1Section in Neurobiology, Yale School of Medicine, New Haven, Connecticut 06510; and 2Department of Neurobiology, The Rockefeller University, New York City, New York 10021
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ABSTRACT |
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Roe, Anna Wang and Daniel Y. Ts'o. Specificity of Color Connectivity Between Primate V1 and V2. J. Neurophysiol. 82: 2719-2730, 1999. To examine the functional interactions between the color and form pathways in the primate visual cortex, we have examined the functional connectivity between pairs of color oriented and nonoriented V1 and V2 neurons in Macaque monkeys. Optical imaging maps for color selectivity, orientation preference, and ocular dominance were used to identify specific functional compartments within V1 and V2 (blobs and thin stripes). These sites then were targeted with multiple electrodes, single neurons isolated, and their receptive fields characterized for orientation selectivity and color selectivity. Functional interactions between pairs of V1 and V2 neurons were inferred by cross-correlation analysis of spike firing. Three types of color interactions were studied: nonoriented V1/nonoriented V2 cell pairs, nonoriented V1/oriented V2 cell pairs, and oriented V1/nonoriented V2 cell pairs. In general, interactions between V1 and V2 neurons are highly dependent on color matching. Different cell pairs exhibited differing dependencies on spatial overlap. Interactions between nonoriented color cells in V1 and V2 are dependent on color matching but not on receptive field overlap, suggesting a role for these interactions in coding of color surfaces. In contrast, interactions between nonoriented V1 and oriented V2 color cells exhibit a strong dependency on receptive field overlap, suggesting a separate pathway for processing of color contour information. Yet another pattern of connectivity was observed between oriented V1 and nonoriented V2 cells; these cells exhibited interactions only when receptive fields were far apart and failed to interact when spatially overlapped. Such interactions may underlie the induction of color and brightness percepts from border contrasts. Our findings thus suggest the presence of separate color pathways between V1 and V2, each with differing patterns of convergence and divergence and distinct roles in color and form vision.
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INTRODUCTION |
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Cross-correlation techniques have been used to
reveal the cooperative computations between groups of neurons both
within and between areas. In the case of the lateral geniculate nucleus
and primary visual cortex (V1), correlated firing reveals pairs of neurons with overlapping receptive fields, i.e., computation of spatial
similarity (Reid and Alonso 1995; Tanaka
1985
). Within V1, correlated firing is found between neurons
with matching orientation and color preferences (Ts'o and
Gilbert 1988
; Ts'o et al. 1986
). Thus far,
little is known about the computations performed in V2 nor the
relationship of the functional maps to those computations. By studying
pairs of V1-V2 neurons, identified according to anatomic location and
classified by color and orientation, we have begun to address the
question of what the relevant computations between V1 and V2 may be.
Within the primate visual pathway, area V2 receives its primary
ascending input from area V1 and is considered the next hierarchical level beyond area V1. V1 and V2 are characterized by quite distinct functional organizations and share strong functional and connectional relationships (Girard and Bullier 1989; cf.
Mignard and Malpeli 1991
; Salin and Bullier
1995
). As revealed by anatomic methods, the interdigitated
lattices of "blobs" and "interblobs" in area V1 project
selectively to the thin and pale cytochrome oxidase stripes in V2,
respectively. Although each of these organizational structures contains
a range of cell types, each is dominated by different populations of
visual cells: thin stripes and blobs are characterized by nonoriented
color-selective cells and pale stripes and interblobs by oriented
broadband cells (DeYoe and Van Essen 1985
; Hubel
and Livingstone 1987
; Livingstone and Hubel 1984
; Roe and Ts'o 1995
; Tootell
1988
; Tootell and Hamilton 1989
; Ts'o and Gilbert 1988
; Ts'o et al.
1990a
; cf. Gegenfurtner et al. 1996
;
Leventhal et al. 1995
; Levitt et al.
1994
). These anatomic studies establish a concrete structural
framework for parallel color, form, and disparity/motion pathways in V1
and V2 (DeYoe and Van Essen 1988
; Hubel and
Livingstone 1987
; Livingstone and Hubel 1984
,
1987a
,b
). Some subsequent studies, however, have diverged from
a strictly segregated view of connectivity (e.g., for review, see
Merigan and Maunsell 1993
).
In this study, we address the issue of what type of interactions exist
between the color and form cortico-cortical pathways and whether within
the color pathway there is further specification of connectivity. To
approach this issue, we have assessed functional connectivity by using
cross-correlation analysis to detect the coincidence of spike firing of
simultaneously recorded V1/V2 cell pairs in Macaque monkeys. Previous
studies using cross-correlation techniques to study cortico-cortical
connectivity have focused on interactions between V1 and V2,
interhemispheric interactions, or thalamocortical relationships (cf.
Bauer et al. 1995; Brosch et al. 1995
,
1997
; Frien et al. 1994
; Girard and
Bullier 1989
; Nowak et al. 1995
; Reid and
Alonso 1995
; Salin et al. 1992
; Toyama et
al. 1977a
,b
). However, these studies have not examined
selectivity of interaction with respect to known functional
compartments within visual cortex. In this study, we have first
optically imaged visual areas V1 and V2 and subsequently targeted
imaged structures (e.g., the blobs and stripes) with multiple
microelectrodes. This approach permits the examination of interaction
with respect to cell type and functional compartment. Our findings
suggest a highly specific set of interactions between color cells that
differ depending on color selectivity, orientation selectivity, and
spatial overlap. In this report, we have chosen to focus on V1/V2
interactions involving color cells. Interactions within the orientation
system will be presented in a subsequent paper.
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METHODS |
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Surgical prep
Eleven hemispheres in nine adult monkeys (Macaca
fascicularis) were used for these experiments. Four of these
monkeys also were used for V2 mapping experiments (Roe and Ts'o
1994; cf. Roe and Ts'o 1992
, 1993a
,b
). After an
initial anesthetic dose of ketamine hydrochloride (10 mg/kg), animals
were intubated endotracheally and a 22-g catheter implanted in the
saphenous vein for drug delivery. Anesthesia was maintained throughout
the experiment by a constant infusion of sodium thiopental (1-2
mg · kg
1 · h
1);. Animals were paralyzed (pancuronium
bromide, 100 µg · kg
1 · h
1) and respirated; after paralysis the level
of anesthetic sufficient during surgical procedures was maintained. To
further assess depth of anesthesia, vital signs including heart rate
and electroencephalogram (EEG) were monitored continuously. Rectal
temperature was maintained at 38°C and expired
CO2 at 4%. After dilation of the pupils
(atropine sulfate 1%), eyes were refracted and fitted with appropriate
contact lens to focus on computer monitor 57 inches in front of the
animal. Fovea were projected onto the monitor with a Topcon fundus
camera. A craniotomy and a durotomy, ~1 cm in size, were made over a
region around the lunate sulcus (centered ~15 mm anterior to
occipital ridge and 10 mm lateral to midline), exposing a visual
cortical area near the V1/V2 border representing 2-5° eccentricity.
Analgesics and antibiotics were administered on recovery. All
procedures were conducted in accordance with National Institutes of
Health guidelines.
Studying interactions between specific functional structures in V1 and V2
OPTICAL IMAGING.
To guide placement of microelectrodes, optical imaging of intrinsic
cortical signals (Frostig et al. 1990; Grinvald
et al. 1986
, 1988
; Ts'o et al. 1990a
) first was
used to localize functional compartments within V1 and V2. The details
of imaging procedures have been described elsewhere (cf.
Grinvald et al. 1986
; Ts'o et al. 1990a
)
and only will be described briefly here. For increased cortical
stabilization during optical recording, an optical chamber was cemented
over the craniotomy, filled with lightweight silicone oil, and sealed
with a coverglass. The cortical surface was illuminated through the
chamber window with 630-nm wavelength light provided by optic fiber
light guides. A slow-scan CCD (charge coupled device) camera
(Photometrics) fitted with standard camera lenses then was positioned
over the chamber.
OPTICAL IMAGING AS A GUIDE FOR TARGETING ELECTRODES.
Multiple functional maps, including those for ocular dominance,
orientation, blob/interblob patterns in V1, and stripe locations in V2
(Ts'o et al. 1990a), were obtained. By revealing
cortical organizations relative to cortical surface vasculature, we
could precisely target cortical structures for purposes of
electrophysiological recording with microelectrodes or for tracer
injections. Once generated, these maps could be used for multiple
recording sessions within the same cortical region.
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ELECTROPHYSIOLOGICAL CHARACTERIZATION. By using optical maps generated either from the same recording session or from previous recording sessions, multiple independently drive microelectrodes (2-5) were targeted in selected V1 and V2 locations (see Fig. 1, C and D). Because we have concentrated primarily on the color and orientation domains, electrodes targeted primarily blobs and interblobs in V1 and thin and pale stripes in V2. In a typical session, one or two electrodes were held in V1 while one or more electrodes sampled multiple targeted zones in V2 stripes. This arrangement enabled the concurrent recording and comparison of interactions of a given cell type (e.g., a V1 color nonoriented cell) with several other cell types (e.g., a V2 color nonoriented cell and a V2 color oriented cell), using identical and simultaneous visual stimulation conditions. Recordings were obtained from superficial layers only (recording depths ranged from 0 to 600 µm).
On each electrode, single cells were isolated and physiologically characterized. To characterize cells, receptive fields were plotted with a hand-held projection lamp. By listening to raw amplified and to discriminated pulse outputs of neural responses (window discriminator by BAK or Gawnwave, courtesy Tim Gawne and Barry Richmond), we qualitatively characterized each unit for ocular dominance, peak and width of orientation tuning, degree of direction selectivity, degree of end inhibition, and color selectivity. Orientation selectivity was rated on a qualitative scale A-D, where A is most narrowly (<30°) and D is most broadly tuned (cf. Livingstone and Hubel 1984VISUAL STIMULATION, SPIKE TRAIN COLLECTION AND CROSS-CORRELATION ANALYSIS. After isolation of single cells on each electrode, neural spike trains were collected from each cell during visual stimulation. Several neuronal spike trains and stimulus sync pulses were recorded simultaneously and time stamped (temporal resolution, 0.1 ms) using a Spike 9 board driven software package (HIST written by Kaare Christian). Poststimulus time histograms and raw cross correlograms were calculated and displayed on-line.
Because of the low spontaneous firing rates typical of cortical neurons, we collected spike trains during the presentation of visual stimulation. Typically, stimuli (STIM software written by Kaare Christian) comprised moving bars of preferred orientation, size, color, and velocity presented on a computer monitor. The eyes subsequently were converged by placing a Risley prism in front of one eye and achieving precise overlap of right and left eye receptive fields of a V1 or V2 binocular cell. This setup ensures stimulation at a known and consistent disparity (roughly 0). When possible, separate stimuli were presented for each isolated cell. For cells with nonoverlapping receptive fields, we presented stimuli optimal for each cell (usually moving light bars the orientation, color, and speed of which were tailored for each cell's preferences). For cell pairs with overlapping receptive fields, we presented stimuli that were effective in stimulating both neurons in the cell pair (e.g., a single bar suboptimal for one or both cells). For example, for two cells with overlapping receptive fields, one of which is red selective and one that is broadband, a red stimulus, which is less effective for the broadband cell but effective in driving each cell, was used. To correct for the increase in spike firing because of visual stimulation, shuffle correlograms were calculated (the shift predictor) (Perkel 1966TRACER INJECTIONS AND HISTOLOGY. To aid in localizing recording sites post mortem, in some experiments pressure injections of red rhodamine or green beads (Lumafluor) were made with a glass pipette. In other experiments, during the recording session electrolytic lesions were made along each penetration by passing current (4 µA for 4 s) through the electrode tip. At the end of data collection, animals then were given a lethal dose of pentobarbital sodium and perfused through the heart with 4% paraformaldehyde. After extraction of the brain, the desired cortical region was removed, flattened, and immersed in 30% sucrose solution. The cortical tissue then was sectioned tangentially at 30 µm and alternate sections either were reacted for cytochrome oxidase histochemistry or coverslipped for visualization of fluorescent bead labeling. We reconstructed our recording site locations on the tissue by aligning electrolytic lesions, tracer injection sites, and imaged surface vasculature patterns with locations and sizes of vascular lumen in superficial sections of cortical tissue. Because our recording locations were indicated directly on the image of cortical surface vasculature (which is in exact registration with the functional images collected), we could accurately align recording sites with the optical images and with cytochrome oxidase stained sections.
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RESULTS |
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Little is known about how color information from V1 is distributed to color-selective structures in V2 and what new properties may arise from such interactions. To examine this issue, we studied the interactions of color-selective cells in V1 with those in V2. Recordings from both V1 and V2 were in the superficial layers. Cross-correlograms were collected between 249 pairs of V1-V2 cells, 146 of which were between color-selective cell pairs (see Table 1). Of the 146 V1/V2 color-color cell pairs studied, 42% (n = 61) were nonoriented/nonoriented, 25% (n = 36) were nonoriented/oriented, 7% (n = 11) oriented/nonoriented, and 26% (n = 38) oriented/oriented cell pairs (see Table 1). We also examined interactions between 38 color V1 and broadband V2 cell pairs, 23 broadband V1/color V2 cell pairs, and 42 broadband V1 and broadband V2 cell pairs. Interactions between oriented-oriented cell pairs will be presented in a separate paper.
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RECEPTIVE FIELD PROPERTIES.
We have used the classification system of Wiesel and Hubel
(1966) and further extended by Livingstone and Hubel
(1984)
and Ts'o and Gilbert (1988)
. Whereas
most V1 nonoriented color cells recorded were dominated strongly by a
single eye, almost all V2 cells were strongly binocular. The vast
majority of nonoriented cells we encountered fell in the Type II (57%
in V1, 50% in V2) or modified Type II (50% in V1, 40% in V2)
classification. Two true double-opponent cells, recorded in V1, were
encountered. In some cases (18/81), broadband cells in V2 displayed
strong secondary responses to specific colors (nonoriented: 5 red, 1 blue, 2 yellow; oriented: 5 red, 5 green). In both V1 and V2, roughly
20-25% of all color cells were related to the blue-yellow system, and
the remaining to the red-green system, consistent with previous reports
of RG/BY ratios in V1 (Ts'o and Gilbert 1988
).
NEURAL INTERACTIONS.
Interactions between V1 and V2 color cells exhibit a strong dependency
on similarity of color selectivity. To illustrate, four examples are
shown in Fig. 2. In Fig. 2A,
the correlogram between two R+/G modified Type II cells, one located
in a V1 blob and the second in a V2 thin stripe. The receptive field
sizes are drawn to scale and visual locations indicated (azimuth,
elevation). Each receptive field was stimulated repeatedly by a red
vertically oriented bar sweeping across its receptive field, during
which spike trains were collected; stimuli were presented through a single eye only. Figure 2A illustrates a strongly peaked
correlogram (strength index = 0.074, peak = 0.0158),
indicating a strong interaction between these two neurons.
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Receptive field overlap
NONORIENTED COLOR V1/NONORIENTED COLOR V2 CELL PAIRS. We also examined receptive field overlap (defined as the larger of the relative proportion of receptive field area in common) and center-to-center receptive field distance as other possible determinants of interaction strength. For nonoriented color cell pairs, neither receptive field separation nor receptive field overlap correlated with interaction strength (data not shown). Both of the color-matched cell pairs shown in Fig. 2, A and C, had an interaction strength of 3; however, the receptive fields in Fig. 2C are overlapped (20%), whereas those of Fig. 2A are not overlapped and, in fact, are >2.0° apart in visual space. Thus nonoriented color cells do not require receptive field overlap for functional interaction and, in fact, can interact over appreciable visual cortical distances.
NONORIENTED COLOR V1/ORIENTED COLOR V2 CELL PAIRS. Like nonoriented color cell pairs, similar color preference was a strong predictor of strong interactions between color-selective nonoriented V1 and oriented V2 cells (n = 30 pairs). In this population, of the seven cell pairs with strong peak strengths (peak size 3), six had similar color specificity.
However, in contrast to the nonoriented color system, oriented cells in V2 exhibit a strong dependency on spatial overlap (Fig. 4). Of 22 (of 30) cell pairs that were considered color matched, 85% (11/13) of those with nonoverlapping receptive fields had peak strengths of 0 or 1; 77% (7/9) of those with overlapping fields had peaks of 2 or 3. This distribution is significantly different [
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ORIENTED V1/NONORIENTED V2 CELL PAIRS.
Interactions between color-matched oriented V1 and nonoriented V2 cell
pairs (broadband, n = 6; color, n = 10)
were seen most often in cell pairs with nonoverlapping
receptive fields (Fig. 6A). Of
these cell pairs, all those with overlapping receptive fields
(n = 5) had peak indices of 0, and 65% of those with
nonoverlapping receptive fields (n = 11) had peak
indices of 2 or 3. The significant dependency on lack of overlap
[2 (0.975) = 5.7, df = 1] suggests
an interaction between oriented cells in V1 with distant color-matched
nonoriented cells in V2.
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DISCUSSION |
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Summary
Previous studies in primates have indicated selective anatomic
connectivity between the blobs in V1 and thin stripes in V2, structures
containing a predominance of color-selective cells (Livingstone
and Hubel 1984). However, no previous study has examined the
connectivity patterns of different types of color cells. In this study,
we have examined the functional interactions between color-selective
cells in V1 and V2 using cross-correlation of simultaneously recorded
spike trains. Although these correlations do not afford us the ability
to determine the precise circuitry underlying the interactions between
cell pairs, we can at least identify which types of interactions
commonly occur and which do not.
Using this method, we find V1 and V2 cells interact with a high degree
of specificity, with respect to color selectivity, with respect to the
extent of orientation tuning, if any, and with respect to spatial
overlap. Figure 8 summarizes the major types of V1-V2 interactions studied in this paper and their
dependencies. Color cell pairs examined in this paper demonstrated a
strong dependency on color-matching. Nonoriented color cell pairs are dependant primarily on color-matching and independent of receptive field overlap (Fig. 8A, top). Nonoriented V1 and oriented V2
cell pairs interact only when receptive fields exhibit spatial overlap (Fig. 8A, middle). In contrast, oriented V1 and nonoriented
V2 cells interact when they are spatially distant and do not
interact when overlapped (Fig. 8A, bottom). We will discuss
functional and spatial specificity of V1-V2 interactions, followed by
possible anatomic bases of these specific interactions, and conclude
with a discussion on the relevance of these findings to color vision. Thus our findings, while confirming the view that the extent of functional and anatomic segregations is not total nor complete within
V1 and V2 (e.g., for review, see Merigan and Maunsell
1993), nevertheless support the notion of a remarkably high
degree of functional segregation overall. Discrepancies or
uncertainties as to the extent of segregation often can be attributed
to variability in cytochrome oxidase staining, which should only serve
as one, imperfect, factor in such analyses.
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Functional and spatial specificity
In V1, interactions among color blob cells exhibit a strong
dependency on color matching; both common input and monosynaptic interactions were observed (Ts'o and Gilbert 1988).
Although color preferences in V2 have been shown to be more varied than
those in V1 (see RESULTS) (Roe and Ts'o
1995
; Ts'o et al. 1991
; Yoshioka et al.
1996
), we find interactions between V1 and V2 cells are also
strongly color matched and are most commonly found between either
red-green selective cell pairs or between blue-yellow selective cell pairs.
Injections into thin stripes result in preferential labeling in V1
blobs spanning regions ~3 mm in extent (Livingstone and Hubel
1984, Figs. 25, 26a, 28, and 30). Our finding that some cell
pairs interact only when their receptive fields overlap and others
interact despite large spatial separation suggests that convergence/divergence factors are cell type specific. That is, different functional cell types are likely to participate in different size networks. Some types, such as nonoriented color cells, have far-reaching interactions, whereas others, such as color-oriented cells, are more restricted in their spatial interactions.
At least two possibilities underlie this finding. One possibility is,
for example, that single nonoriented color cells project to both
nonoriented and oriented V2 color cells; however, although contacts
with nonoriented cells are made by both nearby and far-reaching parts
of the arbor, those with oriented cells are made only by nearby
portions of the arbor (Fig. 8B). Alternatively, there could be separate nonoriented color cell populations, some with large arbors
that contact nonoriented cells in V2; others with restricted arbors
contacting oriented cells in V2. We found no evidence for different
types of nonoriented color cells in V1. However, single axon arbor
reconstructions (Rockland and Virga 1990) suggest the presence of at least two arbor types projecting from V1 to V2, one that
terminates in one or two 200-µm-size clusters separated by 500-1,000
µm and another that is much larger (
3 mm in extent) and more
diffuse in termination pattern; it is not known in which V2 stripes
these arbors terminate. These arbor types could provide the anatomic
substrate for both focal innervation of individual stripes, of
subcompartments within stripes (e.g., nonoriented versus oriented color
regions of a thin stripe), and focal innervation of multiple (thin) stripes.
Sources of common input, feedforward, and feedback interactions
The fact that a majority of V1-V2 correlograms are centered on
zero suggests that coincidence of firing is driven by common inputs
(Bullier et al. 1992; Nelson et al. 1992
;
Roe and Ts'o 1997
). However, the width of V1-V2
correlograms also suggest the presence of both feedforward (positive
latencies) and feedback (negative latencies) interactions (discussed
below). Possible sources of common input include the thalamus, V1, V2,
or feedback from other cortical areas.
It is unlikely that these specific interactions are due to thalamic
input, either geniculate or pulvinar in origin. The possibility that
common drive arises from topographically appropriate LGN (lateral geniculate nucleus) color inputs to V1 and subsequently to V2
is inconsistent with peaks centered on zero, as this would result in
peaks with positive shifts. Furthermore, such inputs would not result
in differences in connectional specificity seen here. Neither are
divergent inputs from the LGN to V1 and V2 likely to provide
significant direct common drive. Direct inputs from the LGN to V2 are
quite sparse (arising almost exclusively from the S layers and
interlaminar zones) and cells projecting to both V1 and V2 virtually
nonexistent (Bullier and Kennedy 1983; Kennedy and Bullier 1985
). Thus the LGN is an unlikely source of common input to V1 and V2.
The pulvinar is also known to provide some anatomic inputs to V1 and V2
in the macaque. After topographically corresponding injections of
different tracers into V1 and V2, ~10% of all pulvinar neurons
labeled (both PL and PL-PI of the lateral inferior pulvinar) were
double-labeled (Bullier and Kennedy 1985, Table 6).
Pulvinar inputs to V2 project preferentially to the thin and thick
cytochrome oxidase stripes (Curcio and Harting 1978
;
Levitt et al. 1995
; Ogren and Hendrickson
1977
); however, it is not known whether they project to (e.g.,
color specific) substripe compartments within V2. Moreover, not only
are pulvinar inputs to V1 diffuse and terminate primarily in layer 1 (Ogren and Hendrickson 1977
), but the degree of their
topographic precision is uncertain (cf. Kennedy and Bullier
1985
; Perkel et al. 1986
). Finally, lesions of
the pulvinar do not lead to deficits of sensory processing per se but
rather to deficits involving saliency and attentional modulation
(Robinson and Cowie 1997
). Thus for reasons of anatomic specificity, robustness, and functionality, pulvinar inputs are unlikely to be the primary contributor to correlation between V1 and V2
activity observed in this study. Finally, feedback projections from
other cortical areas beyond V2 also are thought to be poor in
topographic precision and more diffuse in nature, making them a less
likely distinguishing source of common input (e.g., Salin and
Bullier 1995
; Shipp and Zeki 1989
).
In conclusion, we believe that neurons within V1 and V2 are likely to
be the most dominant sources of common input observed between V1 and V2
color cells. These inputs could act directly or indirectly; however,
because cross-correlation is known to be poor at detecting polysynaptic
interactions (for review, see Fetz et al. 1991), it is
likely that the interactions observed in this study are due to direct
interactions. One candidate for direct common input would be the
superficial layer pyramidal cells located in cytochrome oxidase blobs.
Cells in V1 blobs not only have locally specific connectivity
(Livingstone and Hubel 1984
; Ts'o and Gilbert
1988
) but also exhibit specific projections to thin stripes in
V2 (Livingstone and Hubel 1984
; Rockland and
Virga 1990
). Given the fact that extrinsically-projecting
pyramidal cells are known to give off local collaterals, it is quite
likely that single blob cells have terminations both in nearby blobs as
well as in V2 thin stripes. These neurons are thus well positioned to
give rise to common input to nonoriented V1/nonoriented V2 interactions
as well as nonoriented V1/oriented V2 interactions. In a similar
fashion, neurons in V2 thin stripes also could give rise to V1-V2
coincidence via a feedback projection and a local collateral.
Color Vision
The marked differences in spatial dependence of the three types of
interactions suggests differences in their functional roles in color
vision. The fact that spatially distant nonoriented color cells are
strongly correlated suggests a possible role for these interactions in
the propagation of fill-in of color as a surface property. Not only
would color-matching be important for the "coloring in" of a
bounded surface, but a high degree of spatial precision would not be
necessary (Morgan and Aiba 1985). In contrast, spatial overlap is apparently crucial for the interaction between nonoriented V1 cells and oriented V2 cells. Such emphasis on spatial precision may
underlie the encoding of color contours via the convergence of
nonoriented V1 inputs, similar to the way in which nonoriented thalamic
inputs are thought to converge onto V1 cells to generate orientation
selectivity (Chapman et al. 1991
; Hubel and
Wiesel 1962
; Reid and Alonso 1995
; Toyama
et al. 1977a
,b
). Interestingly, similarity in orientation
selectivity is not a predictor of interaction between color oriented
V1-V2 cell pairs (unpublished data), suggesting that orientation
tuning of color oriented cells in V2 is not propagated from V1 but is
generated de novo in V2.
The surprising finding that color-oriented cells in V1 interact only
with nonoverlapping nonoriented V2 cells suggests yet a different
functional role. These distant interactions between orientation-selective V1 cells and nonoriented V2 cells may play a role
in color and brightness induction from object boundaries or from other
types of inducing lines (e.g., see Ejima and Takahashi 1988; McIlhagga and Mullen 1996
; Rossi et
al. 1996
). For example, in the Craik-Cornsweet illusion, as a
result of an intervening local border contrast, two distant regions of
equal color/luminance appear different in color/luminance. The
feed-forward interaction between oriented V1 cells and nonoverlapping
V2 color cells may be a pathway by which border percepts are propagated
to distant regions of color or brightness.
In conclusion, the specific color interactions described in this paper suggest multiple color pathways between V1 and V2, each with its specific spatial specificities. Interactions between some V1/V2 color cell pairs (nonoriented/nonoriented color cell interactions) occurred over large spatial extents, suggesting a role for these connections in perception of surface brightness/color properties. Other interactions observed suggested a dedicated processing pathway for color contour perception (nonoriented/oriented color cell interactions) and color border induction effects (oriented/nonoriented color cell interactions). The progressive elaboration in receptive field properties of the cells of V1 and V2, and the concomitant increase in the variety of possible interconnections and interactions between these cells then may form the neuronal basis for the wide variety of perceptual abilities and phenomena that we experience in our visual world.
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ACKNOWLEDGMENTS |
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We thank M. Shadlen for constructive comments on this manuscript and L. Hinderstein and C. LoRusso for excellent technical support.
This work was supported by National Eye Institute Grants EY-06347 and EY-08240 and by the McKnight and Whitaker Foundations.
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FOOTNOTES |
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Address for reprint requests: A. W. Roe, Section in Neurobiology, Yale University School of Medicine, 333 Cedar St., SHM I-412, New Haven, CT 06510.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 23 December 1998; accepted in final form 17 June 1999.
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REFERENCES |
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