogether, it contains 14 levels if
one includes the retina and lateral geniculate nucleus
at the bottom as well as the entorhinal cortex and hip-
pocampus at the top. Within this hierarchy, there are
multiple, intertwined processing streams, which, at a
low level, are related to the compartmental organization
of areas VI and V2 and, at a high level, are related to
the distinction between processing centers in the tem-
poral and parietal lobes. However, there are some path-
ways and relationships (about 10% of the total) whose
descriptions do not fit cleanly into this hierarchical
scheme for one reason or another. In most instances,
though,
it is unclear whether these represent genuine
exceptions to a strict hierarchy rather than inaccuracies
or uncertainties in the reported assignment.
During the past decade, there has been an explosion
of information about the organization and connectiv-
ity of sensory and motor areas in the mammalian ce-
rebral cortex. Many laboratories have concentrated
their efforts on the visual cortex of macaque monkeys,
whose superb visual capacities in many ways rival
those of humans. In this article, we survey recent
progress in charting the layout of different cortical
areas in the macaque and in analyzing the hierarchical
relationships among these areas, particularly in the
visual system.
The original notion of hierarchical processing in
the visual cortex
was
put forward by Hubel and Wiesel
(1962,
1965) to account for a progressive increase in
the complexity of physiological receptive field prop-
erties in the cat visual cortex. In particular, they sug-
gested that a serial, feedforward scheme could ac-
count for the generation of simple cells from LGN
inputs, and complex cells, in turn, from simple cells.
Likewise, the properties of hypercomplex cells and
even "higher-order hypercomplex cells" were attrib-
uted to inputs from their immediate predecessors.
However, the pure form of this hypothesis is difficult
to reconcile with the finding of highly reciprocal con-
nectivity and parallel channels discovered in more
recent studies of the visual pathway (cf. Rockland and
Pandya, 1979; Stone et al., 1979; Lennie, 1980; Lennie
et al., 1990; Shapley, 1990). On the other hand, there
is no a priori reason to restrict the notion of hierar-
chical processing to
a
strictly serial sequence. In gen-
eral, any scheme in which there are well-defined lev-
els of processing can be considered hierarchical.
The notion that anatomical criteria could be used
to delineate a hierarchy of cortical areas first received
detailed scrutiny about a decade ago (Rockland and
Pandya, 1979; Friedman, 1983; Maunsell and Van Es-
sen, 1983). Since this hypothesis was last reviewed
systematically (Van Essen, 1985), the number of iden-
tified visual areas and identified connections has in-
creased greatly. In addition, 2 recent studies (Ander-
sen etal., 1990;Boussaoudetal., 1990) have proposed
hierarchical relationships for parietal, temporal, and
frontal areas that are largely, but not completely, con-
sistent with one another and with our previous
schemes. Here, we provide a critical examination of
the degree to which the entire ensemble of available
data fits into an overall hierarchical scheme. We also
review the evidence that the principle of hierarchical
Cerebral Cortex Jan/Feb 1991;1:1—47; 1047-3211/91/»2.00

organization applies to other functional modalities
and to other species besides macaques.
A
related theme in our analysis concerns the nature
of concurrent processing streams in the visual cortex.
These streams are linked at the input side to specific
subcortical inputs from the magnocellular (M) and
parvocellular (P) layers of the LGN (cf. Blasdel and
Lund, 1983; Hubel and Livingstone, 1987) and, at the
output side, to functionally distinct regions of the
parietal and temporal lobes (Ungerleider and Mish-
kin, 1982; Desimone and Ungerleider, 1989). Our
analysis will emphasize that, on the one hand, there
is considerable segregation of information flow
throughout the visual pathway; on the other hand,
there is also substantial intermixing and cross talk
between streams at successive stages of processing.
It is likely that these complexities in the anatomical
circuitry reflect the multiplicity of computational
strategies needed for efficient visual function (DeYoe
and Van Essen, 1988).
Subdivisions and Interconnections of the Visual Cortex
A Cortical Map
Our primary format for illustrating the location of
different visual areas involves the use of 2-D cortical
maps that are generated from contours of layer 4 in a
series of regularly spaced histological sections (Van
Essen and Zeki,
1978;
Van Essen and Maunsell, 1980).
Previous summary maps showing the distribution of
areas (Van Essen and Maunsell,
1983;
Van Essen, 1985)
were based on section drawings from a hemisphere
published by Brodmann (1905). That map was not
especially
accurate,
however, because of the large and
somewhat nonuniform spacing between sections, and
no scale was provided. We have therefore generated
a complete map from a hemisphere used in a previous
study from this laboratory, in which information about
the pattern of interhemispheric connections and about
cortical myeloarchitecture was available for identk
fying certain visual areas (Van Essen et al., 1986).
Figure 1 shows the overall layout of the map, includ-
ing the section contours upon which the map was
based (thin lines; 2-mm spacing between sections),
the location of cortex within sulci (shading), and the
position of the fundus of each sulcus (dashed lines).
As in previous cortical maps, it was necessary to in-
troduce a few cuts, or discontinuities, to prevent se-
rious distortions in the representation, and these are
indicated by heavy solid lines along the perimeter.
In addition to the obvious cut that surrounds area VI
(the elliptical region on the left), there are 2 smaller
discontinuities, one along the ventrolateral side of
the frontal lobe (upper right), and the other at the
temporal pole (lower right). The remainder of the
perimeter of the map represents intrinsic borders be-
tween the cortex and various noncortical structures
(e.g., the dentate gyrus, amygdalar nuclei, and corpus
callosum). This map also differs from its predecessors
in that it contains the entirety of the cerebral cortex,
including archicortical, paleocortical, and transition-
al regions, as well as the standard 6-layered neocortex.
Visual Areas
Our current understanding of the layout of different
visually related areas is indicated by the color-coded
scheme in Figure 2. Altogether, there are 32 separate
neocortical areas that are implicated in visual pro-
cessing, based on the occurrence of visually respon-
sive neurons and/or the presence of major inputs from
known visual areas. Each of these visual areas is shad-
ed with a different color. The overall extent of the
visual cortex corresponds closely to the visually re-
sponsive regions identified in the 2-deoxyglucose
study of Macko and Mishkin (1985). However, not all
of these areas are exclusively visual in function.
Nonvisual contributions include inputs from other
sensory modalities (especially auditory and somato-
sensory), visuomotor activity (i.e., related to eye
movements), and attentional or cognitive influences
(cf. Andersen, 1987; Maunsell and Newsome, 1987;
Goldman-Rakic, 1988; Desimone and Ungerleider,
1989).
We have drawn a distinction between 25 areas
that appear to be predominantly or exclusively visual
and another
7
neocortical areas that are less intimately
linked to vision and will be considered visual-asso-
ciation areas. This is unlikely to reflect a strict di-
chotomy, though, and there may well be a continuum
in the degree to which various areas are selectively
involved in visual processing.
There are
9
visual areas in the occipital lobe, which
are shaded in purple, blue, and reddish hues in Figure
2.
The 10 visual areas of the parietal lobe (1 of which
is associational) are in shades of yellow, orange, or
light brown; the 11 areas of the temporal lobe are in
various shades of green; and the 2 visual-association
areas of the frontal lobe are in dark shades of brown.
The criteria used in identifying these areas are dis-
cussed in detail below.
On the remainder of the cortical
map,
various func-
tional or regional domains are delimited in black and
white by heavy outlines. These include somatosen-
sory, auditory, motor, olfactory, gustatory, subicular,
hippocampal, entorhinal, retrosplenial, and cingulate
regions, plus medial, dorsal, lateral, and orbital regions
of the prefrontal cortex. Most of these regions have
been further subdivided into specific cortical areas,
indicated by fine lines, on the basis of cortical archi-
tecture and/or connectivity. Many of these areas are
denoted by the same type of numbering scheme
promulgated by Brodmann (1905). However, in many
instances, we have used areal identifications from more
recent studies that differ substantially from Brod-
mann's original scheme. (This can be seen by com-
paring Fig. 2 of the present study with Fig. 9 of Van
Essen and Maunsell, 1980).
The demarcation of areal boundaries on the cor-
tical map involved several stages. As noted, a few
visual areas were explicitly identified by architectonic
criteria in the hemisphere from which the map was
made, and the locations of several additional areas
were constrained by the pattern of interhemispheric
connections that had been determined in this hemi-
sphere. For the remaining areas, it was necessary to
transpose boundaries not only from a different brain,
2 Organization of Macaque Visual Cortex • Felleman and Van Essen

9—,
80G-R
1
cm
15
16-
-16
Rgora 1. A 2-0 map
of
cerebral cortex in macaque monkey, prepared by the method of Van Essen and Marred (1980). Rne tofid
Ones
represent the contours of layer
4
from a ssriss of 16 horizontal sections taken at 2-mra interval! through the cortex. Hwien along the margins of the map correspond to the different section tevets indicated
in
the lateral [upper feft) and medial (inter kfi\ views of the hemisphere. St&fog indicates cortex lying within various tufa, an) the fundus
of
each sulcus
is
indicated by nasty
dashed lines.
SoV
foes along the perimeter of the map nlicate regions where artificisl cuts have been made to reduce distortions. Dssted
Snes
along the perimeter represent
the margins of the cortex, where
it
adjoins various noncortxal structures: the corpus calbsum/indoseum gnseum ((op), olfactory tubercle and amygdatar nuda [ritfo), and dentate
gyrus of the htppocampus (Aonomj. the scale on the map has been adjusted to correct
to
the estimated 16% shrinkage that occurs during rctotogkal processing (d. Van Essen
and MaunseB, 1980: Van Essen et aL, 1986). AUT. amsrior mtdde tEmporsI subs; AS, arcuate sukus;
CaS,
csfcarine sutaa; CaS, central sulcus: CiS, cingubte sukuc HF,
hrppocarnpal fissure: IOS, inferior nxtphal sulcus: PS, mtraparietal sukus; LS. lunate sukuc
OTS,
occiuitDieinMal sutas;
POS,
peneOHnapnal sukus: PS, principal sutcuc RF.
rhinsl fissure; SF. syhnan fissure; STS, superior temporal sukus.
Cerebral Cortex Jan/Feb 1991, V 1 N 1 3

MEDIAL PREFRONTAL
1 cm.
Figure 2. Map of cortical areas in the macupja. The brawns of 32 visual areas are inditatad with colors that indicate whether they are in the ocapital lobe [purple, Hue,
and reddish ftues|, parietal lobe \yeSow, ormgt and ligtl brom hues), temporal lobe [great hues], or frontal lobe [trom Aues). The references used in placemen of boundaries
for the different visual areas are fated in Table 1. The scale appfies arty ID the map; the brain drawings are smater by 20% (cf.
fig.
1). The specific studies used in estimating
the border of the various nonvisual areas are as foBowc Somstosensory areas 3a. 3b, 1, 2, 5, 7b,
3L
Ri (retroHisutar), PB (postaudhory),
fy
(msufar granular), and Id (msufar
dytgranularj were based on Jones and Burton (1976), Jones et aL (197B), Robinson end Burton |1980). Friedman
a
a). (1986). Huerta et aL (1987), and Andersen et aL (1990).
Note that, in this scheme, areas 1 and
2
intervene between SI and area 3b. bi other primates, inducting the marmoset and the owl monkey, Sll appears to directly adjoin area
3b,
and it has been suggested diet more derated mapping will reveal the same manuanau in the macaque (Cuai et aL, 1989: Krubitzer and Kaas, 1990). Auditory areas
Al
(primary auditory),
Rl
(rostrotateraf), CM (caudomecfial). tnd L (lateral) were based on Merenieh and Brugge (1973L The postaudhory area (ft) is described as a somatoseraory
area by Robinson and Burton (1980) and as an auditory area by Friedman et at (1986). We have included
it
as pan of the auditory arm in our analysis, but obviously this
issue merits further investigation. Areas of the hippocampal comptai (HC), including the entorhinal conei (ER), areas 35 and 36. presuboifum, prosutriculum, subkulum, and fields
CA1 and CA3, were based on Amaral et aL (1987), Insausi et aL (1987), and Saunters et aL {1988). Olfactory areas, including the pirifarra cortex (P1R) and paianiygdatoid
conn (PAC), were based on Insausti e) aL (1987). Orbhofromal areas 11, 12, and 13. prnsrxortai (Pro), periaUocortei (Pall), lateral prefromal area 45. dorsal preframa) areas
9 and 10, and medial prefmntal areas 14. 25, and 32 were based on Barfaas and Pandys 11989) and fnsaustj et aL (1987). Motor areas
4
(primary motor) and 6 (premotor and
arcuate premnor, or 6s and 6i), supptsmemary motor area ISAM], and medial eye field \MEF, or supplementary eye fields, SEF) were based on Brodmam (1905). Mateffi et al.
(1986), tnsaustj et aL (1987). Schlag and Sd%fley (1987), Hutchins et aL (1988). and Mam et aL (1988). Finally, dngutata and other linti areas 23. 24. 29 (retrosptenial).
30 (PGrn or 7m), and prostrate [PS, divided by an artificial cut into dorsal (d) and ventral (v) sectors] were based on msaustj et al. (1987) and Sarites (1970). A few regions
in the posterior ortutofraraal, lateral prefromal, and anterior sytvian cortices have not been dosety stnfied and are left unspecifiad here.
4 Organization of Macaque Visual Cortex • Felleman and Van Essen

but usually from a diflFerent type of representation as
well, because the best available information on areal
boundaries, in may cases, was on a drawing of
a
brain
or on a series of brain sections cut at a diflFerent angle
than the horizontal plane used for our map.
1
Table
1
provides additional information pertaining
to the identi6cation and characterization of diflFerent
visual areas. The areas are grouped according to their
geographic location in diflFerent lobes (column 1).
Columns 2 and 3 give the acronyms and full-length
names, respectively, that we prefer for each area. Col-
umn 4 provides information about the degree of to-
pographic organization, rated on a scale of 1-4 (see
below). It also identifies the visual-association areas
alluded to above. Column 5 provides a measure of
the confidence with which diflFerent areas have been
identified, as discussed below. Column 6 provides 1
or more references that have been particularly useful
in determining the extent and the boundaries of each
area. These citations do not necessarily reflect either
the most recent study or the original study involved
in its identification. They are designated by abbrevi-
ations based on the first letters of the authors' sur-
names plus the publication
year.
A
key that links these
abbreviations to the standard text citations is given in
the table notes. This format, which we will use in
other tables as well, provides a compact representa-
tion that allows more rapid recognition of specific
references than is attainable with a simple numerical
listing.
In general,
3
methodological approaches have been
most useful in identifying diflFerent visual areas: (1)
Connectivity analysis relies on finding a character-
istic pattern of inputs and outputs for each cortical
area. This approach has proven useful for nearly all
visual areas and is considered in detail below. (2)
Architectonicstelies on a distinctive structure as seen
in Nissl, myelin, or other staining techniques. It offers
a reliable approach for only a minority of the areas
listed in Table 1 and was used to map 3 of the areas
(VI,
V3, and MT) in the particular hemisphere illus-
trated in Figure 2. (3) Topographic organization re-
lies on an orderly mapping of the visual field in each
area, as revealed physiologically or anatomically.
About half of the identified visual areas show a mea-
surable degree of topographic organization. Howev-
er, the precision and orderliness of the visual repre-
sentation varies widely. As indicated in column 4 of
Table 1, we have grouped areas into 4 categories:
extremely precise and regular topography (category
1),
intermediate resolution (category 2), coarse and
irregular (category 3), and finally, little or no dis-
cernible topography (category 4). In addition, some
visual areas (most notably
V3
and VP) contain incom-
plete representations, including only the superior (S)
or inferior (I) contralateral quadrant; nonetheless,
several lines of evidence argue that these areas should
be considered distinct from one another (cf. Burk-
halter et al., 1986). Hence, topographic information,
like architectonics, is a valuable tool, but can be in-
adequate or even misleading when applied in isola-
tion from other approaches.
In addition to these 3 primary methodological ap-
proaches, the identification of some areas has been
facilitated by information about physiological char-
acteristics, as evidenced by distinctive receptive field
properties of neurons, and by examining the behav-
ioral consequences of restricted lesions or focal
electrical stimulation. Ideally, each area should be
independently identifiable using all 5 of the afore-
mentioned approaches. In practice, however, the
identification of most areas is based only on a subset
of these approaches, often just 1 or 2 (cf. Van Essen,
1985).
Different cortical areas vary in the reliability with
which they have been identified and the precision
with which their borders have been mapped, as in-
dicated by the 3 categories of confidence level in
column 5 of Table 1. The first 2 categories include
areas we consider to have been identified with a rea-
sonably high degree of confidence. Category
1
refers
to areas, such as VI and
V2,
whose borders have been
mapped with considerable precision (usually to with-
in 1-2 mm). Category 2 refers to areas, such as V3A
and
V4,
whose identity is widely accepted but whose
borders are known only approximately. Category 3
includes areas whose identification is less secure and
more open to debate. This is the largest of the 3 cat-
egories, and it signifies that the basic task of deter-
mining how the cortex is partitioned into specific
areas is by no means complete.
Most regions of the visual cortex have more than
1 name that is in common use. Table 1 provides a
partial listing of these alternative terminologies. In
dealing with the nomenclature issue, we have drawn
a distinction between (1) names that are simply dif-
ferent descriptors for what is clearly the same under-
lying visual area (e.g., areas 17
vs.
VI, V3vvs. VP, and
MT
vs.
V5;
column 7), and (2) names that reflect sub-
stantially different schemes for partitioning the cortex
(column 9). In some cases, the alternative scheme is
a more coarse partitioning than the one we prefer
(e.g., TEO vs. PITd and PITv). In other cases, the
alternative scheme is even more fine grained (e.g.,
POa-i and POa-e vs. LIP). In still other cases, most
notably in the inferotemporal cortex (IT), the rela-
tionship between different schemes is more complex
and irregular.
Surface Area
Measurements of the surface area of different regions
of the cortical map (Table 2) provide useful infor-
mation about the absolute and relative amounts of
cortical machinery devoted to different types of pro-
cessing. The total extent of the cerebral cortex in this
particular hemisphere, after correcting for shrinkage
during histological processing, is 10,575 mm
2
, of which
9940 mm
2
(94%) is neocortex. Besides the neocortex,
there are 245 mm
2
of the hippocampus proper (fields
CA1
and
CA3,
the subiculum and the prosubiculum),
120 mm
2
of paleocortex (pyriform and periamygda-
loid cortex), and 270 mm
2
of transitional cortex [en-
torhinal cortex (ER), periallocortex, parasubiculum,
presubiculum, and prostriate cortex]. The visual cor-
Cerebral Cortex Jan/Feb
1991,
V 1 N 1 5