J Neurophysiol
88: 2796 –2808, 2002; 10.1152/jn.00403.2001.
Spatial Organization and Magnitude of Orientation Contrast
Interactions in Primate V1
H. E. JONES, W. WANG, AND A. M. SILLITO
Department of Visual Science, Institute of Ophthalmology, University College London, London EC1V 9EL, United Kingdom
Received 16 May 2001; accepted in final form 23 July 2002
Jones, H. E., W. Wang, and A. M. Sillito. Spatial organization and
magnitude of orientation contrast interactions in primate VI. J Neurophysiol 88: 2796 –2808, 2002; 10.1152/jn.00403.2001. We have
explored the spatial organization of orientation contrast effects in
primate V1. Our stimuli were either concentric patches of drifting
grating of varying orientation and diameter or grating patches displaced in x–y coordinates around a central patch overlying the classical receptive field (CRF). All cells in the sample exhibited response
suppression to iso-oriented stimuli exceeding the CRF. Changing the
outer stimulus orientation revealed five response patterns: 1) orientation alignment suppression (17% of cells)—a suppressive component
tuned to the same orientation as the cell’s optimal, 2) orientation
contrast facilitation (63%)—responses to orientation contrast stimuli
exceeded those to the center stimulus alone, 3) nonorientation specific
suppression (3%), 4) mixed general suppression and alignment suppression (14%), and 5) orientation contrast suppression (14%)—
cross-oriented stimuli evoked stronger suppression than iso-oriented
stimuli. Thus most cells (94%) showed larger responses to orientation
contrast stimuli than to iso-oriented stimuli, and over one-half showed
orientation contrast facilitation. There appeared to be a spatially
structured organization of the zones driving the different response
patterns with respect to the CRF. Nonorientation-specific suppression
and orientation contrast suppression were predominantly evoked by
orientation contrast borders located within the CRF, and orientation
contrast facilitation was mainly driven by surround stimuli lying
outside the CRF. This led to different response patterns according to
border location. Zones driving orientation contrast facilitation were
not necessarily contiguous to, nor uniformly distributed around, the
CRF. Our data support two processes underlying orientation contrast
enhancement effects: a simple variation in the strength of surround
suppression drawing on the fact that surround suppression is tuned to
the same orientation as the CRF and a second process driven by
orientation contrast that enhanced cells’ responses to CRF stimulation
by either dis-inhibition or orientation contrast facilitation. We suggest
these processes may serve to enhance response levels to salient image
features such as junctions and corners and may contribute to orientation pop-out.
tatory influences. In this work we consider the influence of the
orientation of the surround stimulus. While it has long been
recognized that, for many V1 cells, surround suppression is
tuned to the same orientation as the cell’s excitatory response
and is diminished as the orientation of a surrounding stimulus
deviates from this (e.g., Blakemore and Tobin 1972; Gilbert
and Wiesel 1990; Kastner et al. 1997; Knierim and Van Essen
1992; Lamme 1995; Orban et al. 1979; Sillito et al. 1995), our
observations suggest that more complex interactions may apply. Previously we reported that, for some primate V1 cells,
orientation contrast could induce an effect that was greater than
that predicted from a simple modulation of the strength of
surround suppression (Sillito et al. 1995). Other studies report
findings consistent with this view (Knierim and Van Essen
1992; Li and Li 1994; Nothdurft et al. 1999), although some
have not seen this effect in the cat (Sengpiel et al. 1997;
Walker et al. 1999). This issue is of great interest because such
orientation contrast effects may link to mechanisms underlying
perceptual pop-out for this class of stimuli (Bergen and Julez
1983; Treisman and Gelade 1980), or for moving stimuli, to a
process extracting the motion of corners or angled junctions in
images. Our work on direction contrast showed that the location of the border between center and surround stimuli with
respect to the CRF strongly influenced the response pattern
observed (Jones et al. 2001). Here, we explore the influence of
orientation context between a central and surrounding stimulus
generated in a range of spatial configurations. The results show
that the location of borders with respect to the classical receptive field (CRF) is a key variable influencing both the strength
and the way V1 cell responses are affected by orientation
contrast. We discuss the mechanisms that may underlie these
observations.
METHODS
Primate V1 cells show strong surround suppression to moving stimuli (Sceniak et al. 1999; Sillito et al. 1995), and we
recently dissected the way this is modulated by reversing the
direction of the surround stimulus (Jones et al. 2001). The data
suggested that direction contrast may reduce both local and
lateral inhibitory influences and possibly enable lateral facili-
We recorded single-unit responses from the parafoveal primary
visual cortex of anesthetized [sufentanil (4 ␮g/kg/h) or halothane
(0.1– 0.4% in 70% N2O-30% O2)] and paralyzed (0.1 mg/kg/h vecuronium bromide) monkeys (Macaca mulatta). The animals were
treated according to the published guidelines on the use of animals in
research (EEC Directive 86/609/EEC, National Institutes of Health
Guidelines for the Use of Laboratory Animals). Full experimental
details are provided elsewhere (Jones et al. 2001).
Data were collected and visual stimuli were generated using a VS
system (CED, UK) in conjunction with a Picasso Image Generator
Address for reprint requests: A. M. Sillito, Dept. of Visual Science, Institute
of Ophthalmology, University College London, Bath Street, London EC1V
9EL, UK (E-mail: [email protected]).
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.
INTRODUCTION
2796
0022-3077/02 $5.00 Copyright © 2002 The American Physiological Society
www.jn.org
ORIENTATION CONTRAST EFFECTS IN PRIMATE V1
(John Daughman), presented on a Tektronix 608. Prior to running the
experimental protocols described below, we quantitatively checked
preferred orientation and direction of motion and classed cells as S or
C type. We assessed the location and extent of the CRF using a battery
of tests and derived CRF size from the test giving the largest value
(Jones et al. 2001). First we explored the spatial locations from which
a small patch of optimally oriented drifting grating evoked responses.
We also defined the area (width and length) from which a moving bar
elicited excitatory responses. We then varied the diameter of an
optimally oriented patch of grating centered over the receptive field.
Finally, we varied the inner wall diameter of an annulus of optimally
oriented grating. To minimize adaptation effects from persistent presentation of optimally oriented stimuli and to generate control data for
subsequent tests, the protocols varying patch size or annulus inner
wall diameter also varied stimulus orientation. A blank stimulus was
included in each block to assess spontaneous activity.
We used concentric sinusoidal gratings to explore the interactions
between an inner stimulus patch centered over the CRF and an outer
annulus. Contrast, spatial frequency, and drift rate were identical for
both, and we varied the orientation of both stimulus components in a
randomized interleaved sequence. The phase of our inner and outer
stimuli were locked together with reference to the center of the
display, thus iso-oriented concentric stimuli appeared as a single
grating. Controls for responses to inner and outer stimuli alone were
repeated periodically in the test sequences. Spatial frequency ranged
from 1 to 4 cpd and drift rate spanned 1– 4 Hz. Grating contrast
[(Lmax ⫺ Lmin)/(Lmax ⫹ Lmin)] was 0.36 with a mean luminance of 14
cd/m2. The interface border between cross-oriented inner and outer
stimuli encompasses a range of spatial frequencies and orientations
that might provide a separate or additional stimulus driving the
observations. The calculated energy of these components is very low
relative to those of the main stimuli. Nonetheless, we checked for effects
from the interface by using a narrow gap (set to the mean unmodulated
contrast level) between inner and outer stimuli. The data indicated that
these boundary properties were not a factor underlying our findings.
Individual cells were studied for 6 –16 h and observations repeated
several times.
We used a range of protocols to assess the influence of the spatial
configuration of the stimuli on orientation contrast effects. First, we
varied the diameter and hence the location, with respect to the CRF,
of the border between center and surround stimuli (range, 0.3– 6°).
Second, we varied the outer diameter of the surround annulus (range,
2–9°). Third, we varied the inner diameter of the annulus while the
diameter of the center patch was fixed. In this case, when the center
patch diameter was smaller than the inner wall of the annulus, the
luminance of the resulting gap was set to the mean luminance of the
contrast gratings.
We also used two square grating patches to locate facilitatory
zones. One patch, containing an optimally oriented drifting grating,
was centered over the CRF. The other was presented in randomized
sequence at a range of locations around the field either at the optimal
or at the orthogonal orientation. Its contrast was also varied between
two values, either 0.36 (to match the central patch) or 0 (no second
stimulus present to assess the response to the central stimulus alone).
Patch sizes ranged from 0.5° to 2°.
Quantifying responses
Responses were computed from the mean firing rate averaged over
the full number of stimulus presentations. Typically we presented 3–5
stimulus cycles of each stimulus condition repeated over 5–20 trials.
Cells were regarded as orientation biased if the ratio of the response
to the optimal versus the nonoptimal orientation was 3:2 or greater
and as orientation selective if the ratio was 3:1 or greater. We
calculated a patch suppression index using the formula [1 ⫺ (Rplat/
Ropt)] ⫻ 100, where Ropt and Rplat denote the responses to optimal and
plateau stimuli, respectively (see Jones et al. 2001).
J Neurophysiol • VOL
2797
We compared the responses evoked by iso-oriented and orientation
contrast stimulus configurations. Cells were regarded as showing
“orientation pop-out” if the response to an optimally oriented center
stimulus in the presence of an orthogonal outer stimulus (⫾30°) was
significantly larger than the response when both stimuli were present
at the optimal orientation (P ⬍ 0.05, paired t-test). In some cases,
responses to orientation contrast stimuli exceeded the response to the
center stimulus alone. Cells were only classed as “orientation contrast
facilitation cells” if the response to the orientation contrast configuration was significantly larger (P ⬍ 0.05) than the responses to the
iso-orientation configuration and the inner stimulus alone, and if the
response enhancement evoked by the orientation contrast condition
(normalized with respect to the response to the center stimulus alone)
exceeded 10%. Cells were classed as “nonorientation specific surround cells” if there was no significant difference between the responses to iso-orientation and orientation contrast stimulus conditions
(P ⱖ 0.05). Cells were classed as “orientation contrast suppression
cells” if the response to orientation contrast was significantly smaller
(P ⬍ 0.05) than to the iso-orientation stimulus.
We graphically represented the data collected with bipartite concentric stimuli using two-dimensional iso-response contour maps and
three-dimensional surface maps. Distance between contours was defined by (Rmax ⫺ Rmin)/(1 ⫹ number of levels); Rmin defined the first
level, and we used a spline fitting algorithm to interpolate between
responses. We used the same procedure to represent the data from the
two patch experiments.
To explore the location of zones driving orientation contrast facilitation, we adapted methodology previously used in area MT (Xiao et
al. 1997, see also Jones et al. 2001). We calculated the strength of
facilitation for each surround stimulus location according to the formula F ⫽ [(Rcs/Rc) ⫺ 1] ⫻ 100, where F is the enhancement elicited
by a surround stimulus location, Rc is the response to the center
stimulus, and Rcs is the response to the combination stimulus. We then
computed two selectivity indices (FIs) by calculating the length of the
mean vector
冑冋冘
册 冋冘
2
n
FI ⫽
Fi 䡠 sin 共␣i兲
i⫽1
n
⫹
冘
i⫽1
册
2
Fi 䡠 cos 共␣i兲
n
Fi
i⫽1
where Fi is the magnitude of the surround facilitation at each surround
angular location, ␣i. The Unimodal Selectivity Index (USI) was
derived from the actual ␣i values, whereas the Bimodal Selectivity
Index (BSI) was calculated with each ␣i value doubled. The USI
assessed the tendency for surround facilitation to be concentrated in
one location, whereas the BSI reflected the tendency for facilitation to
be concentrated along an axis on opposite sides of the CRF. For both,
a value of 1 indicated that only a single surround position (or axis)
was effective in modulating activity, whereas a value of 0 denoted an
uniform distribution. We used the Rayleigh test (Batschelet 1981) and
the USI and BSI values to subdivide the response patterns into three
groups: uniform surround facilitation (Rayleigh test, P ⬎ 0.05), asymmetric surround facilitation (Rayleigh test, P ⬍ 0.05 and USI ⬎ BSI),
and bilaterally symmetric facilitation (Rayleigh test, P ⬍ 0.05 and
BSI ⬎ USI).
We identified the most effective location by calculating the mean
vector angle (Batschelet 1981). Thus the optimal angle OPA
⫽ arctan
冤
n
¥ Fi 䡠 sin 共␣i兲
i⫽1
n
¥ Fi 䡠 cos 共␣i兲
i⫽1
冥
. For bilaterally symmetric surround
cells, the OPA represents the angle of the axis through the two optimal
surround locations.
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H. E. JONES, W. WANG, AND A. M. SILLITO
RESULTS
Our data draw on observations from 70 cells (44 S and 28 C
cells). All exhibited surround suppression for iso-oriented
stimuli [mean suppression, 69.4 ⫾ 2.17% (SE); range, 30 –
100%]. We observed no significant differences between S and
C cells except in two instances highlighted below.
Response patterns to orientation contrast stimuli
We observed five response patterns using concentric centersurround stimuli. These are summarized in Fig. 1 and were
defined on the basis of the effect of varying the orientation of
a surrounding stimulus on the response to an optimally oriented
central stimulus (although the data were extracted from test
sequences that randomly interleaved the orientation of both
stimulus components).
ORIENTATION ALIGNMENT SUPPRESSION. The records in Fig. 1,
A and B, typify the response expected from a suppressive
mechanism tuned to a cell’s optimal orientation. The dotted
curve shows the response to varying the orientation of an
optimal sized patch of grating. The solid line plots the response
to varying the orientation of the surrounding annulus in the
presence of the inner held at its optimal orientation. There is a
clear suppressive effect tuned to the optimal orientation. As the
annulus deviated from the cell’s preferred orientation, the
degree of suppression diminished to zero, leaving the response
at the level evoked by the inner alone. This pattern of orien-
tation pop-out (“orientation alignment suppression”) is broadly
what would be expected from previous work. Twelve cells
showed this response pattern.
CONTRAST FACILITATION. Another pattern is
shown in Fig. 1C, again using an optimal diameter center stimulus. Once more, the cell showed a clear suppressive effect tuned to
the cell’s optimal orientation. However, in this case, when the
surround stimulus orientation deviated from optimal by more than
30°, the response increased substantially above that to the center
stimulus (“orientation contrast facilitation”). This might be considered to reflect the addition of a component of orientation
contrast facilitation above the modulation of the surround suppression, although dis-inhibition might also play a significant role.
Forty-four cells showed this response pattern, and for over onehalf (23/44) the responses to orientation contrast stimuli exceeded
the response to any single stimulus tested. This latter group
included individual cells showing increases of 300% or more.
ORIENTATION
MIXED GENERAL SUPPRESSION AND ORIENTATION ALIGNMENT
SUPPRESSION. Some cells (10) showing suppressive effects
tuned to the optimal orientation also exhibited a nonorientation
tuned suppressive component as shown in Fig. 1D (“mixed
general suppression and orientation alignment suppression”).
We observed two
cells (both S type) that exhibited the same level of suppression
to any orientation of the outer stimulus (“nonorientation specific suppression,“ see Fig. 1E).
NON-ORIENTATION SPECIFIC SUPPRESSION.
FIG. 1. Response patterns to orientation
contrast stimuli. A and B: 2 examples of orientation alignment suppression. For each cell,
the dotted line plots the response (i/s) to varying the orientation of an optimal diameter (1°)
center patch of grating. Solid line shows the
effect of varying the orientation of an outer
annulus of grating (inner wall diameter 1°) in
the presence of the optimally oriented inner
patch. Gray shading denotes ⫾SE. Short black
line denotes spontaneous activity level. C: orientation contrast facilitation. Tuning curves
plot the cell’s response to varying the orientation of an optimal diameter center patch
presented alone (dotted line), varying the orientation of an outer annulus presented alone
(dashed line), and varying the orientation of
the outer annulus in the presence of the optimally oriented inner patch (solid line). The
response to the orientation contrast configuration clearly exceeded that to the center stimulus. Patch diameter, annulus inner wall diameter, and interface diameter are 1°. D: mixed
general suppression with a component of
alignment suppression. Stimulus conventions
as in A. Patch/interface diameter, 0.75°. E:
nonorientation specific suppression. Stimulus
conventions as in A. Patch/interface diameter,
2°. F: orientation contrast suppression. Tuning
curve plots the effect of varying the orientation of an annulus in the presence of an optimally oriented center patch. Arrowhead denotes the response to the center patch (0.75°)
presented alone. The annulus elicited no suppressive influence when presented at the cell’s
optimal orientation, but exerted potent suppressive effects as the orientation of the outer
deviated away from the optimal orientation.
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ORIENTATION CONTRAST EFFECTS IN PRIMATE V1
TABLE
2799
1. Magnitude of orientation contrast effects, normalized with respect to the response to the test center stimulus alone
Response Pattern
Iso-Orientation Configuration, %
Orientation Contrast Configuration, %
Non-orientation specific suppression (n ⫽ 2, 3%)
Orientation contrast suppression (n ⫽ 10, 14%)
Mixed general suppression/orientation alignment suppression (n ⫽ 10, 14%)
Orientation alignment suppression (n ⫽ 12, 17%)
Orientation contrast facilitation (n ⫽ 44, 63%)
Supra-optimal orientation contrast facilitation (n ⫽ 23, 33%)
⫺52
⫺2 ⫾ 13.71
⫺82 ⫾ 3.61
⫺63 ⫾ 5.03
⫺27 ⫾ 4.95
⫺30 ⫾ 5.94
⫺52
⫺67 ⫾ 7.24
⫺56 ⫾ 5.21
⫺4 ⫾ 5.97
⫹118 ⫾ 24.39
⫹107 ⫾ 24.07*
Values are mean ⫾ SE. * For the supra-optimal group, the mean response increase for the orientation contrast configuration translated into a mean increase
of 66 ⫾ 14.57% SE above the value for the optimal diameter center stimulus alone.
ORIENTATION CONTRAST SUPPRESSION. The final pattern is
shown in Fig. 1F. Here, the suppression driven by the surround
stimulus was minimal at the optimal orientation (arrowhead
denotes the response to the optimally oriented inner stimulus)
and maximal when the orientation differed by roughly more
than 30°. Although this might be considered to reflect what is
often referred to as cross-orientation inhibition, clearly it is not
simply that, and we have termed it “orientation contrast suppression.” Two cells (both S type) showed only this response
pattern. Another eight cells also showed orientation contrast
suppressive effects; however, for these, the response pattern
depended on the interface diameter between the inner and outer
stimuli. Generally, these cells showed orientation contrast suppression for borders within the CRF and orientation contrast
facilitation for borders outside the CRF (see below).
For the first three response patterns described above, responses to iso-oriented stimuli were significantly smaller than
to orientation contrast stimuli. Thus 94% of our sample (66/70
cells) showed orientation pop-out.
For each response pattern, we compared the response modulation evoked
by iso-oriented and orientation contrast stimulus configurations. This is summarized in Table 1, where the values denote
the percentage decrement (⫺) or increment (⫹) observed with
respect to the response to the center stimulus alone. For a given
cell, the values for iso-orientation and orientation contrast
configurations were derived from data using the same interface
diameter between the inner and outer stimuli, and in each case
the data derives from the interface diameter that evoked the
most potent orientation contrast response modulation. Hence,
the lower level of iso-orientation surround suppression observed for orientation contrast facilitation cells followed from
the fact that orientation contrast facilitation was most often
evoked by interface diameters larger than the CRF. Thus at
these diameters, suppression was already partially implemented in the response to the center stimulus.
MAGNITUDE OF ORIENTATION CONTRAST EFFECTS.
ANGULAR DEVIATION UNDERLYING THE EFFECTS. Although it
might seem convenient to reduce the description of these effects to
TABLE
either cross-orientation facilitatory or inhibitory influences, our
data suggested much more focused interactions linked to much
smaller differences in orientation between the inner and outer
stimuli (e.g., Fig. 1, C and F). This is summarized in Table 2,
which shows the smallest deviation in orientation between the
inner and outer stimuli that elicited a significant change in response and the angular deviation that evoked the maximal response change, for each response pattern. Overall, over 50% of
cells showed significant changes in output for angular deviations
of 22.5° or less. Even when considering angular deviations eliciting maximal changes in output, ⬍25% of cells required angular
deviations exceeding 67.5°.
Dissection of the spatial focus driving orientation contrast
interactions
INTERACTIONS OBSERVED VARYING THE INTERFACE DIAMETER
FOR CONCENTRIC STIMULI. The location of the border between
the inner and outer stimuli with respect to the CRF could
markedly influence the magnitude and nature of the effect
observed, and a given cell could show different effects for
different border locations. The cell in Fig. 2, A and B, showed
orientation alignment suppression for a border diameter that
equated to its CRF (0.75°, Fig. 2A). Thus as the outer stimulus
deviated from the cell’s optimal orientation, the suppression
diminished to zero, leaving the response at the level seen with
the inner alone. Testing the cell with a 2° center stimulus
revealed a different response pattern (Fig. 2B). The center
stimulus produced a smaller response because of surround
suppression. However, varying annulus orientation, although
revealing additional suppression at the optimal orientation,
actually enhanced the response above that evoked by the 2°
center stimulus as its orientation deviated from optimal. Thus
for this spatial configuration, the cell exhibited strong orientation contrast facilitation, although the absolute response level
was lower than to the optimal, CRF-sized, center stimulus.
Another set of interactions is shown in Fig. 2, C and D. An
inner stimulus smaller than the CRF (Fig. 2C) evoked orientation
2. Degree of angular deviation underlying orientation contrast effects
Response Pattern
Smallest Angular Deviation
(range; degrees)
Angular Deviation for Maximal Effect
(range; degrees)
Orientation contrast suppression
Mixed general suppression/orientation alignment suppression
Orientation alignment suppression
Orientation contrast facilitation
18 ⫾ 3.29, 5–22.5
34 ⫾ 4.76, 20–67.5
24 ⫾ 4.49, 5–67.5
41 ⫾ 4.46, 10–90
31 ⫾ 5.73, 22.5–45
58 ⫾ 4.36, 20–90
45 ⫾ 4.91, 10–67.5
57 ⫾ 4.37, 20–90
Values are mean ⫾ SE.
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H. E. JONES, W. WANG, AND A. M. SILLITO
FIG. 2. Changing border location influences orientation
contrast effects. A and B: tuning curves plot the responses
of a cell to varying the orientation of a center patch presented alone (dotted line), varying the orientation of an
annulus presented alone (dashed line), and varying the
annulus orientation in the presence of the optimally oriented center patch (solid line) for 2 different border locations. Patch diameter, annulus inner wall diameter, and
interface diameter were 0.75° in A and 2° in B. C and D:
responses of another cell for 2 different border locations.
Each tuning curve shows the effect of varying annulus
orientation in the presence of an optimally oriented center
stimulus. Arrowhead denotes the response to the optimally
oriented center stimulus presented alone. Interface diameter was 0.5° in C and 1° in D. E–G: each tuning curve plots
the response of the same cell to an annulus of varying
orientation in the presence of an optimally oriented inner
stimulus, for 3 different interface diameters. In each record,
the arrow head denotes the response to the optimally oriented inner patch presented alone. For E, the border between the inner and outer stimulus (0.3°) was located
within the classical receptive field (CRF, 0.75°). For F, the
border was located at the edge of the CRF (0.75°), whereas
for G, it was located outside the CRF (1.5°). Scale bars
denote response magnitude (i/s). H–J: histograms summarize the percentage of cells tested at locations within (H),
on the edge of (I), and outside (J) the CRF, exhibiting the
various patterns of orientation linked surround influences.
If a cell showed different effects at different border locations, it is represented more than once in the histograms.
The category for points on the edge of the CRF refer to
observations where the border diameter corresponded to
the CRF diameter.
contrast suppression. Conversely, for an inner stimulus diameter
exceeding the CRF (Fig. 2D), the pattern switched to orientation
contrast facilitation. In four cells, we were able to track changes
from orientation contrast suppression, through orientation alignment suppression to orientation contrast facilitation with increasing border diameter (e.g., Fig. 2, E–G). Overall, this suggests the
presence of three mechanisms that are isolated by different centersurround border interfaces. These respectively generate orientation contrast suppression, orientation alignment suppression and
orientation contrast facilitation.
Although it was not possible to identify any single spatial
focus with respect to the CRF that drove a specific pattern of
orientation contrast dependent effects, our data suggested a
general trend. The histograms in Fig. 2, H–J, summarize the
percentage of cells tested at locations within, on the edge of
and outside the CRF exhibiting the different response patterns.
The majority of orientation contrast facilitatory effects were
J Neurophysiol • VOL
seen on the edge of and outside the CRF, while orientation
contrast suppressive effects were virtually confined to border
diameters within the CRF. Orientation alignment suppression
was seen at all locations but showed the largest incidence on
the edge of the CRF. It is possible that we might have observed
more instances of orientation contrast suppression if we had
tested loci within the very central region of the CRF; we did
not use stimuli that would test this point in these experiments
(DeAngelis et al. 1992). We only observed nonorientation
specific suppression with interfaces within the CRF.
Although we emphasize a broad transition of effects for centersurround interfaces moving from within to without the CRF, we
observed exceptions to this rule. Some cells (see above) only
exhibited orientation alignment suppression. Others (n ⫽ 7)
showed only orientation contrast facilitation. Figure 3 shows a
series of curves for the responses of a cell to an outer stimulus
alone, an inner stimulus alone, and the combination of the two for
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ORIENTATION CONTRAST EFFECTS IN PRIMATE V1
FIG. 3. Changing border location did not always influence orientation contrast responses. Tuning curves in the left column plot the cell’s response to
varying the orientation of an annulus centered over the receptive field. Tuning
curves in the middle column plot the response to varying the orientation of a
central patch, while those in the right column plot the response to varying the
orientation of the annulus in the presence of a center patch held at its optimal
orientation. The 4 rows correspond to stimulus components and combinations
for interfaces at diameters of 0.5°, 1°, 2°, and 3°, respectively.
a set of border diameters spanning within (0.5°), on the edge of
(1°), and outside (2° and 3°) the CRF. In all cases, the combination stimulus evoked a potent facilitation of the response to the
center alone when the outer orientation deviated from the optimal
by 30° or more. These effects were very strong and reproducible,
as is highlighted by the small error bars for the responses denoted
by the gray shadows.
INTERACTIONS
STIMULI. We
USING
NONCONTIGUOUS
INNER
AND
OUTER
further examined the spatial characteristics of
the mechanism driving orientation contrast effects by varying
the inner and outer boundaries of the outer stimulus while
holding the dimensions of the inner stimulus constant (e.g.,
Fig. 4). The effect of varying the outer wall of the outer
stimulus on the combination response is shown in Fig. 4, A–C.
There was possibly a very small enhancement of the level of
orientation contrast facilitation in the step from 2° to 3°, but the
most notable feature was the appearance of stronger iso-orientation suppression to the largest (4°) value tested for the outer
diameter. On the other hand, when the outer wall of the outer
annulus was held at 4° while varying its inner diameter from 1°
to 3° (generating a 0°, 1°, and 2° gap, Fig. 4, D–F) orientation
contrast facilitation was also largely unchanged, and if anything, most strongly expressed for the largest gap. Together,
these observations suggest that processes driving orientation
contrast were expressed throughout the surrounding area of
visual space. Interestingly, in both sets, maximum surround
suppression for the iso-oriented condition was seen when the
surround stimulus was most extensive.
We dissected the mechanisms driving these interactions in a
different way (Fig. 4, G and H) by using two square patches of
drifting grating, one centered over the CRF (and presented at
the cell’s optimal orientation) and the second displaced over a
set of coordinates to map the surrounding area of visual space.
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The second patch was presented either at the optimal or at the
orthogonal orientation. The central point of each surface plot
shows the response to the inner patch alone and the other
locations in the surface plot show the way the response to this
center stimulus was modified by the presence of the second
stimulus at these locations. Using 1° patches (G), there was no
effect from the second patch at 90° except for a fractional
enhancement at one extreme side of the area tested, whereas
the second patch at 0° evoked suppression from all locations
around the field with a maximal effect at one end. This contrasts with the effects revealed using 2° stimuli (H). Here the
second stimulus at 0° elicited virtually no effect from most
locations, while that at 90° evoked a strong facilitation from all
locations around the field. This suggests that some minimal level
of spatial integration was required before the orientation contrast
facilitation was enabled. Presumably any of the concentric surrounding stimuli met this criterion but a 1° patch did not.
The cell in Fig. 5A showed an asymmetric pattern of suppression for an iso-oriented second stimulus. With an orthogonal stimulus, it showed a strongly asymmetric area of facilitation to the top right, separated from the CRF by a clear
suppressive zone. We also tested its responses while varying
the location of the inner wall of a surrounding annulus (Fig. 5,
E–H). Essentially there was a simple modulation of surround
strength as the annulus orientation was changed and this pattern held as a 0.2° and then a 0.5° gap was introduced.
However, increasing the gap to 1° (Fig. 5H) revealed a strong
orientation contrast facilitation to the ⫺90° direction of motion
of the annulus. We suggest that this facilitatory effect was
drawn from the asymmetric facilitatory zone shown in Fig. 5A,
but for the other stimulus configurations with smaller gaps it
was masked by the counteracting inhibitory region.
For our orientation contrast facilitation cell group (n ⫽ 44),
the data from the two patch paradigm indicated a wide variety
of spatial configurations driving facilitatory effects. We analyzed the data and subdivided cells into three groups using the
criteria of Xiao et al. (1997; see METHODS). Only 14% of cells
showed spatially uniform facilitation. An example is shown in
Fig. 5B, where the orthogonal stimulus evoked strong facilitatory effects from all locations around the receptive field and up
to the edge of the area tested. The remainder had heterogenous
surrounds. Fifty-three percent of cells showed spatially asymmetric facilitation where facilitation was concentrated in one
surround location. For the example in Fig. 5D, the orthogonal
stimulus elicited a strong facilitatory effect from the bottom
left location whereas all other locations evoked suppression.
Thirty-three percent of cells showed bilaterally symmetric regions. For the example in Fig. 5C, the orthogonal stimulus
evoked powerful facilitation from the ends, but not the sides, of
the field. For cells exhibiting heterogenous surrounds, we
checked if the regions evoking facilitation were localized to the
ends, sides or corners of the field. All regions evoked orientation contrast facilitation, there was no evidence to suggest that
the mechanisms underlying the effect were concentrated in
either end-zones or side-bands.
Orientation contrast interactions in nonorientation tuned
cells
We had expected nonorientation tuned cells to exhibit uniform surround suppression. Surprisingly they did not. Of nine
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H. E. JONES, W. WANG, AND A. M. SILLITO
FIG. 4. Exploring the spatial characteristics
of mechanisms underlying orientation contrast
effects. A–F: tuning curves document the effect
of varying the outer (A–C) or inner (D–F) diameter of the outer annulus on orientation contrast effects. In each record, the tuning curve
depicted by the dotted line shows the effect of
varying the orientation of a 1° center patch. The
solid line plots the effect of varying the orientation of the outer annulus while the inner stimulus was presented at its optimal orientation. In
all cases, the diameter of the center patch was
fixed (1°). In A–C, the inner diameter of the
annulus was also fixed at 1°, while its outer
diameter was varied through 2° (A), 3° (B), and
4° (C). In D–F, annulus outer diameter was fixed
at 4°, and its inner diameter was varied through
1° (D—no gap), 2° (E—1° gap), and 3° (F—2°
gap). G and H: surface/contour plots depict the
same cell’s responses to a stimulus configuration
that comprised an inner stimulus (a square patch
containing an optimally oriented grating drifting
in the cell’s preferred direction of motion) centered over the CRF and a second stimulus (another square patch of grating) which was positioned at a range of x–y locations around the
central stimulus (as depicted by the schematic
diagram). In G and H, the 2 plots show the
modulatory effect of the outer stimulus when it
was presented at either the same orientation as
the center (0/0) or when it was orthogonally
oriented (0/90). Center and second patch were
1° square for G and 2° square for H. For each
plot, responses are normalized to the response
elicited by the center patch alone (100%). Color
scale bar depicts response scale values.
cells studied, four exhibited orientation alignment suppression
and five orientation contrast facilitation. Thus these cells were
strongly sensitive to orientation contrast but not to orientation
per se. Figure 6 documents the responses of a nonorientation
tuned layer 4C␤ cell (CRF size 0.5°) to varying the orientation
of both the center patch and outer annulus, at three border
diameters. The diagonal trough running between the axes represents all those points where the orientation of the inner and
outer stimuli were identical over a complete sequence of absolute orientations. Clearly, responses were minimal when the
J Neurophysiol • VOL
orientation of the inner and outer stimuli were the same.
Moreover, for each border diameter, responses to orientation
contrast stimuli exceeded the response to the inner stimulus
alone and for the 0.5 and 1° configurations, the resultant output
exceeded the response to the optimal inner patch presented
alone. Essentially, iso-oriented stimuli drove the mechanism
generating patch suppression, resulting in a reduced response,
but this was disenabled when they were at different orientations. Thus despite the cell’s lack of orientation tuning, its
output was extremely sensitive to orientation differences.
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ORIENTATION CONTRAST EFFECTS IN PRIMATE V1
2803
FIG. 5. A–D: these surface/contour plots
depict the responses of another 4 V1 cells to
the duo-square paradigm. Graphical conventions as Fig. 4. E–H: these tuning curves
document the effect of varying the inner diameter of an annulus on the responses of the
cell illustrated in Fig. 5A. Conventions as in
Fig. 4, D–F. In all records, the outer diameter
of both the center patch and the annulus were
fixed and annulus inner diameter was varied
through 0.5° (A—no gap), 0.7° (B— 0.2°
gap), 1° (C— 0.5° gap), and 1.5° (D—1°
gap).
Apart from the lack of orientation tuning, this response
pattern was characteristic of many orientation tuned cells and
for smaller interface diameters a very similar pattern could be
seen in the surface plots documenting the responses of some
orientation tuned cells.
Multi-orientation interactions in orientation tuned cells
As we varied the orientation of the concentric inner and
outer stimuli in a randomized sequence for all cells studied, we
had the data to generate the same surface plots for orientation
tuned cells. For the cell in Fig. 7, A–D, interface diameters
within the field (0.5°, 0.6°) evoked a response pattern resembling that of the 4C␤ cell. Conversely, when the interface
diameter matched (0.75°) or exceeded (1.5°) the CRF, orientation tuned responses emerged. However, these were still
modulated by the orientation of the outer, so that the response
was minimal when the outer was at the cell’s optimal orientation and maximal when it deviated by 45° or more. The cell
J Neurophysiol • VOL
was sharply orientation tuned to the center stimulus for all
these diameters. Thus the interplay between the inner and outer
stimuli, when the interface was within the field, seemed to
facilitate responses to all orientations of the inner providing the
outer orientation was different and suppress them when they
were the same. This effect was not the trivial consequence of low
orientation selectivity to the center patch at small diameters.
Figure 7, E–F quantifies this enabling effect of the outer on
the inner stimulus for two further orientation tuned cells. The
histograms plot the response to the center stimulus at 90° to the
cells’ optimal orientation, the outer stimulus at the optimal
orientation and to the combination of the two. In both cases the
firing level driven by the inner alone was at the spontaneous
rate and the response to the combination was much greater than
the sum of the components to the two single stimuli.
The pattern of interaction shown in Fig. 7, A and B, for
border diameters within the CRF was seen for 28% of our
sample. The majority of the other cells exhibited response
profiles of the type shown in Fig. 7,C and D, at all interface
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H. E. JONES, W. WANG, AND A. M. SILLITO
for most orientation tuned cells, the influence of the orientation
contrast provided by the outer stimulus is only reflected in the
modulation of the response to the inner at orientations in the
envelope of orientations centered around the cells’ optimal
(e.g., Fig. 7, C and D).
Orientation contrast facilitation and firing level
FIG. 6. Nonorientation tuned cells are sensitive to orientation contrast.
Surface plots show the response of a nonorientation tuned layer 4C␤ cell to
varying the orientation of both a center patch and outer annulus in a randomly
interleaved sequence for 3 interface diameters (A, 0.5°; B, 1°; and C, 2°).
Magnitude of the cell’s response is shown by the height and shading of the
contour. Diagonal running from bottom left to top right represents all those
points where the orientation of the inner and outer stimuli were the same, over
a complete sequence of absolute orientations. The cell gave a vigorous response to all those conditions where the orientation of the inner and outer
stimuli differed, and a minimal response to all the conditions where they were
the same. Difference in response between the aligned and nonaligned conditions was statistically significant for all 3 interface diameters (P ⬍ 0.001,
Mann-Whitney U test). Color scale bar shows response scale values.
diameters. The above observations suggest a focal interaction
within the CRF that highlights the cell’s output for orientation
contrast irrespective of absolute orientation and indicate that
this mechanism is present in a small proportion of orientation
tuned cells as well as for nonorientation tuned cells. However,
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We took great care to ensure that we avoided saturating
responses and used a contrast of 0.36 for all observations.
However, given the limited data on the prevalence of orientation contrast facilitation from previous studies, and the failure
of certain groups (Sengpiel et al. 1997; Walker et al. 1999) to
observe it, we considered possible links between orientation
contrast facilitation and absolute response strength. First, we
checked if the magnitude of the normalized enhancement reflected the cell’s initial firing rate (i/s) to the center stimulus but
there was no significant correlation (Spearman R) between the
two values. In Table 3, we compare the mean firing level of
orientation contrast facilitation cells to three stimulus conditions (the optimal center stimulus, the center stimulus used in
the test paradigm, and the response to the orientation contrast
configuration) first for the entire group, and then subdivided
into “supra-optimal” and “facilitation only” categories. For the
combined sample, there was no significant difference between
the firing rates associated with the best single stimulus and the
configuration evoking orientation contrast facilitation, although both were significantly larger than the response to the
inner test stimulus (P ⬍ 0.001, Wilcoxon). Interestingly, two
factors appeared to contribute to the identification of the “supra-optimal” group, these cells showed significantly lower
responses to the best single stimulus as well as higher firing
rates to orientation contrast stimuli. There was nothing in the
details of the tests or our procedures to suggest that we may
have missed the most appropriate “optimal” single stimulus for
these cells. Overall, we favor the view that these cells were
characterized by rather stronger inhibitory processes within the
central regions of the CRF and that this accounted for the lower
firing rates to the best single stimulus.
The two square dissections of the spatial organization
of the mechanism integrating the facilitatory effect of stimulus configurations generating orientation contrast provided
much smaller foci for stimuli generating the contrast effects
than the annulus paradigm. If the integration performed
some type of spatial summation one might predict that the
effects elicited by the two square paradigm would be lower
and that they might decline with distance from the CRF.
Neither possibility was supported by the data. There was no
statistical difference between the magnitudes of the effects
elicited with contiguous concentric annuli or single squares of
drifting grating in effective locations (Mann-Whitney U test;
P ⫽ 0.79). Given the high degree of asymmetry revealed by the
analysis of the two square data this is hardly surprising because
only certain regions seemed to drive the effects (consider in
this case the examples in Fig. 5) and hence spatial summation
by the concentric stimuli may not exert larger effects because
the regions driving the effects are circumscribed for many
cells.
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ORIENTATION CONTRAST EFFECTS IN PRIMATE V1
2805
FIG. 7. Orientation contrast interactions
for an orientation tuned cell. A–D: surface
plots show the response of an orientation
tuned cell to simultaneously varying the orientation of a center patch and outer annulus
for 4 border diameters (A, 0.5°; B, 0.6°; C,
0.75°; and D, 1.5°). Conventions as in Fig. 6.
There was a significant difference in response magnitude between the aligned and
nonaligned conditions at all interface diameters (P ⬍ 0.001, Mann-Whitney U test). E
and F: cross-oriented stimuli that elicit little
or no effect when presented in isolation
evoke potent excitatory effects when presented together. Bar histograms show the
responses (i/s) of 2 cells to an outer annulus
presented at the cell’s optimal orientation, a
center patch presented at the orthogonal orientation, and the combination of the two.
Error bars denote ⫾SE.
Direct surround effects
An important question concerns the direct effects of the
surround stimulus in the absence of CRF stimulation. As the
tuning curves for the outer stimulus alone in Figs. 1 and 3
show, orientation contrast facilitation did not appear to be
linked to direct excitatory effects driven by the outer stimulus
(although subliminal facilitation could be a factor) and clear
responses to the annulus alone were nearly always restricted to
the cell’s optimal orientation (e.g., Fig. 3). Across our sample
of “orientation contrast facilitation cells” the mean firing rate
evoked by an orthogonally oriented surround stimulus presented alone was low (1.5 ⫾ 0.5 ips) and could not in any
additive sense account for the variance in response to the inner
alone and the combination firing levels discussed above. InTABLE
deed the response to the combination of stimuli was significantly higher than to the sum of the responses to the components (P ⬍ 0.001, Wilcoxon paired test) for each cell in the
sample.
DISCUSSION
Our data taken with moving stimuli highlight a series of
processes that contribute to the influence of orientation context
on primate V1 cell responses. The most common pattern of
influence (94% of our sample) was an orientation contrast
dependent modulation in which cells gave larger responses
when the surrounding stimulus orientation differed to that over
the CRF. Given that the majority of primate V1 cells show
strong surround suppression (Jones et al. 2001) this is consis-
3. Firing rates for orientation contrast facilitation cells
Response Pattern
Optimal Single Stimulus
(i/s)
Test Inner Stimulus
(i/s)
Orientation Contrast
(i/s)
All cells
Facilitation only
Supra-optimal only
33 ⫾ 4.52
42 ⫾ 8.65
24 ⫾ 2.84
21 ⫾ 2.50
21 ⫾ 4.72
21 ⫾ 2.94
34 ⫾ 3.83
33 ⫾ 6.71
39 ⫾ 4.44
Values are mean ⫾ SE.
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H. E. JONES, W. WANG, AND A. M. SILLITO
tent with an orientation contrast dependent modulation of the
surround suppression (e.g., Gilbert and Wiesel 1990; Kastner
et al. 1997; Orban et al. 1979; Sengpiel et al. 1997; Walker et
al. 1999). The mechanism would follow from the fact that long
range horizontal connections target cells of similar orientation
preference and contact local inhibitory interneurons as well as
spiny cells (Gilbert and Wiesel 1989; Kisvarday and Eysel
1992; Malach et al. 1993; Ts’o et al. 1986). However, the
majority of cells in our sample (63%, 44/70) showed an enhancement of the response to levels above that to the inner
stimulus alone as the orientation of the surround deviated away
from the cells’ optimal. Furthermore, roughly one-half the cells
in this group (23/44) gave responses to orientation contrast
stimuli that exceeded the cells’ responses to an optimal, CRFsized, inner stimulus alone. These effects were mainly (although not exclusively) seen for orientation contrast between a
center and surrounding stimulus where the diameter of the
central stimulus was the same size or greater than the CRF. For
some cells they appeared to draw on the fact that the surround
suppression was already implemented by a central stimulus
that extended beyond the CRF and derived from a modulation
of this (e.g., Fig. 2, A and B). For this reason we suggest that
this effect might involve dis-inhibitory interactions, mediated
via connections to the local inhibitory interneurons driving the
suppression from other inhibitory interneurons linked to different orientations. This is plausible from the anatomical viewpoint as indicated by, for example, papers establishing the
connectivity of GABAergic basket cells in V1 (e.g., Kisvárday
and Eysel 1992; Kisvárday et al. 1993, 1994; also Das and
Gilbert 1999).
In cases where the orientation contrast drove supra-optimal
responses, it is likely that a surround suppressive mechanism
was already implemented within the CRF, so that the response
to an “optimal stimulus” was already in part diminished by an
inhibitory mechanism that had the capacity to scale further as
the stimulus size increased. Several lines of evidence invoke an
inhibitory mechanism within the CRF driven by an optimal
stimulus (Borg-Graham et al. 1998; Creutzfeldt and Ito 1968;
Douglas et al. 1991; Ferster 1986; Sillito 1975, 1977) and this
sits in a number of models of visual cortical mechanisms
(Dragoi and Sur 2000; Jones et al. 2001; Li 1999, 2000;
Somers et al. 1998) and of the processes contributing to surround suppression (Sceniak et al. 1999). From this viewpoint,
the scaling of the orientation contrast facilitation would build
on the strength of the iso-orientation inhibition implemented in
the CRF center. This does appear to vary in primate V1 cells
(Jones et al. 2001). In some cells we observed facilitatory and
supra-optimal facilitatory effects for interfaces between center
and surround stimuli that sat within the CRF (e.g., Fig. 3).
Again we would suggest that this reflects a strong inhibitory
process implemented at the very center of the CRF and a
dis-inhibitory mechanism driven by the orientation contrast.
Although the observation that orientation contrast effects
can deliver response magnitudes that exceed those to the central stimulus alone seems compatible with a dis-inhibitory
mechanism, the effect has not been previously reported. Some
studies (e.g., Li and Li 1994; Nothdurft et al. 1999) include
examples that might be taken to suggest the presence of the
effect but the question remains why have others not seen this?
One issue may follow from the fact that we used moving
stimuli for all our tests in contrast to those used in studies
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drawing on data from behaving primates which have often used
static patterns. Second, although some previous studies have
used moving stimuli, many of these were carried out in cat
(e.g., Kastner et al. 1997; Sengpiel et al. 1997; Walker et al.
1999). If dis-inhibitory mechanisms, as we suggest above,
largely underpin orientation contrast facilitation, then the proportion of such effects in cat would be expected to be much
lower than for primate, since the incidence of surround suppression itself in the cat is much less (N. M. Oakley, P. C.
Murphy, H. E. Jones, and A. M. Sillito, unpublished data).
Third, a key feature distinguishing our work from that of others
is that we explored a wide range of spatial interfaces between
inner and outer stimuli. Only 7 of the 44 cells showing orientation contrast facilitation showed the effect at all interface
locations with respect to the CRF size. Thus had we adopted
the procedures used in many previous studies where only one
interface diameter was used to explore orientation contrast
effects we may have failed to detect the majority of examples
reported in this study. This is doubly underlined by the fact that
the single interface diameter selected in many previous studies
never exceeded the size of the CRF (see for example, Sengpiel
et al. 1997; Walker et al. 1999 in the cat), whereas we recorded
the majority of orientation contrast facilitatory effects for interface diameters exceeding the CRF (as shown in Fig. 2).
Approximately 20% of the cells showing orientation contrast
facilitatory effects showed orientation contrast suppression for
interfaces within the CRF and orientation contrast facilitation
for interfaces outside. Although cross-orientation inhibition
within the CRF has been described and considered by many
previous studies (Carandini et al. 1998; Creutzfeldt and Ito
1968; DeAngelis et al. 1992; Morrone et al. 1982; Pei et al.
1994; Sillito 1975), this orientation contrast suppression was
much more sharply focused either side of the optimal (with the
range of deviations for maximal suppressive effects spanning
from 22.5– 45°). The way these processes interact may depend
on the space constants of the areas driving the two processes,
but the balance seems to suggest that the force of the orientation contrast dis-inhibition/facilitation mechanism is likely to
draw on focuses outside the CRF, while the orientation contrast
suppression draws on a focus underlying the core of the CRF.
It must be noted that for these cells as the interface diameter
moved outside the CRF the orientation contrast suppression
switched to iso-orientation “surround suppression” as well as
orientation contrast facilitation. We also observed two cells
showing only orientation contrast suppression as well as the
two showing suppression driven by all orientations. These
might reflect specialized interneurons within the circuitry mediating some of the effects discussed above.
Another issue is highlighted by the observations for nonorientation tuned cells. Here the points made about the influence
of orientation contrast for the orientation tuned cells applied for
any orientation. Hence the cells provided a potent signal for
orientation contrast between their CRF and surrounding space
but not for orientation per se. It suggests that mechanisms
integrating the surround driven orientation contrast effects
could be implemented across the network in a fashion that
stands above the mechanism linked to orientation tuning. Normally it would appear linked to the orientation tuned CRF of
cells because it is only revealed when they fire and that firing
is orientation specific. Certainly we observed some orientation
tuned cells (e.g., Fig. 7) that displayed a pattern of interplay
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ORIENTATION CONTRAST EFFECTS IN PRIMATE V1
between center and surround stimuli for interface diameters
within the CRF that appeared very similar to those seen for the
nonorientation tuned cells. It appears that the orientation contrast between inner and surround stimuli within the CRF enabled responses that were otherwise submerged. Clearly there
is a great complexity and subtlety to the interactions influenced
by orientation context. Obviously if orientation tuned receptive
fields are built from the convergent input from nonorientation
tuned cells in primate V1 then the presence of the behavior
characterizing the nonorientation tuned fields for stimulus interface diameters within the CRF is hardly surprising.
The absolute firing levels of the cells under the different
stimulus conditions underlines the view that a dis-inhibitory
process might contribute to the different classes of effect. First,
for the entire population of cells showing facilitatory effects
(including the supra-optimal), the firing levels for the optimal
stimulus and for the interface diameter driving the best orientation contrast facilitation were not significantly different
(mean, 33 ⫾ 4.52 and 34 ⫾ 3.83 i/s), although both were
significantly different to the mean for the inner stimulus. Thus
we suggest that globally the orientation contrast serves to reset
the lower firing level associated with a particular inner stimulus
to that obtained by the best single stimulus. For the cells
showing supra-optimal responses it was notable that overall
they gave a significantly lower response to the best CRF sized
single stimulus than the cells showing facilitation only, as well
as a higher response to orientation contrast. The former being
consistent with the view that they reflected a higher level of
suppression elicited within the CRF. The larger response to the
orientation contrast configuration in these cells at least raises
the possibility that some additional mechanism to a dis-inhibitory process might further enhance their response. This could
be orientation contrast facilitation. There are grounds for this
type of interaction from both anatomical and physiological data
(Das and Gilbert 1999; Kisvárday et al. 1997; Sillito 1975;
Sillito et al. 1995), and it might be unmasked by the disinhibitory influence. Alternatively it could reflect a more potent
dis-inhibition and further work is necessary to isolate this.
The location, relative to the CRF, of the border between the
concentric center and surround stimuli was not the only spatial
parameter examined in these experiments. We checked the
effect of varying either the outer diameter of the outer stimulus,
or the inner diameter, while holding that of the inner stimulus
constant (Fig. 4). From this, it was clear that locations both
close to and remote from the CRF could drive the orientation
contrast facilitation with similar effect and that the effect did
not seem to sum with the area of the cross-oriented outer
stimulus. On the other hand, the strength of the surround
suppression elicited under iso-orientation conditions did seem
to increase with the area of the surround stimulus. We further
dissected the spatial organization driving these effects by using
a discrete second patch instead of an annulus to drive the
orientation context effects. There were two main conclusions
from this data, first, that there was an influence of patch size on
the effect seen, and second, that while for some cells the zones
driving orientation contrast facilitation were located uniformly
around the field (14%) in the majority of cases they were
heterogenous. Indeed for many (53%) the orientation contrast
facilitation was driven from predominantly only one location.
We found no evidence for a link between the effects and either
side bands or end-zones although in 33% of the cells the zones
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2807
driving effects were bilaterally symmetric. Interestingly, the
magnitude of the facilitatory effects driven by the discrete
patches of grating were not less than those drawn from the
surrounding concentric stimuli (see RESULTS). This suggests
that the orientation context per se, and its location, rather than
the absolute extent of the stimulus providing the context was
important. These data should not from this viewpoint thus be
seen to necessarily reflect processes underlying orientation
pop-out. Rather we suggest they may reflect a mechanism that
integrates the components of moving contours that form junctions such as corners. The facilitatory effects of orientation
contrast were seen for a wide range of angular deviations
extending from ⬍22.5° to 90° and would provide a broad filter
highlighting foci where the orientation of a moving contour
changed. Our use of moving stimuli make it difficult to directly
compare our data with those studies showing facilitatory interactions when line elements or Gabor patches are added in a
sequence along an axis parallel to a cell’s optimal orientation
(Ito and Gilbert 1999; Kapadia et al. 1995; Polat et al. 1998),
although we do see facilitatory effects from optimally oriented
surround stimuli that exclude the CRF center (Jones et al.
2001). The clear conclusions from our data are that orientation
context exerts a potent effect on the responses of virtually all
primate V1 cells and that the effect is strongly influenced by
the spatial characteristics of the stimulus configuration driving
the context. Finally, all the processes described whether for
nonorientation tuned cells or orientation tuned cells seem to
highlight foci where there is a change in orientation.
We are indebted to D. Matin and N. Burt for skilled technical assistance.
The support of the Medical Research Council is gratefully acknowledged.
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