Anatomical and physiological asymmetries related to visual areas V3 and VP in macaque extrastriate cortex

ANATOMICAL AND PHYSIOLOGICAL ASYMMETRIES RELATED TO VISUAL AREAS V3 AND VP IN MACAQUE EXTRASTRIATE CORTEX A. BUKKHALTER.* Biology Division

Abstract--This

D.

216-76,

report provides

IO area V2 in extrastriate

J. FELLEMAN, California

to V2, we have obtained

asymmetries

properties

Visual cortex

relating

Extrastriate

in cortico
monkey

address: Department University

-_-

of Neurosurgery,

Medical

Box 8057,

School, St. Louis,

MO

63 I IO, U.S.A. tPresent address: Department iour, :To

SUNY.

Stony

of Neurobiology

Brook,

whom correspondence

NY

11794,

and reprint

ESSEN:

of cortex immediately

anterior

to previous suggestions that

myeloarchitecture,

this conclusion

is based

and single-unit

phys-

about color and motion.

Functional

asymmetries

restricted preferentially to inferior (area ALLS) or superior (areas 21a, 21 b) portions of the contralateral hemifield (Palmer c’t rd., 1978; Tusa and Palmer, 1980; Tusa et al., 198 I). The present report is concerned with a pair of visual areas in the macaque that appear to provide a further exception to this rule. One of these areas, V3, is located in dorsal extrastriate cortex and contains a representation restricted to the inferior contralateral quadrant; the other area, VP, is located in ventral extrastriate cortex and contains a representation of the superior contralateral quadrant. Taken together, the two make up a complete hemifield representation; indeed, until recently they had been regarded as a single area, V3, forming a continuous strip along the anterior margin of V3 (Zeki, 1969; Cragg, 1969). However, we have found numerous anatomical and physiological differences which are so pronounced that in our opinion it is more appropriate to consider them as two separate areas. The evidence bearing on this issue has arisen from several independent studies carried out in this laboratory over the past 6 years (Van Essen et al., 1979, 1982; Newsome ct ~1.. 1980; Burkhalter and Van Essen, 1983, 1986; Felleman and Van Essen, 1983, 1984; Felleman et al., 1984; Van Essen CJIal., 1986). The purpose of the present article is to illustrate and briefly review the major lines of evidence relating to the identification of these areas and to the assessment of their functional asymmetries.

Visual cortex in mammals consists of a large number of distinct visual areas, most of which contain topographically organized representations of the contralateral half of the visual field. In striate cortex (VI), the representation is fine-grained and very precise (Van Essen el al., 1984). At higher stages, topographic organization becomes progressively coarser and appears to be altogether eroded in high level visual areas in the temporal and parietal lobes (Gross et al., 1972; Van Essen and Zeki, 1978; Robinson et a/., 1978). It is often supposed that all topographically organized visual areas must contain a complete representation of the contralateral hemifield. This would ensure that for each area there is coverage of the entire visual field between the two hemispheres, which makes sense if each area contributes to a particular visual function or constellation of functions. Nonetheless, there is no compelling reason why this must invariably be the case. Several of the extrastriate areas that have been mapped physiologically in the cat contain representations that appear to be

Washington

Contrary

VAN

CA 91 125. IJ.S.A.

evidence that this strip of cortex includes two

connections,

Macaque

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organization

monkey.

to the processing of information

cortex

and D. C. Pasadena,

area, VP. The evidence supporting

INTRODUCTION

*Present

NEWSOME?

an overview of the functional

separate areas, V3 and the ventral posterior iological

T.

of Technology.

visual cortex of the macaque

a single area. V3, lies anterior on dorso-ventral

W.

Institute

and BehavU.S.A.

requests should be

addressed. 63

A. BLJRKHALTER CI ul.

64

METHODS

The various anatomical and physiological procedures used in these experiments have been described in detail in other publications from this laboratory. In brief, the anatomical methods included the Gallyas stain for myelin (Gallyas, 1979; Van Essen er al., 1981) the degeneration stain of Wiitanen ( I969), horseradish peroxidase (HRP) histochemistry (Mesulam, 1978), ‘H-proline autoradiography (Cowan et al., 1972), and Nissl staining with cresyl violet or neutral red. Surgical procedures for making lesions and tracer injections and for cutting the corpus callosum are described in Van Essen et al. (198 1; 1986) and Maunsell and Van Essen (1983b). For the analysis and display of anatomical results, two-dimensional maps of various portions of cortex were prepared from contours from histological sections (Van Essen and Maunsell 1980). Physiological recordings for mapping of visual topography were carried out as described in Van Essen et al. (1981). Quantitative analysis of single unit properties was

stimulus carried out using computerized presentation and data analysis procedures (Maunsell and Van Essen, 1983a). Cells were routinely tested for selectivity to stimulus orientation, disparity, direction, speed, and color. Color selectivity was determined by presenting isoluminant narrow band and white stimuli (retinal illuminance, 200 td) on a uniform white background of 50 td.

RESULTS

Overview of visual areas in the macaque

It is useful to show at the outset how the two areas to be discussed in detail, V3 and the ventral posterior area, VP, are situated with respect to other visual areas in the macaque. These relationships can best be assessed by displaying results on two-dimensional, unfolded maps of the hemisphere, thereby circumventing the fact that more than half of visual cortex is buried in one or another of the 7 major sulci of the occipital, temporal, and parietal lobes.

VISUAL AREAS IN THE MACAQUE MOWEY

Fig. I. Visual areas in the macaque monkey, as displayed on lateral and medial views of an intact hemisphere (upper and lower left) and on an unfolded, two-dimensional map of the cortex (right). The two dimensional map was prepared according to the procedure of Van Essen and Maunsell (1980). Abbreuiarions: AIT-anterior inferotemporal area; DPL-dorsal pre-lunate area; LIP-lateral intraparietal area; MST-medial superior temporal area; MT-middle temporal area; PIT-posterior inferotemporal area; PO-parietn-occipital area; P!+prostriate area; STP-superior temporal poiysensory area; TF-area TF of Bonin and Bailey; VA-ventral anterior area; VIP-ventral intraparietal area; VP-ventral posterior area.

4A

48

4co 4w

5 6

Fig. 2. Projections from VI to V2 and V3. (A) Darkfield photomicrograph of a horizontal section through dorsal occipital cortex, including a focal injection of ‘H-proline in VI (left) near the inferior vertical meridian representation. Labeled axons traverse a short distance of white matter (WM) and terminate in two closely-spaced patches in V2 on the posterior bank of the lunate sulcus (right). (B) A section from a more ventral level of the lunate sulcus containing a small patch of label on the anterior bank of the lunate sulcus. This patch can be unambiguously assigned to V3 because of its distance from the VI/V2 border and because a lesion along the VI horizontal meridian led to degeneration (not shown) at the fundus of the lunate su1cus, thus demonstrating the topographic reversal expected for the V2 and V3 representations. In both A and B, anterior is to the right, and medial is up. (C) Retrogradely labeled cells in VI following an HRP injection in V3 in a separate experiment. All of the labeled cells in this section, and nearly all in VI of this hemisphere, were located in layer 4B, the stria of Gennari.

_ Fig. 3. Myeloarchitecture of V3 and VP. (A) Myelin-stained horizontal section through the annectant gyrus, with the lunate sulcus below and the parieto-occipital sulcus above. A heavily myelinated strip of cortex is present on both banks of the annectant gyrus; white bands indicate the uncertainty limits for each of the myeloarchitecture borders. Asterisks represent the extent of callosal-recipient cortex present on an adjacent degeneration-stained section, which serves to define the anterior border of V3 (see text). (B) A section through the occipito-temporal sulcus (OTS) from the same hemisphere, stained and photographed in identical fashion as the section in (A). The antero-medial bank of the OTS is above, the postero-lateral bank below. Asterisks mark the extent of callosal-recipient cortex seen in the adjacent degeneration-stained section. VP extends approximately to the middle of this callosal-recipient strip and is 2-4 mm wide (Newsome er al., 1980, and unpublished evidence). VP is slightly more tightly myelinated than V2 in this section, but we did not find this to be consistent enough to permit reliable identification of VP.

66

Visual

cortex

functional

Fig~~re 1 shows a summary diagram of 20 known or suspected cortical areas that are involved in visual processing as judged by physiological and/or anatomical evidence. These 20 areas. whose full names are given in the figure legend, are distinguished from one another on the basis of their architecture, connections. topographic organization and/or the functional properties of their constituent neurons. The dilferent areas vary in terms of the confidence with which they have been identified and the precision with which they have been mapped. Also, not all of these areas are exclusively visual in function. In brief, there are 8 topographically organized visual areas which have been identified with reasonable confidence (VI, V2, V3, V3A, V4. VP, MT, and PO), plus an additional visual region, VA/V4. which may either be a distinct area or a ventral extension of V4. There are at least 3 areas (MST, PIT, and AIT). and possibly a fourth (DPL) which are visually responsive but which lack obvious topographic organization. Finally, there are seven areas (TF, PS, VIP, LIP, STP, 7a, and 8) which are known either to be visually responsive or to receive major projections from other visual areas, but which may be involved in auditory, somatosensory, motor, or other types of processing as well. The available evidence bearing on the existence and function of these areas has recently been reviewed (Van Essen, 1985). The numerous visual areas illustrated in Fig. I are richly interconnected by many direct corticocortical pathways and also by linkages involving the pulvinar, superior colliculus and other subcortical nuclei. The cortico-cortical pathways follow several organizational principles that provide a basis for suggesting an orderly anatomical hierarchy of visual areas (Maunsell and Van Essen, 1983b; Van Essen and Maunsell, 1983). In particular, these pathways tend to occur as reciprocal pairs having a basic asymmetry in laminar organization, as previously noted for a number of corticocortical pathways by Tigges et al. (1973, 1981). Wong-Riley (1978) and Rockland and Pandya ( 1979). On these grounds the information flow can be construed as ascending (forward-going) in one direction (e.g. from Vl to V2) and descending (feedback) in the other (e.g. from V2 to VI). In the current version of the cortical hierarchy, based on more than 50 robust and reasonably consistent projections, there are 7 hierarchical levels, beginning with VI at the lowest and including several temporal, parietal.

asymmetries

in macaque

and frontal areas at the highest Essen, 1985).

07

two levels (Van

Many of the basic issues and problems involved in identifying extrastriate visual areas are brought into focus by considering the organization of cortex in the long strip immcdiately anterior to V2. As noted in the introduction, this strip was originally thought to bc a single area, V3. In terms of topographic organization, it is clear from both physiological mapping studies and pathway tracing after focal lesions or tracer injections that this strip indeed contains a single representation of the contralateral hemifield (see below). The topographic organization is a mirror image of that in V2, with the representation of the inferior contralateral quadrant adjoining that of dorsal V2 in the lunate and parieto-occipital sulci, and the representation of the superior contralateral quadrant adjoining that of ventral V2 in the inferior occipital sulcus, occipito--temporal gyrus, and occipito-temporal sulcus. Within this strip, however, there are many distinct dorso-ventral asymmetries that have recently been discovered. The differences between dorsal and ventral regions are sufficiently robust and consistent that in our opinion these should be considered as separate visual areas. each having an incomplete visual field representation. We have maintained the name V3 for the dorsal region and have adopted the name VP. the ventral posterior area, for the ventral region based on a likely homology with the correspondingly named area in the owl monkey (Newsome and Allman, 1980). For clarity, we will use this terminology in the course of reviewing the evidence for the existence of these areas. In the Discussion we will return to the issue of terminology and will suggest alternative names (V3d/V3v or VDjVV) which would be more appropriate if a different set of hotnologies obtained. (I) Asymmetric projections of‘ VI. The original studies of Zeki (1969) and Cragg (I 969) provided convincing examples of lesions near the representation of the inferior vertical meridian in dorsal VI that led to degeneration in 2 separate foci in the lunate suicus, clearly corrcsponding to areas V2 and V3. Their cases illustrating projections from the superior field representation in ventral VI were not as convincing, however. This is because the lesions either were close to the horizontal meridian. so

6X

A. BURKHALTEK

that they produced only a single strip of degenrather than widely separate foci, or they were so close to the Vl/V2 border that some inadvertent involvement of V2 might have occurred. We have reassessed this issue by making various combinations of lesions and tracer injections in relevant parts of Vl. V3, and VP. Figure 2(A)-(C) shows results from two such experiments. In the first, an ‘H-proline injection was made in dorsal Vl near the inferior vertical meridian representation. Figure 2(A) shows a darkfield photomicrograph of a section that includes the injection site in Vl (left), with label transported across a short stretch of white matter (WM) to V2 on the posterior bank of the lunate sulcus (right). The projection to V2 was distinctly patchy, but the center-to-center spacing between patches was small (1.5-2-O mm). The total extent of label in this region (3-4 mm) was well within the confines of V2, whose anterior border was revealed by the degeneration resulting from a lesion in Vl that included the horizontal meridian (not shown). A separate focus of transported label [Fig. 2(B)] was found on the anterior bank of the lunate sulcus anterior to the degeneration at the V2 horizontal meridian and in the location expected for V3 (Zeki, 1969; Van Essen and Zeki, 1978). This result, along with similar results from lesions and/or proline injections in 8 other hemispheres, confirms the existence of a projection from dorsal VI to V3 (Van Essen et al., 1979, 1986; see also Van Essen, 1985). In three separate experiments, one of which is illustrated in Fig. 2(C), we made HRP injections into V3 and found that the projection from Vl to V3 originates almost exclusively from cells in layer 4B (Felleman and Van Essen, 1984). Interestingly, this is the same layer of VI that projects heavily to MT (Lund et al., 1976; Maunsell and Van Essen, 1983b). It contrasts with the projection to V2, which includes a major contribution from layers 2 and 3 as well as layer 4B (Lund ef ul., 1981; Livingstone and Hubel, 1984; Van Essen et al., 1986). A reciprocal pathway from V3 to VI was demonstrated by making proline injections in V3. This pathway is of the feedback pattern, insofar as it terminates outside the granular layer (4C), mainly in layers 6, 4B and 1 of VI (Felleman and Van Essen, 1984). A consistently different outcome came from experiments designed to trace the connections of ventral VI. In seven cases of lesions and/or tracer injections in the upper field representation eration

1'1(11.

in VI, the expected connections with V2 and MT were confirmed, but there was no detectable projection to VP, i.e. to cortex immediateiy anterior to ventral V2 (Van Essen et (II.. 1979. 1986; see also Van Essen, 1985). A similar conclusion resulted from three cases of combined HRP and proline injections into VP. These resulted in massive retrograde and anterograde labeling in ventral V2. but no detectable retrograde or anterograde label in the topographically corresponding portion of VI (Burkhalter and Van Essen, 1983). We conclude from these experiments that there is a major and consistent asymmetry of VI projections, such that dorsal Vl is reciprocally interconnected with V3 but ventral Vl has no corresponding relationship with VP. (2) Myeloarchitecture. Another important asymmetry concerns the appearance of V3 and VP in myelin-stained sections, as is illustrated in Fig. 3. On the left [Fig. 3(A)] is a photomicrograph of cortex in the vicinity of the annectant gyrus, an internal bulge between the lunate and parieto-occipital sulci in dorsal extrastriate cortex. On both sides of the annectant gyrus there is a zone of cortex heavily myelinated in layers 4, 5 and 6 over an extent of approximately 3 mm. The uncertainty limits for the transition from moderate to dense myelination are indicated by solid white lines in the subjacent white matter. The relationship of this heavily myelinated region to area V3 was determined by examining callosal connections in the same hemisphere, as assessed from the pattern of degeneration following transection of the corpus callosum. Callosal inputs are known to be concentrated along the anterior margin of V3 (Zeki and Sandeman, 1976; Van Essen and Zeki, 1978; see below), and their location is indicated by asterisks in Fig. 3(A). The fact that the heavily myelinated zone is of the approinto the V3 priate width and extends callosal-recipient strip provides strong support that it is a valid architectonic marker for V3. In ventral extrastriate cortex, the region corresponding to VP consistently lacked heavy myelination, as illustrated by the region of the occipito-temporal sulcus shown in Fig. 3(B). The location of the anterior margin of VP was determined from the pattern of callosal inputs (Newsome et al., 1980; see below) and is indicated by asterisks on both anterior and posterior banks of the sulcus. Both VP and ventral V2 are lightly to moderately myelinated, and we found no consistent architectonic transition akin

Visual cortex functional

FIN. 4. The full extent of V3 in one hemisphere from myeloarchitectonic dimensional denote

map of extrastriate

the uncertainty

Individual

criteria limits

as judged

and displayed

on a two-

occipital cortex. Thin lines for

the V3

sections, which were examined

boundaries

on

at 0.25 0.5 mm

intervals through the region of interest. The heavy solid line is drawn

approximately

boundary

estimates.

micrographs “A”

The

through regions

the midpoints from

which

of these

the photo-

of the preceding figure were taken are noted by

and “R”.

The fundus of each major sulcus is marked

by a dashed line. ilhhrc~rirrtion.~:

IOS-inferior

occipital

sulcus: LS-lunate

sulcus: POS-parieto-occipital

sulcus;

IPS--lntra-parietal

sulcus: OTS-occipito-temporal

sulcus;

STS--superior

temporal

sulcus.

to that just illustrated for V3. A similar asymmetry in myeloarchitecture of V3 vs VP was found in seven other hemispheres in which part or all of these areas could be independently identified by the pattern of callosal inputs or the projections from VI or V2 (Van Essen et ~1.. 1986). The full extent of V3 is indicated in the two-dimensional map of extrastriate occipital cortex shown in Fig. 4. This map is from the same hemisphere illustrated in Fig. 3(A) and (B). and the regions from which the photomicrographs were taken are indicated by A and B. respectively. V3 is more than 2cm long on the map. but only l-3 mm wide. In this particular case there is a bifurcation near the medial end. with one heavily myelinated strip extending to the medial wail and another running a short distance towards the intraparietal sulcus. The

asymmetries

in macaque

6’)

other 6 cases that have been fully mapped arc roughly similar insofar as V3 is elongated along a roughly medio-lateral axis. but there arc significant individual differences. For example. none of the other maps of V3 have a pronounced bifurcation, and 5 of the 7 cases show one or more gaps in the heavily myelinatcd strip. It remains to be determined whether these gaps represent true discontinuities in V3 or local irregularities in myeloarchitecture. In any event. the most important point in the present context is the absence of a comparable strip of heavy myelination in ventral extrastriate cortex. Thus, V3 and VP show consistent differences in their myeloarchitecture. (3) Visual topogrirphy ~itid callo.vtrl itiprfs. There are several distinct sources of information about the topographic organization of V3 and VP. The most direct, of course, is from standard physiological mapping experiments, which have been carried out for most of VP (Ncwsomc r’f u/., 1980: Gattass (‘1 N/., 1981) and for parts of V3 as well (Zeki and Sandcman. 1976; Van Essen and Zeki, 1978; Gattass it r/l., 1981). A second approach relies on the information from focal lesions or tracer injections in VI or V? (Zeki, 1969, 197 I ; Crag, 1969; Van Essen (31(I/.. 1979. 1982) in conjunction with available knowledge of visual topography in these prcceding areas (Daniel and Whitteridgc, 1961; Van Essen et nl., 1984; Gattass cutIJ/., I98 I ). The third source comes from the pattern of callosal inputs, which. as already mentioned. tcrminatc preferentially in regions of vertical meridian representation. The degree to which topography and callosal inputs are correlated varies considerably in different areas, being fairly sharp l’or V2, fairly crude for V4 and MT. and intermediate for V3 and VP (Van Esscn and %cki. 1978; Van Essen (‘I rrl., I98 I, 1982: Newsomc C/ nl., 1980). Figure 5 summarizes these points by showing a two-dimensional map of the occipital lobe in a hemisphere for which: (i) callosal inputs were mapped by staining for degeneration following transection of the splenium of the corpus callosum (stippling); (ii) the borders of V3 Lvcrc identified on the basis of myeloarchitecturc (set Fig. 4): and (iii) a composite map of topographic organization in V3 and VP was cmstrutted on the basis of the aforementioned mapping and pathway-tracing experiments carried out on a number of other hcmisphcrcs. There are several important points encoded in this figure. First. callosal inputs are concen-

A. BURKHALTER et cd.

Fig. 5. Topographic organization of V3 and VP and its relationship to callosal inputs, as displayed on the same two-dimensional map of extrastriate occipital cortex illustrated in the preceding figure. Stippled areas represent callosal-recipient cortex. The borders of V3 were determined from myelin-stained sections in the same hemisphere. The borders of VP, and the topographic organization of both areas are based on physiological mapping and pathway tracing experiments in other hemispheres. Solid circles represent the vertical meridian, and open squares represent the horizontal meridian.

trated along the anterior borders of both V3 and VP. However, the pattern of inputs is somewhat asymmetric: ventrally, there is a smooth, continuous strip which has been shown to run fairly evenly along the edge of VP (Newsome ef al., 1980), whereas dorsally the inputs are more irregular, and the association with the architectonically determined borders of V3 is less precise. In other hemispheres the irregularities in dorsal callosal-recipient cortex can be even more marked (Van Essen and Zeki, 1978; Van Essen et al., 1982). Second, both V3 and VP appear to contain full representations of their respective contralateral quadrants (inferior for V3, superior for VP). This conclusion is based

mainly on the finding that tracer injections 111~lli parts of dorsal VI (foveal, paracentral. and peripheral) consistently project to V3; the same is true for projections of ventral V2 to VP (Van Essen et al., 1979, 1982, 1985; Newsome CI tri., 1980; see also Van Essen, 1985). Third, the representations in V3 and VP are approximately congruent with those in the corresponding subdivisions of V2, insofar as there is usually no dramatic misalignment along their common borders. There is a substantial degree of local disorder in the topographic organization of V2, V3, and VP, though. This, coupled with the marked individual variability in the exact shape of V3 and in the uncertainty concerning the full extent of VP, makes it premature to conclude whether the relative emphasis on central vs peripheral vision is the same in all three areas. (4) Comparisons with the owl monkejl. Although the asymmetric pattern of callosal inputs to V3 and VP does not in itself constitute strong evidence for a distinction between the two areas, it does provide for an important comparison with the owl monkey. Newsome and Allman (1980) showed that the pattern of callosal inputs to ventral occipital cortex in the owl monkey is essentially the same as in what we subsequently found for the macaque, with a narrow strip running parallel to and slightly anterior to ventral V2. Based on that evidence and on physiological recordings indicating that this strip contains a visual representation restricted mainly to the superior contralateral quadrant, they identified it as the ventral posterior area, VP. Our choice of the same name for the corresponding region in the macaque reflects a presumed homology that is supported by the similarities in location, topographic organization, and callosal inputs (see Discussion). (5) Physiological asymmetries. If there were no functional correlates of the aforementioned anatomical asymmetries, the advisability of drawing a major distinction between V3 and VP in the macaque would be seriously questionable. To address this issue we have made single unit recordings from both areas, with the aims of surveying the selectivity for a variety of stimulus parameters and of using essentially identical recording techniques for the two areas (Burkhalter and Van Essen, 1986: Fellernan et al., 1984). In particular, we tested individual cells for their selectivity to stimulus color, orientation, disparity, direction, and speed. By using computer-controlled visual stimulation and response analysis, it was possible to obtain

Visual cortex

functional

asymmetries

in macaque

71

DIRECTION

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600

640

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Fig. 6. Examples of single-unit recordings from V3 and VP. Panels on left show polar plots of responses to stimuli moving in different directions (at 30” increments) for a strongly direction-selective cell in V3 and a relatively nonselective cell in VP. Panels on right show the responses of the same pair of cells to a series of monochromatic stimuli (460-660 nm) and to white light (W). All stimuli were adjusted to be equal in luminance. The V3 cell lacks substantial color selectivity and responds reasonably well to white. The VP cell is strongly color selective and is inhibited by white. For both direction and color series, each cell was tested 3 or 5 times for each stimulus value, with stimuli presented in pseudo-random order. Standard errors for each response are indicated by error bars. The index for direction selectivity was calculated according to the formula DI = I -(null/best), where “best” is the response above background for the most effective stimulus and “null” is the response above background to the stimulus 180“ opposite the best. The index for color selectivity was calculated according to the formula CI = I - (worst/best), where “best” is response above background to the most effective monochromatic stimulus and “worst” is response above background to the least effective monochromatic stimulus.

bias-free measures of each type of selectivity. The total number of cells studies was 147 in V3 and 96 in VP. Some recordings were lost before all test series were completed, so the total number of successful tests is not the same for each parameter. We will concentrate here on the results for direction selectivity and color selectivity, as these revealed the most striking differences between areas. Figure 6 illustrates some of the response properties found in two different cells, one in V3 and the other in VP. Each cell was tested for direction selectivity, with responses shown in a polar plot (Fig. 6, left panels), and for selectivity to a series of monochromatic stimuli of equal luminance and to isoluminant white light (Fig. 6, right panels). It is obvious at a glance that the V3 cell is highly direction selective but not strongly color selective, and that the reverse is true for the VP cell. In the overall population for each area there was considerable variability from cell to cell in the degree of selectivity for quantitative,

each parameter,

making it important to have quantitative indices of selectivity. For direction selectivity we used an index that compares the response to the best direction of stimulus movement to that of the opposite (null) direction. The expression for this index, given in the figure legend, ranges from 0 for a completely nonselective cell to I for a cell that gives no abovebackground response to the null direction; cells inhibited in the null direction have an index greater than I (Baker et al., 1981; Maunsell and Van Essen, 1983a). The direction indices (DI) for the cells illustrated were 0.98 for the V? cell and 0.42 for the VP cell. For color selectivity we calculated a color index (CT), which compares the response to the most t’s the least effective monochromatic stimulus. As with the direction index, the color index ranges from 0 for a completely nonselective cell to I for a cell that is unresponsive at the least effective wavelength, and greater than I for a cell inhibited by the least effective wavelength. The color indices

A. BURKHALTER

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Fig. 7. Histograms of direction indices (left) and color indiecs (right) for the entire populations of cells studiid in V3 (upper panels) and VP (lower pa&s). For each histogram the subset having an index greater than 0.7 is shown in solid.

were 0.33 for the V3 cell and 1.1 for the VP cell in Fig. 6. It should be noted that a color index of 0.3 does not signify a robust selectivity, given the magnitude of the standard errors associated with each wavelength tested. Purely random fluctuations, coupled with typical values of standard errors, would lead to a color index of 0.2X1.3 even for cells completely lacking in genuine color selectivity. A summary comparison of color and direction indices in V3 and VP is shown in Fig. 7. The most important aspect of this comparison in the present context is that the distributions for the two areas are obviously different for both color and direction selectivity. This can be seen by comparing the means and standard errors for each type of index (0.57 + 0.016 in V3 vs 0.74 & 0.03 in VP for color indices; 0.60 f 0.026 in V3 vs 0.39 f 0.028 in VP for direction indices). These differences are statistically highly significant (P < 0.0005, Student’s r-test). It can also be seen by comparing the percentage of cells above a criterion level for each index. We used a cutoff value of 0.7, which corresponds to a 3.3-fold difference between maximum and minimum response, combined with a requirement that the difference between maximum and minimum exceed twice the sum of the standard errors. Cells meeting these criteria are indicated

by solid bars to the right of the cutoff. The percentage of color selective cells is 60% in VP vs 21% in V3, and the percentage of direction selective cells is 13% in VP vs 40% in V3. The higher incidence of color selectivity in VP is not attributable to sampling closer to the fovea1 representation, as the average eccentricity for our VP population was actually greater than that of the V3 population. It should be emphasized that the choice of a cutoff value of 0.7 for each index is artificial, in the sense that it does not necessarily signify a distinction between biologic&y natural cell classes. Rather, it reflects our estimat-ion of what constitutes a reasonable degree of selectivity from an information-processing standpoint. Whether or not genuine functional cell classes exist in visual cortex is an important question in itself that is dealt with in greaterdetail elsewhere (Van Essen, 1985). Another possible physiological difference between V3 and VP is in the size of receptive fields. Over the range of common eccentricities represented in the two populations (4-15 deg), V3 receptive fields were 1.25-5.5 deg in size (mean 2.6 deg) whereas VP cells were nearly twice as large on average (range 3.0-8.1 deg, mean 4.6 deg). However, these were hand-plotted receptive fields done by different invesEigators in

Visual

cortex

functional

different monkeys. Moreover, a comparable asymmetry in receptive field size was found in recordings from dorsal vs ventral V2 in the same hemispheres as the V3 and VP recordings. We therefore suspect that this particular asymmetry reflects a systematic difference in the subjective process of how receptive field boundaries are plotted by different investigators, especially since no dorso-ventral asymmetry was found in a recent physiological investigation of V3 (their V3d) and VP (their V3v) (G. Gross, personal communication). No pronounced differences between V3 and VP were found in terms of selectivity for orientation, length, or disparity. Hence, the properties relating to these parameters will not be discussed further. A few of the V3 cells we encountered had multiple, sharply tuned peaks in their orientation or direction tuning curves. These cells may play an important role in a more advanced stage of form or motion analysis than occurs in VI. However, the apparent lack of such cells in VP might simply reflect inadequate sampling, so we do not consider this to be a well documented physiological asymmetry. (6) Asymmetric higher level connections. The consistent asymmetry in connections with VI has already been discussed in detail. We have looked for evidence of additional connectional asymmetries following tracer injections into V3 and VP in separate experiments (Burkhalter and Van Essen, 1983; Fellernan and Van Essen, 1984). Both areas have several linkages in common, including major reciprocal connections with V2, V3A, and MT. One possible asymmetry is that strong connections with area TF in the temporal lobe were found with two out of three VP injections, whereas this pathway was absent after two V3 injections and very sparse in a third. This is not simply a consequence of Table

I. Comnarisons

asymmetries

TF having connections predominantly with areas concerned with upper-field representations, as there is a major projection to TF from the portion of V4 representing inferior fields (Fellernan and Van Essen, 1983). There were additional asymmetries in the projections of V3 and VP to the parietal lobe, but these may be related to the topographic organization of target areas that have not been adequately characterized. Along the same lines, there is a projection from V3 to V4 and from VP to a region designated as VA/V4 in Fig. 1. Whether this constitutes a genuine connectional asymmetry depends on the ultimate status of the target region VA/V4 which, as the name implies, may either be a part of a large area V4 having a complete hemifield representation or a separate area (VA) restricted to an upper-field-only representation (see Van Essen, 1985).

DISCUSSION

The distinction between V-3 rend VP Table 1 provides a brief comparison of the major characteristics of V3 and VP as described in the Results. The first two on the list, dorsal vs ventral location and inferior vs superior field representation, are included as reminders of the basic differences in geography and topography. The remaining six comparisons constitute the evidence that these are distinct visual areas. In order to evaluate this evidence, it is important to know how reliable these differences arc and how they compare to differences that are found among other extrastriate areas in the macaque. Connections. In apparent contradiction to the present observations, several previous reports have suggested or implied that ventral VI does project to what we are calling VP and/or that between

V3 and VP VP (V3V) Ventral superior

V3 (V3d) Dorsal inferior

Location reoresentation Connections (I) With VI (2) Callosal inputs Architecture (3) Myelin stain Physiology (4) Color selectivity (CI 2 0.7) (5) Direction selectivity (DI >_ 0.7) Homologies (6) Comparison with owl

in macaque

monkey

Reciprocal Irregular

None Regular

Heavy

Medium

21%

64 %

40%

I 3“Aa

No corresponding lower-field-onlv area

Probable with VP

homology

74

A. BURKHALTER el al.

dorsal Vl does not always project to V3 (Zeki, 1969; Cragg, 1969; Ungerleider and Mishkin, 1979, 1982; Rockland and Pandya, 1979, 1981; Weller and Kaas, 1983). A detailed critique of these experiments is presented elsewhere (Van Essen, 1985; Van Essen et al., 1986). In brief, some of these experiments do not provide a critical test of the pattern of Vl projections, because the lesion or tracer injection was too close to the horizontal meridian to permit detection of separate foci, because it was too close to the Vl/V2 border to rule out inadvertent involvement of V2, or because the pattern was reconstructed in insufficient detail to ascertain the complete pattern of projections. Once such cases are excluded, we are not aware of any convincing examples of the absence of a Vl projection to V3 or the presence of a Vl projection to VP. It should be emphasized, however, that the important issue in the present context is whether there is a substantial asymmetry, not whether there exist any exceptions whatsoever to the general pattern. For example, if more sensitive tracer techniques were to reveal a weak or occasional projection from Vl to VP or from VP to VI, the significance of the overall asymmetry would be reduced, but not entirely negated. What significance should be attached to the connectional asymmetries described here? Clearly, the occurrence of an asymmetry does not by itself provide an infallible basis for subdividing the cortex into different areas, for one would otherwise be forced to argue that Vl actually consists of two separate areas, only one of which projects to V3 and for that matter, to the pons (Glickstein et al., 1983). Pitted against this are many compelling similarities between dorsal and ventral Vl that are unique to this area and outweigh the one or two known differences. On the other hand, many cortical areas have originally been identified on the sole basis of being a particular projection field. V3 itself was initially identified on the grounds that it was a VI projection field that was topographically distinct from V2. Hence, we are inclined to take the connectional asymmetries seriously, but also as only part of a collection of important comparisons. Myeloarchitecture. Judgements relating to subtleties of cortical myeloarchitecture can be as much an art as a science, and numerous instances could be cited of mistaken or controversial assigments of myeloarchitectonic boundaries. Nonetheless, there are several recent

examples of successful correlations between myeloarchitectonic transitions and area1 boundaries in primate extrastriate cortex that were reliably identified with independent anatomical or physiological criteria. These include area MT in several species and areas V2 and DM in the owl monkey (Allman and Kaas, 197 I, 1974, 1975; Allman et al., 1973; Spatz and Tigges, 1972; Van Essen et al., 1981). From detailed examination and reconstruction of numerous cases, we are convinced that the myeloarchitectonic identification of V3 in the macaque is reliable, aside from an uncertainty relating to possible gaps along its length that we consider to be minor in the present context. It is unfortunate that VP cannot as yet be distinguished from V2. However, this does not obviate the discrimination between V3 and VP; in a similar sense, area MT can be reliably distinguished from neighboring areas V4 and MST even though neither of these areas is as yet individually recognizable solely on the basis of myeloarchitecture. Physiology. There is ample reason to be wary about claims of differences in functional properties between areas. Even within a single visual area there are many instances of marked discrepancies in estimates of certain types of stimulus selectivity. For example, the reported incidence of disparity selectivity in VI ranges from none to 84% (Hubel and Wiesel, 1970; Poggio and Talbot, 1981); the reported incidence of color selectivity ranges from 10 to 75% for Vl (Hubel and Wiesel, 1968; Bertulis et al., 1977) and from 20 to 100% for V4 (Zeki, 1973; Schein et al., 1982). However, in many cases the discrepancies are largely attributable to a reliance on subjective judgments for classifying cells, with the particular criteria used varying considerably from one study to the next. In the present situation we have not only applied objective, quantitative criteria for assessing response properties, but have used essentially the same recording and analysis procedures for studying the two areas under consideration. Thus, we are confident that the differences in color selectivity and direction selectivity are not only statistically significant, but are genuine in a biological sense. The differences are assuredly not absolute, in the sense of particular types of selectivity being universal in one area and completely absent in the other. Despite previous subjectively based reports of an extremely low incidence of color selectivity (O-5%) in V3 (Zeki, 1978; Van Essen and Zeki, 1978; Baizer, 1982), we found about

Visual

cortex

functional

20% of V3 cells to be color selective by our criteria. This discrepancy is probably attributable to our acceptance as color selective those cells that responded well to white light but to only a restricted range of monochromatic stimuli (for a discussion of this issue, see Van Essen, 1985). In VP, not all cells are color selective, and a substantial percentage are direction selective, but the same is true of V4, an area that is generally credited with a considerable degree of functional specialization for color (Zeki, 1978). A possible complication to our interpretation of these results concerns the properties of cells in the dorsal and ventral subdivisions of V2. Previous subjectively based single unit studies of dorsal V2 have reported a low incidence of color selectivity, ranging from 4 to 16% (Baizer et al., 1977; Zeki, 1978; Van Essen and Zeki, 1978), whereas our quantitative analysis of a small population (28 cells) in ventral V2 yielded a higher incidence of 64% (Burkhalter and Van Essen, 1982). If this were to reflect a genuine dorso-ventral functional asymmetry in V2, which nonetheless appears to be a single area by many other criteria, then similar reasoning could be used to argue that functional asymmetries do not provide a strong basis for treating V3 and VP as separate areas. However, we have recently recorded from dorsal V2 using multi-unit recording techniques, and have found a 40% incidence of color selectivity (De Yoe and Van Essen, 1985). Since multi-unit recordings are likely to underestimate the degree of selectivity in single units, it seems likely that there is no dramatic dorso-ventral asymmetry in color processing within V2 that would be comparable to what we have found for V3 z’s VP. Moreover, our estimate of direction selectivity in ventral V2 (20%) is in reasonable agreement with previous reports of 8816% for dorsal V2 (Baizer ef al., 1977; Van Essen and Zeki, 1978). Cot~chsions

regarding

V-7 and VP

The overall interpretation of the dorsoventral asymmetries described in this report can best be handled by addressing three general questions. First, are the differences indeed substantial enough to warrant the conclusion that there are separate visual areas adjoining dorsal and ventral VI?? Second. what are the likely homologies of each region, and what is the terminology to reflect these appropriate relationships? Third, irrespective of issues of

asymmetries

in macaque

75

terminology and homology, what is the significance of the various dorso-ventral asymmetries from the standpoint of information processing in the visual pathway? One area or t,vo? There is no universally accepted definition of precisely what constitutes a visual area in the cerebral cortex. so it is impossible to resolve this issue in an entirely unambiguous fashion. What can be rigorous, firmly stated, though, is that the overall differences between V3 and VP are comparable to or even larger than the differences often used to distinguish other extrastriate area in primates For example, the differences between V3 and VP are arguably greater than those between V3A and V4 (Van Essen and Zeki, 1978), or between MT and MST (Van Essen of al.. 198 I ; Maunsell and Van Essen, 1983a). Put another way, V3 is more similar to MT than to VP in its myeloarchitecture, connections, and physiological properties; VP is more similar to V4 than to V3 in its connections and physiological properties. What links V3 and VP together are: (i) topographic complementarity, with the two regions combined making up a hemifield representation; (ii) adjacency to V2; (iii) occupancy of the same hierarchical level (Maunsell and Van Essen, 1983b); and (iv) a historical association that was based in part on an incorrect identification of the outputs of VI. It seems abundantly clear that differences are large enough to warrant separate labels for the two regions, so that descriptions of various results can be easily and unambiguously related to one or the other region. Given the precedents noted in the Introduction of visual areas in other species which contain only partial representations of the contralateral hemifield, it is appropriate in our opinion, to go one step further and consider V3 and VP as separate visual areas. However. this is a matter of opinion, not of indisputable logic. Terminolog~~ wulhomolog~~. Considerations of terminology can play an important role in provoking careful evaluations of basic evolutionary relationships among neural structures. In the present case. the critical issue is the relationship among three different areas adjoining V2, two in the macaque and one in the owl monkey. Four distinct evolutionary possibilities are illustrated schematically in Fig. 8. The first possibility is that the ventral area in the macaque is phylogenetically unrelated to the dorsal area, but shares a common ancestor with VP in the owl monkey. The appropriate terminology to reflect this is the

A. BLJRKHALTER er al

16

POSSIBLE

EVOLUTIONARY

RELATIONSHIPS

Common II Owl Monkey Macaque II Ancertor Scheme 7

2

3,

4 Fig. 8. Four schemes showing possible evolutionary relationship among areas adjoining V2 in the macaque and the owl monkey. Each scheme shows one or more hypothetical visual areas (dashed outlines) in an ancestor common to both species. Arrows indicate the presumed lineages associated with each hypothetical area.

V3/VP scheme we have advocated in the present report. A second possibility is that a unitary area V3 (containing both upper field and lower field representations) in the common ancestor diverged to form distinct areas (or subdivisions) in the macaque, and that VP in the owl monkey originated from a separate area in the common ancestor. In this case, use of terms such as V3d and V3v would be most appropriate for the macaque, and it would not be of great significance whether these were regarded as separate areas or asymmetric subdivisions of the same area. A third possibility is that all three areas have a separate evolutionary origin, in which case the ventral area in the macaque should not be called either VP or V3v, but something else such as VV. Lastly, it is entirely possible that all three areas are homologous, i.e., that they diverged from a single area V3, In this case neither the V3/VP nor the V3d/V3v terminology would be misleading, and both should be acceptable. None of the terminological schemes illustrated in this figure is neutral; each is prejudicial in favor of some evolutionary relationships and against others. Nevertheless, it is obviously necessary to assign labels to these areas in order to

discuss them coherently, and it is Ihereforc necessary to make educated guesses as to which homologies are most likely. Issues of homology between areas can be notoriously difficult to resolve unambiguously. unless the species are very closely related or the number of common characteristics is especially numerous. In comparing visual cortex in Old World and New World monkeys, the only homologies that have been established beyond a reasonable doubt are for areas VI, V2, and MT, for which there is extensive anatomical and physiological evidence of similarities so striking that they could hardly have come about by convergent evolution (see Van Essen. 1979, 1985). For VP in the owl monkey and the macaque, the evidence for homology is strong, but not as compelling as for these other areas. To recapitulate, VP in both species is an elongated strip immediately anterior to ventral V2, sharing a horizontal meridian representation with it and having a vertical meridian representation associated with a narrow strip of callosal inputs. In the macaque, VP has strictly an upper-field representation, but in the owl monkey it may also contain a highly compressed representation of part of the lower contralateral quadrant as well (J. Allman, personal communication). The notion that a single area V3 diverged during evolution into separate areas VP (V3v) and V3 (V3d) in the macaque (Scheme 2 or 4) is more difficult to assess at present. In essence, such a possibility can only be evaluated by examining living relatives of ancestors that would have contained the original area V3. In nonprimates, a single area (19, or V-III) adjoining most (but not all) of V2 has been described for the cat and the squirrel (Donaldson and Whitteridge, 1977; Tusa et al., 1979; Hall P( al., 1971). However, this is not a universal characteristic of nonprimates, and a pattern of multiple areas adjoining V2 has been reported for the mouse and rat, for example (Wagor et NI., 1980; Olavarria et al., 1982; Olavarria and Montero, 1984). In the bushbaby, a prosimian primate, the available evidence indicates that there are multiple visual areas adjoining V2, not just a single area V3 (Allman et al., 1979). Additional evidence from other species is much to be desired, but at present there is no strong basis for assuming that a unitary area V3 must be a characteristic of early primate evolution. The various schemes in Fig. 8 do not address the issue of whether there is an explicit homo-

Visual

cortex functlonal

logue in the owl monkey of V3 in the macaque. One candidate for this is the dotso-medial area (DM). which is a heavily myelinated Vlrecipient area adjoining part of dorsal V2 in the owl monkey (Allman and Kaas, 1975; Lin e/ al., 1982). However. this possibility is complicated by the fact that DM contains a complete hemilield representation. Obviously, the explanation for this would depend very much on whether V3 in the common ancestor had a complete or only a lower-field representation. In any event, there are still other possibilities for V3 homologues in the owl monkey, such as the medial area, M (Allman and Kaas, 1976) or the compressed lower-field representation suggested for VP in the owl monkey (Allman, personal communication). Taking all these factors into consideration, there is no compelling evidence for or against any of the schemes of Fig. 8. Schemes I and 4 seem to us the most plausible, though, from which it follows that the V3/VP terminology is most reasonabie. The V3d/V3v alternative also corresponds to a plausible set of evolutionary relationships and hence should constitute acceptable usage as well. As more evidence accrues relating to issues of homology, it may eventually be possible to choose unambiguously among these and other alternatives. When considering such issues, it is important to keep in mind that homologous areas in different species need not be identical in all respects. For example, given that there are major species differences in color vision, originating in the retina, the incidence of color selectivity in visual areas of the owl monkey will almost certainly turn out to be much lower than in the corresponding areas of the macaque. Obviously, a low incidence of color selectivity in owl monkey VP should not be construed as evidence against a homology with macaque VP, any more than a difference in the incidence of color selectivity would be used as evidence against a homology of VI in the two species. In other words. evidence that plays an important role in distinguishing among areas within a species does not necessarily have the same impact when assessing homologies across species. For the cross-species comparisons the critical issue. as already noted, is whether the overall constellation of characteristics reveals a collection of similarities that are unlikely to have arisen from convergent evolution (see also Campbell and Hodos. 1970). The converse point is also worth making.

asymmetries

in macaque

Evidence that is especially relevant for making cross-species comparisons need not have quite the same significance for identifying areas within a species. For example. the fact that VP in the macaque and the owl monkey both share a horizontal meridian representation with V2 is, in our opinion, particularly significant because the adjacency is in both cases with ventral VS. In contrast, the fact that VP and V3 in the macaque also share a horizontal meridian representation with V2 is not as meaningful in this context, because the two areas are not in corresponding parts of the brain, the adjacency being with different subdivisions of V2. Funclional usymmetries. Although we have dealt most intensively with the problems of identifying and naming visual areas, the physiological comparisons have a significance on their own which is independent of these terminological issues. Whatever name is used for each area, the fact remains that there is a basic asymmetry in the way visual information is processed in upper 1’s lower parts of the visual field. It is not yet clear how widespread such asymmetries are in the macaque. There are some hints that other visual areas, in particular V4 and the area ventral to it denoted as VA/V4 in Fig. I, may lack complete representations of the contralateral hemifield (see Van Essen, 1985). There is also evidence of asymmetries in the proportion of cortex devoted to upper vs lower fields in areas VI and MT (Van Essen (‘1 NI., 1981, 1984). It is natural to wonder whether there are psychophysical correlates of these asymmetries. In this regard, it should be recalled that none of the known physiological asymmetries are absolute, in the sense of a complete absence of one type of selectivity in one area (e.g. color in V3 or direction selectivity in VP). Also, any asymmetries relating to V3 and VP might well be cancelled by compensatory asymmetries in other areas. Thus, any perceptual consequences might be rather subtle, but nonetheless would be worth testing for. There are reports of small differences in reaction time and in visual acuity for stimuli presented in upper c’s lower fields (Payne, 1965; Millodot and Lamont, 1974), but these might simply be related to physical differences in the length of pathways within the brain or to retinal asymmetries related to photoreceptor or retinal ganglion cell densities (Van Buren. 1963). Another ditference is that reaction times to stimuli depth are shorter when in stereoscopic

A.

7x

UUHK~*ALTER ef ul

presented closer than the fixation distance in the lower field and farther than the fixation distance in the upper field (Jules2 et al., 1976). However, this may be related to a tilt of the visual horopter from the fronto-parallel plane that results from disparity-processing mechanisms in Vl (Helmholtz, 1925; Cooper and Pettigrew, 1979). Finally, clinical studies in humans have demonstrated a variety of differential effects of dorsal (occipito-parietal) US ventral (occipitotemporal) lesions on visual function (Meadows, 1974; Damasio et al., 1980, 1982). However, the perceptual deficits reported to date have been associated with the entire hemifield contralateral to the lesion (outside whatever local scotoma might be present). Hence, the results are of interest with respect to dorso-ventral functional asymmetries but not (as yet) with respect to upper-field us lower-field asymmetries. In short, we are not aware of any published examples of convincing asymmetries in cortical processing capabilities in upper vs lower fields in monkeys or humans, but this may well be a consequence of insufficient or inappropriate types of testing. thank C. Shotwell and K. Tazumi for histological work and preparation of figures, and L. Rodriguez for typing the manuscript. This work was supported by NIH grant EY 02091. Acknowledgements-We

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