J Neurophysiol 89: 525–533, 2003;
10.1152/jn.00048.2002.
Surround Modulation Measured With Functional MRI in the Human
Visual Cortex
ADRIAN L. WILLIAMS,1 KRISHNA D. SINGH,2 AND ANDREW T. SMITH1
1
Department of Psychology, Royal Holloway, University of London, Egham TW20 0EX; 2Department of Vision Sciences,
Aston University, Aston Triangle, Birmingham B4 7ET; and MARIARC, University of Liverpool,
Liverpool L69 3X, United Kingdom
Submitted 25 January 2002; accepted in final form 4 September 2002
It was discovered many years ago that stimuli outside what
is now called the classical receptive field (CRF) of a visual
neuron in the mammalian cerebral cortex can influence the
magnitude of the excitatory response to an appropriate stimulus
presented inside the CRF (Blakemore and Tobin 1972; Maffei
and Fiorentini 1976; Nelson and Frost 1978). Such effects were
typically suppressive but in some cases facilitatory. Surprisingly little importance was attached to these effects, which
tended to be regarded as minor determinants of physiological
response properties. However, the 1990s saw a resurgence of
interest in this topic. Many studies were conducted that together have provided detailed information about the nature of
contextual effects arising from stimulation outside the CRF.
There is now a growing sense that the responses of neurons are
profoundly influenced by the visual context and that these
influences may be of fundamental importance in understanding
the operation of visual neurons.
In V1 neurons of both cats and macaque monkeys, contextual effects are typically suppressive. These are maximal when
the CRF and surround orientations are the same and reduced or
absent when they are very different (Gulyas et al. 1987; Levitt
and Lund 1997; Li et al. 2000; Li and Li 1994; Sillito et al.
1995). There is considerable variability among neurons (e.g.,
Nothdurft et al. 1999). As in the early studies, facilitation is
also sometimes seen and the relative contrasts of the center and
surround stimuli can be important (Polat et al. 1998). There are
also some reports that the tuning properties of the CRF response can be altered (e.g., Gilbert and Weisel 1990). The
relative direction of motion of center and surround stimuli is
important in direction-sensitive neurons both in areas 17 and
18 of the cat (Kastner et al. 1999; Li 1999) and particularly in
monkey areas MT and MST (Allman et al. 1985; Eifuku and
Wurtz 1998; Tanaka et al. 1986). Influences from outside the
CRF may vary with cortical lamina (Raiguel et al. 1995) and
they may be asymmetric (Xiao et al. 1997).
In the context of psychophysical measurements of human
perception, related phenomena have been demonstrated and a
similarly complex picture emerges. One approach has been to
measure the effect of contextual stimuli on contrast detection
thresholds. The threshold for detecting a grating patch is elevated by the addition of flanking patches (Bowling 1985; Ejima
and Takahashi 1983; Snowden and Hammett 1998) but several
authors have reported facilitatory effects (e.g., Tanaka and Sagi
1998; Yu and Levi 2000) and a few have obtained both
facilitation and suppression under different circumstances
(e.g., Polat 1999). Another approach is to study the effect of
context on the perceived contrast of a suprathreshold target.
Ejima and Takahashi (1985) reported that perceived contrast is
reduced if flanking gratings have a higher contrast than the test
grating but is increased if they have a lower contrast. Others
have found only suppressive effects (Cannon and Fullenkamp
1991; Olzak and Laurinen 1999; Xing and Heeger 2000).
Despite the widespread occurrence of these contextual influences, their purpose remains unclear. One function could be
contrast normalization (e.g., Heeger 1992). However, the complexity and stimulus specificity of some of the observed effects
suggests additional, more sophisticated functions (e.g., Sillito
et al. 1995).
Address for reprint requests: A. Smith, Dept. of Psychology, Royal Holloway, University of London, Egham TW20 0EX, United Kingdom (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
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0022-3077/03 $5.00 Copyright © 2003 The American Physiological Society
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Williams, Adrian, L., Krishna D. Singh, and Andrew T. Smith.
Surround modulation measured with functional MRI in the human visual
cortex. J Neurophysiol 89: 525–533, 2003; 10.1152/jn.00048.2002.
Visual context profoundly influences 1) the responses of mammalian
visual neurons and 2) the perceptual sensitivity of human observers to
localized visual stimuli. We present data from functional MRI studies
demonstrating contextual modulation in the human visual cortex.
Subjects viewed a circular grating patch that was continuously
present. A surround grating was added in an ON– OFF block design to
reveal its effect on the central region. Stimulus-correlated activation
was quantified and visualized on a flattened map of the occipital gray
matter. Modulation was measured in a region of interest activated by
the central grating alone. The observed effects were predominantly
suppressive, consistent with the effects typically found in single
neurons and perception. Suppression was greatest when the surround
and center had the same orientation and was reduced or absent when
it was orthogonal. When spatial phase was manipulated, suppression
was greatest for in-phase center/surround gratings and much reduced
or reversed (facilitation) for opposite-phase stimuli. With eccentric
stimulus presentation, suppression was reduced and facilitation became more common. The findings provide a direct demonstration of
the existence of powerful and stimulus-specific surround effects in
human visual cortex.
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A. L. WILLIAMS, K. D. SINGH, AND A. T. SMITH
GENERAL METHODS
Subjects
The subjects were eight healthy adults including the three authors
and five volunteers who were paid for their time. Some participated in
more than one experiment. Subjects were screened in accordance with
standard procedures and informed consent was obtained in writing.
Visual stimulation
Visual stimuli were generated by a computer and were projected
onto a rear-projection screen by means of an LCD projector (resolution 1024 ⫻ 768 at 75 Hz). The subject lay supine in the scanner. In
Experiment 1, the subject looked upwards at a mirror in which an
image of the projection screen was reflected binocularly. This arrangement gave an image that was approximately circular and had a
diameter of 9° (maximum) at the viewing distance of 3.5 m. In
Experiment 2 (which involved peripheral stimulus presentation), the
subject looked with the dominant eye into a custom-built optical
device that magnified the image on the screen by a factor of three.
This gave a monocular, circular image of diameter 27°. The nondominant eye was occluded. In all experiments, the mean luminance of the
image was approximately 240 cd/m2.
The stimuli were sine gratings that reversed in phase (counterphased) at 5 Hz. Counterphase gratings were used because they give
stronger activation than static gratings in fMRI experiments. They are
illustrated in Fig. 1. A block design was used in which a central
grating patch was continuously present and a surround grating annulus
appeared and disappeared with a squarewave temporal profile (30-s
cycle; see Fig. 1). This made it possible to set up tonic activation in
those parts of the retinotopic visual areas that represent the visual field
locations occupied by the central patch and to observe the effect of the
appearance of the surround on that activation. The central grating was
always horizontal. The diameter of the central grating was always
three times the period of the grating (see Fig. 1A). The spatial
frequency of the annular grating was always the same as that of the
FIG. 1. The stimuli used and their time courses. In each case the time profile of the center and surround stimuli are shown on
the left. Each ON– OFF cycle lasted 30 s and 8 cycles were presented (only 4 are shown). Images from the 2 phases of the block
design are shown on the right. A: sample stimuli used in the main experimental conditions. A central, counterphasing grating
stimulus was continuously present while the surround, which could have the same or the orthogonal orientation, appeared and
disappeared. B: control stimulus. The center appeared and disappeared and there was no surround. C: ROI definition stimulus, used
for defining the cortical representation of the central stimulus. The center and annulus, which were both flickering, were presented
in opposite temporal phases to demarcate the boundary between them.
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In this study, we use functional MRI (fMRI) to study the
effect of a surround grating on the magnitude of the activity
evoked in the visual cortex by a target grating. Contextual
effects in single units vary greatly among neurons, making it
difficult to assess the importance of each type of effect or to
deduce their overall consequences at the population level.
Psychophysical findings reveal the net result of such effects on
our perception, but do not allow us to map these results onto
their substrates. Potentially, fMRI can reveal the overall trends
seen in large neuron populations while still allowing different
visual areas to be studied separately. The purpose of the
experiments in this paper is to explore the feasibility of using
fMRI in this way, to establish some basic findings, and to relate
them to existing psychophysical and neurophysiological results.
This work was previously published in abstract form (Williams et al. 2001a,b).
EFFECTS OF VISUAL CONTEXT IN HUMAN VISUAL CORTEX
Data acquisition
Imaging was performed with a 1.5-T whole-body General Electric
LX/Nvi scanner equipped with a 40 mT/m gradient system. The
subject was positioned with the head in an RF receive-transmit headcoil. Local variations in blood oxygenation (BOLD response) were
measured using susceptibility-based fMRI, applying gradient-recalled
echo-planar imaging (EPI) sequences.
Either 20 or 24 parallel, 3-mm-thick planes were imaged using a
T2*-weighted sequence (TR ⫽ 3000 ms, TE ⫽ 40 ms, field of view ⫽
190mm, 64 ⫻ 64 voxels). The planes were axial and were chosen with
the aid of a midsagittal T1-weighted scout image to include the entire
occipital lobe. Each experimental run lasted for 4 min, during which
time functional images were acquired continuously. Each point in the
acquisition volume was sampled once every 3 s.
For each subject, a sagittal T1-weighted SPGR volume scan of the
posterior third of the brain was acquired (voxel size 0.78 ⫻ 0.78 ⫻ 1.6
mm). This was used to determine the anatomical localization of
functional responses. The analysis included simulated cortical flattening to obtain two-dimensional representations of cortical gray matter
(Engel et al. 1997; Sereno et al., 1995).
Data analysis
Each functional volume was first processed using a 3-D motion
correction program, AIR (automated image registration) (Woods et al.
1992). This realigns the functional volumes in the time series so as to
compensate for movement of the head within a run and then reslices
the volumes. Spatial smoothing of the functional signal was performed by convolution with a 3-D Gaussian function of SD 4 mm.
This smoothing reduces spatial noise (Friston et al. 1995).
Activation profiles were analyzed and visualized using BrainTools
(http://www.aston.ac.uk/⬃singhkd/mri3dX), which was developed by
the second author. The temporal activity profile of each voxel was
correlated with an ideal response profile. The latter consisted of a
squarewave representing the ON– OFF surround stimulus cycle, which
was retarded in phase by 6 s, representing the expected hemodynamic
delay, and smoothed with a Gaussian kernel (SD ⫽ 3 s). The timecourse of each voxel was smoothed with the same Gaussian, to reduce
temporal noise. Any linear trend over time was corrected. Cortical
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activation was then estimated for each 4-min run as the stimuluscorrelated activation (SCA), which is the product of the correlation
coefficient for the voxel and the SD of the signal, calculated over the
entire run (Bandettini et al. 1993). In terms of the equivalent General
Linear Model, SCA is the amplitude of the main component of interest
and it is linearly related to the mean percentage signal change from
baseline.
To visualize the functional activation values, a 2-D representation
of occipital cortex was derived from the 3-D anatomical data set,
using an algorithm developed at Stanford (Teo et al. 1997; see
http://white.stanford.edu/⬃brian/mri/segmentUnfold.htm). This algorithm simulates a process of flattening a portion of the gray matter
(typically centered in the calcarine sulcus) into a 2-D surface. Having
obtained a flattened representation of the occipital cortex of each
hemisphere in each subject, activations were superimposed as pseudocolor overlays.
To observe the modulatory effects of a surround stimulus on the
response to a central stimulus patch, a region of interest corresponding
to the central patch had to be carefully defined. Since the center and
surround are spatially adjacent and fixation is always imperfect, there
will inevitably be a zone of cortex around the boundary that is
stimulated by both center and surround during the course of the
experiment. When estimating activity caused by the center stimulus
alone, it is important to exclude this zone of contamination by the
surround. This was achieved with the aid of the ROI definition
stimulus (see Visual stimulation). In one phase of a block design, a
high-contrast flickering checkerboard filled a circular patch corresponding to the size and location of the circular grating patch used in
the main experiments. In the other phase, this patch disappeared and
a concentric circular checkerboard annulus was presented (see Fig.
1C). Following correlation with a model waveform describing the
temporal profile of the central patch, activation by the patch itself gave
a positive correlation while activation caused by the surrounding
annulus gave a negative correlation. When displayed as a colored
overlay on a flattened representation of the cortex, these correlations
appeared as a red/orange patch surrounded by blue/purple (see Fig.
2A). To define the region of interest to be used for quantitative
measurements of activation in the main experiments, a region comfortably larger than the (red) center-related activation was first defined
on the flatmap. The 3-D voxels that fell within this area were identified. To strip off the surround and leave a region of cortex corresponding to the central stimulus only, any voxels that did not 1) have
a positive correlation with the center stimulus and 2) have an uncorrected P value of ⬍0.01 were eliminated. This was to avoid the
blurring effect of multiple microsaccades around the fixation point. By
setting a threshold well above zero correlation, voxels in the border
region that may be contaminated by direct activation from the surround are largely eliminated, leaving a relatively pure, central region
of interest. Figure 2B shows the flatmap of Fig. 2A after thresholding
in this way. The set of voxels included in the ROI on this basis defined
the central measurement zone that was used for all other experimental
conditions run in the same session. For each such experimental
condition, activation in the included voxels was averaged to yield a
mean activation value for the central region.
Because the stimulus was usually foveal, it was not possible to
distinguish the visual areas (V1, V2, and V3) with adequate reliability.
The region of interest must be assumed to include the central portions
of several visual areas, not just V1.
Experiment 1: Effect of an annular surround
on a foveal target
In this experiment we examined the effect on the activation produced by a centrally fixated circular grating of an annular surround
grating of either the same or the orthogonal orientation. The central
target grating was horizontally oriented, had a contrast of 25%, and a
spatial frequency of 1.0 c/°. Its diameter was 3°. The surrounding
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center and its width was always equal to the radius of the center. Its
orientation could be either the same (parallel) or orthogonal.
A small central fixation spot (0.25° diam) was continuously present
during all experiments. To aid fixation and to maintain attention in a
constant state, the subject was given a task relating to the spot. The
spot changed randomly in color at a rate of 0.5 Hz and the subject was
asked to count the number of times he/she saw one particular color
that had been identified beforehand.
To measure the activity produced by the central grating itself, an
additional block design was used in which the central grating stimulus
appeared and disappeared and there was no surround (see Fig. 1B).
This is referred to as the “control stimulus” and its purpose was to
make it possible to express the effects of surrounds on center activation (obtained in the main experiments) as a proportion of the center
activation itself.
The control stimulus could also have been used to identify the patch
of visual cortex that responded to the central stimulus (the region of
interest or ROI). However, to identify the ROI with maximum accuracy, a flickering central checkerboard stimulus was alternated with a
flickering checkerboard surround (see Data analysis for the rationale
for this choice). This stimulus is referred to as the “ROI definition
stimulus”.
The stimulus and its time course are shown in Fig. 1C. The
checkerboard had a high contrast and the frequency of contrast reversal was 8 Hz. The dimensions of the center and surround were the
same as in the main experiments.
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A. L. WILLIAMS, K. D. SINGH, AND A. T. SMITH
conditions (Fig. 3C–F), “activation” (better thought of as temporal modulation of activation in this case) reflects the effect of the appearance of
the surround on activity in the center, since the center stimulus itself is
continuously present and gives no modulation. As expected, these conditions show less systematic variation than the control conditions. What
there is tends to be negatively correlated with the correlation waveform,
i.e., it reflects suppression by the surround, rather than facilitation.
Figure 4 summarizes the results, averaged across subjects. Figure 4,
left, shows the results in terms of SCA. The control condition gives a
large positive response. A grating surround of the same orientation,
contrast, and spatial frequency as the center (the parallel surround
condition) causes marked suppression of activity. When the surround
grating is orthogonal in orientation, however, this suppression is
absent. An ANOVA showed that the difference between the parallel
and orthogonal conditions was statistically significant: F(1,12) ⫽
5.99, P ⬍ 0.05. Figure 4, right, shows the same results expressed as
a percentage of the activation produced by the center grating itself
(control condition). It shows that, for a parallel surround, the suppression is about 28%.
These results reflect activity in several visual areas (at least V1, V2,
and V3). It is therefore possible that they mask important differences
between these areas. Estimating the positions of the boundaries on the
basis of retinotopic mapping data (see Fig. 2) and analyzing the areas
separately suggests that the results are similar in all areas. However,
the reliability of these estimates is low in the fovea because of
corruption of temporal phase data by fixation instability.
Experiment 2: Effects of peripheral viewing
and spatial phase
In this experiment, we investigate two separate factors that may
influence the magnitude of the surround suppression that we report in
Experiment 1.
First, we examine the importance of retinal location. Xing and
Heeger (2000) have recently reported that the reduction of the perFIG. 2. A: stimulus-correlated activation produced by the ROI definition
stimulus (see Fig. 1C) shown as a pseudocolor overlay on a computationally
flattened representation of the occipital cortex of 1 hemisphere in 1 subject.
Flatmap shows a circular patch of cortex of radius 45 mm. Hue (see key)
represents stimulus-correlated activation (see text for definition). The region
activated by the center stimulus (flickering checkerboard) appears as red/
orange and that produced by the surround (flickering checkerboard presented
in the opposite temporal phase) appears as blue/purple. Color saturation
represents the correlation coefficient, so that the most highly correlated voxels
are the most prominent. Boundaries of V1 and V2, obtained from separate
retinotopic mapping experiments, are also shown. Strong activity is seen in the
first three visual areas. The relatively inactive area at the bottom of the flatmap
is the lateral occipital cortex. B: same flatmap as A after thresholding to remove
all voxels whose activation is negative and also those that are positive but have
a P value ⬍ 0.01. All that remains is a red/orange patch, which was used to
define the representation of the central stimulus for purposes of quantitative
measurement. C: same flatmap, showing an illustrative result from Experiment
1 (effect of parallel grating annulus). Again, hue represents stimulus-correlated
activation and saturation reflects correlation. The surround region shows strong
positive activation reflecting the appearance of the surround stimulus; central
region shows negative activity, reflecting suppression of the response to the
invariant central stimulus by the surround. D: corresponding result for an
orthogonal surround. The central suppression is now weak or absent. E:
flatmap from a different subject covering a larger area (radius 65 mm) showing
results obtained with peripheral stimulus presentation in Experiment 2. The
data are from the ROI definition condition. In V1, 2 distinct representations of
the center stimulus can be seen as red/orange patches, one in each of the two
quadrants (top and bottom) represented in the hemisphere shown. Further
representations can be seen in V2d and V3, each of which represents one
quadrant of the visual field, but these are less reliable and less circumscribed.
In this example, activation is strong in V2d and V3, but not discernable in V2v
or V3A and weak in VP and V4. F: the flatmap shown in E with colored
overlay showing the effect of a parallel surround grating on a peripherally
presented center grating. The two gratings had the same spatial phase.
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annulus had the same spatial frequency and contrast but could be
either horizontal (parallel to the center stimulus) or vertical (orthogonal). The spatial phase relationship between the two gratings was
randomized. The central grating was present continuously, while the
surround repeatedly appeared for 15 s and then disappeared for 15 s.
The background was unpatterned and its luminance was the same as
the mean luminance of the gratings.
Within a single scanner session, each of the two types of stimulus
presentation (parallel and orthogonal surround grating) was repeated
at least three times and the results averaged, so as to obtain accurate
estimates of the effect of the surround. Control runs and ROI definition runs (see Visual stimulation) were also conducted. This first
experiment, which was long and required sustained motivation, was
conducted on the three authors and one experienced volunteer only.
In each hemisphere of each subject, an ROI corresponding to the
cortical representation of the center stimulus was defined using the
thresholding method. For each repetition of each of the two main
experimental conditions (parallel and orthogonal surround), the mean
activation in the central region was calculated and the results were
then averaged across the three or four identical runs. Activations for
the control condition were obtained using the same ROI. Data from
one hemisphere had to be discarded due to signal dropout.
Figure 3 shows sample BOLD time courses for one subject along with
the waveform used for correlation with the data. In the ROI definition and
control conditions (Fig. 3, A and B), activation simply reflects the appearance of the center grating. These conditions gave relatively large
(about 2 and 1%, respectively) signal changes that were correlated with
the stimulus profile (dotted lines). In the parallel and orthogonal surround
EFFECTS OF VISUAL CONTEXT IN HUMAN VISUAL CORTEX
529
ceived contrast of a central grating target caused by a surrounding
grating is much greater when the stimuli are presented in the peripheral visual field (eccentricity 10°) than when presented in the center.
We therefore repeated our experiments with peripheral presentation of
the stimuli.
Second, the fact that we randomized the spatial phase relationship
of the center and surround gratings in Experiment 1 may be important.
Several studies have reported that spatial phase has no effect on
suppression (e.g., Solomon et al. 1993; Xing and Heeger 2001; Zenger
and Sagi 1996) and it was on this basis that we randomized phase in
Experiment 1. But other studies have found phase to be important. In
an early study, Ejima and Takahashi (1985) reported that, when a
target grating was in phase with two flanking gratings, facilitation was
seen for low surround contrasts and suppression was seen for high
contrasts. When they were in opposite phases, only suppression was
seen and it tended to be less marked. More recently, Olzak and
Laurinen (1999) measured perceived contrast of a center grating
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stimulus as a function of surround contrast and phase. They found that
perceived contrast was reduced when the surround was in phase but
not when it was in antiphase, although with plaid stimuli they found
suppression in both phase relations. In view of the latter studies, and
the substantial variability observed in our results with random phase,
we studied two fixed phase relations separately in Experiment 2.
In a single imaging session, we separately presented circular gratings in the foveal and peripheral visual field. These were surrounded
by parallel gratings that were either in the same spatial phase as the
target or in the maximally different phase (180°). The contrasts of the
center and surround gratings were both 25%. There was minimal
separation between the two zones and so the in-phase stimulus appeared as a large, almost undifferentiated patch while the antiphase
stimulus had a clearly demarcated center. We also presented control
stimuli and ROI definition stimuli similar to those used in Experiment
1 but appropriately adjusted in size, location, and spatial frequency.
Different stimulus sizes and grating spatial frequencies were used
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FIG. 3. Typical BOLD time courses from one subject
in Experiment 1. A—D: normalized T2*-weighted signal
averaged across the voxels in the region of interest
representing the central stimulus (solid lines), which is
expressed as percentage signal change, relative to the
mean over the time period in the region of interest as a
whole. Also shown (dotted lines) is the ideal waveform
used for correlation with the observed response profile.
A: stimulus was the ROI definition stimulus (Fig. 1C)
and the activation has a high amplitude and is highly
correlated with the ideal waveform. B: control stimulus
was used and the profile is similar but of lower amplitude. C and D: central stimulus was invariant and any
stimulus-correlated change is due to the influence of the
surround on the central region of interest, the response is
weak but tends to be negatively correlated with the ideal
profile, reflecting suppression, particularly in the case of
the parallel surround. E and F: same data as shown in C
and D after averaging across the 8 stimulus cycles.
Again, the dotted line is the theoretical response for the
surround grating, which appears after 15 s. For a parallel
surround (E), the response for the central ROI shows a
weak negative correlation (about ⫺0.5% signal change)
but for an orthogonal surround there is very little correlation. The SE bars relate to the 8 stimulus cycles.
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A. L. WILLIAMS, K. D. SINGH, AND A. T. SMITH
FIG. 4. Mean results of Experiment 1, averaged
across subjects. Left: difference between the two
phases of the block design in terms of stimuluscorrelated activation (SCA, see text). The control
stimulus (the central patch itself) gives a large, positive response. The modulation of this response
caused by a surround is negative for a parallel (isoorientation) surround grating and near zero for an
orthogonal surround. Right: same data expressed as
suppression/facilitation ratios. Positive values on the
right ordinate reflect facilitation and negative values
reflect suppression. Results are averaged across 7
hemispheres in 4 subjects, each of whom underwent
repeated measurements. Error bars ⫾ SE.
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in the foveal and peripheral conditions. There were two reasons for
this. First, the cortical magnification factor (cortical extent in mm per
degree of visual angle) falls sharply with increasing eccentricity. As a
result, a given visual stimulus produces a much smaller area of
activation on a cortical flatmap if presented in the periphery than in
the fovea. It is therefore necessary to use a large stimulus in the
periphery so as to obtain an active ROI large enough to give activation
measurements with an acceptable signal-to-noise ratio. Second, spatial frequency sensitivity varies with eccentricity and we wished to
compare stimuli of like sensitivity. Consequently, it was desirable to
scale the peripheral stimulus in spatial frequency as well as size. The
number of spatial cycles in the central and surround zones was held
constant and the entire stimulus was scaled.
In foveal presentation conditions, the grating spatial frequency was
1.5 c/°, the center diameter was 2°, and the width of the annulus was
1°. The fixation spot was in the middle of the center grating, as in
previous experiments. In the peripheral presentation condition, the
grating spatial frequency was 0.375 c/°, the center diameter was 8°,
and the width of the annulus was 4°. The stimulus eccentricity was 7°.
The stimulus was presented in one quadrant of the visual field (i.e.,
offset from the fixation point both horizontally and vertically). To
obtain the best estimate of surround modulation, four center gratings
were presented simultaneously, one in each quadrant, each with its
own surround (the surrounds partially overlapped). Each center region
was located on the flatmap and analyzed separately and then the four
results were averaged. Seven subjects were tested.
A typical result for peripheral presentation is shown as a color
overlay on a flatmap in Fig. 2, E and F. Within V1, two active regions
can be seen in the ROI definition condition (Fig. 2E), reflecting the
center stimuli in the upper and lower quadrants of the hemifield
represented. Further active regions can be seen in V2 and V3. Activation was measured in these regions, defined using the thresholding
procedure used in Experiment 1. Figure 2F shows the result obtained
in the main experiment, using center and surround gratings in the
same spatial phase, for the flatmap shown in Fig. 2E.
Figure 5 shows quantitative results for all conditions, averaged
across 14 hemispheres and including all visual areas up to V3. In Fig.
5A, the results are shown in terms of suppression/facilitation ratios, as
in Fig. 4, right. For foveal presentation, there is a very large (76%)
suppressive effect when the center and surround stimuli are in phase,
but this completely disappears when the stimuli differ in phase by
180°. This is broadly consistent with Fig. 4, in which suppression is
about 28% with phase randomized and strongly suggests that spatial
phase is indeed important for contextual modulation of this kind. For
peripheral presentation (Fig. 5A, right), the results are quite different.
In-phase stimuli give only modest suppression and antiphase stimuli
FIG. 5. A: results for Experiment 2 expressed as suppression/facilitation
ratios. Left: mean suppression ratios resulting from a parallel (isooriented)
grating surround in each of two spatial phases, with central fixation. B: results
for Experiment 2 expressed as activation levels. Left (foveal presentation) and
right (eccentric presentation): same data as the left and right in A, together with
activations obtained in the control and ROI definition conditions (see text).
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EFFECTS OF VISUAL CONTEXT IN HUMAN VISUAL CORTEX
DISCUSSION
The results described in this paper reflect a preliminary
attempt to study the effects of surround stimuli on the neural
activity evoked in human visual cortex by a small target
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stimulus, using fMRI methods. Using a simple, circular sine
grating stimulus to evoke a BOLD response and a restricted set
of surround gratings, we have demonstrated suppression of
activity by a surround stimulus and, in one case, facilitation.
Explorations of contextual effects of this kind in the realm of
both perception (changes in detection thresholds and in perceived contrast) and single-unit neurophysiology are very
much more comprehensive than our study and yield a rather
complex picture, suggestive of an interplay of several different
mechanisms with different properties (e.g., Polat 1999). We
have merely sampled the resultant of these influences in a very
limited set of stimulus conditions. However, our results show
that contextual effects can be studied using fMRI methods,
because activity arising from the target, activity arising from
the surround, and modulatory effects of the surround on the
target can all be distinguished and measured separately. This
opens a new avenue for exploring what is increasingly seen as
a fundamentally important aspect of visual function.
Relation to other studies
There are obvious parallels between our results and the
various studies of detection thresholds, perceived contrast, and
single-unit responses reviewed earlier. If we take the view that
reduced activation as measured by blood oxygenation reflects
reduced neural activity (see Relationship between fMRI and
neuronal activity), the results can be compared directly.
Our two main findings are 1) that surround effects are
predominantly suppressive and 2) that such effects are tuned
for orientation. Both phenomena have been demonstrated
clearly in single neurons, both in area 17 of the cat (e.g., Li and
Li 1994; Nelson and Frost 1978) and in area V1 of the macaque
monkey (e.g., Jones et al., 2001; Levitt and Lund 1997).
Likewise, both results have been found repeatedly in the realm
of psychophysics (e.g., Cannonand Fullenkamp 1991; Ejima
and Takahashi 1983; Xing and Heeger 2000).
A third finding of our study is that suppression appears to
give way to facilitation as stimulus eccentricity increases (Fig.
5). There are several reports of facilitation in single units (e.g.,
Gilbert and Wiesel 1990; Sillito et al., 1995), although they are
less frequent and are more controversial (e.g., Walker et al.,
1999) than reports of suppression. This state of affairs is
paralleled by the fact that suppression is the norm in our own
data. We know of no physiological evidence that facilitation
increases with stimulus eccentricity, although surround effects
do not appear to have been studied as a function of receptive
field eccentricity in the context of single neurons. In terms of
psychophysics, there also several reports of facilitation (e.g.,
Ejima and Takahashi 1985; Tanaka and Sagi 1998), but, again,
few studies in which stimulus eccentricity was manipulated.
Our results do not mirror those of Xing and Heeger (2000),
who report that suppression of perceived contrast is increased,
not reduced, in the periphery.
A fourth finding is that suppression occurs when the surround is in the same spatial phase as the center but not when it
is in the opposite phase. This closely mirrors the effects of
phase on perceived contrast found by Olzak and Laurinen
(1999).
A recent attempt to summarize and model the perceptual
effects of surround stimuli on the perceived contrast of gratings
has been provided by Xing and Heeger (2001). Although that
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give a marked (24%) facilitation. Thus there appears to be a marked
shift from suppression to facilitation when moving from the fovea to
the periphery. A two-way ANOVA shows that the effects of location
(central versus peripheral; F(1,52) ⫽ 9.67, P ⬍ 0.003) and spatial
phase (F(1,52) ⫽ 23.5, P ⬍ 0.0001) are both statistically significant.
When peripheral stimuli are used, the different visual areas (V1,
V2, etc.) are easier to distinguish than when foveal stimuli are used.
This is because 1) fixation instability blurs the areal boundaries more
in the fovea than in the periphery because of greater cortical magnification and 2) a foveal stimulus fills each quadrant (at low eccentricities) so there is no gap between its representations in adjacent areas.
In some subjects, we were able to discern distinct peripheral activations in some or all of V1, V2d, V2v, V3, and VP (see Fig. 2E). But
we were unable to do this in enough cases to obtain reliable data for
all visual areas. We therefore used a region of interest that encompassed all areas in which activity was evident, as in Experiment 1.
Where distinct activations were evident, the thresholding method,
used to define the representation of the center stimulus, picked out and
summed the different activations, excluding the inactive zones separating them. Additional measurements of the separate areas were
made in cases in which this was feasible. Based on these cases, the
magnitude and stimulus specificity of suppression and facilitation
appear to vary little among the retinotopic visual areas up to V3.
In interpreting the difference between foveal and peripheral presentation, it is instructive to look at the raw activation levels, which
are shown in Fig. 5B. For foveal presentation, the control stimulus
yields about 27% of the activation produced by the ROI definition
stimulus. This figure is closely consistent with the result (23%)
obtained in Experiment 1 and presumably reflects the lower contrast
and the single orientation and spatial frequency of the control stimulus
compared with the ROI definition stimulus. But for peripheral presentation, the control stimulus gives a much higher activation, while
ROI definition gives only slightly higher activation, leading to a much
higher ratio of 87%. This difference is consistent across subjects. The
reason for it is open to debate, but given that (in Fig. 5A) suppression/
facilitation is calculated as a percentage of the response to the center
stimulus alone, the high control activation has consequences for
calculating suppression. In terms of raw activation levels (Fig. 5B),
the difference between foveal and peripheral surround suppression
looks rather less dramatic, particularly in the 0° case. However, the
appearance of facilitation (peripheral presentation, 180° phase) cannot
be explained away, since facilitation, as well as suppression, would be
reduced (as a percentage) by an increased response to the control
stimulus.
It should be borne in mind that four “centers” (targets) were
presented simultaneously in the peripheral presentation condition, so
as to obtain a separate measurement from each quadrant of the visual
field and so as to maximize the number of measurements obtained
from the dataset. It is possible that these center stimuli interacted with
each other, each contributing surround modulation to the others,
despite their spatial separation. On the face of it, a larger surround
should (if anything) increase the magnitude of any suppressive effect
observed with a smaller surround. But there is some evidence that
suppression is associated with near surrounds and facilitation with
more distant surrounds (Polat 1999), which might explain the observed shift toward facilitation with peripheral viewing. It should also
be borne in mind that the different visual areas (V1, V2, and V3) were
activated patchily in the peripheral condition (see Fig. 2, E and F), so
it is possible that the weighting of the contributions from the different
areas may be slightly different in the foveal and peripheral conditions.
531
532
A. L. WILLIAMS, K. D. SINGH, AND A. T. SMITH
demand arises principally in synapses, so that inhibition is
expected to increase oxygen consumption, in practice, levels of
excitation and inhibition tend to track each other, with the
result that the BOLD response reflects spike count fairly accurately. Likewise, Rees et al. (2000) have provided empirical
evidence that the BOLD response is directly related to spike
count in visual area V5. Boynton et al. (1999) have argued that
fMRI activation is closely correlated with contrast and that this
in turn is related to spike count. Logothetis et al. (2001)
themselves found an extremely high correlation between local
field potentials and spiking output when stimulus contrast was
varied. Thus, in many cases, it may be sufficient to assume that
inputs and outputs, synaptic activity and spikes, excitation, and
inhibition are all highly correlated with each other. Obviously
the correlation cannot be perfect or no processing could occur,
but the difference may be too subtle to matter at the current
stage of development of fMRI. Unfortunately, to the extent that
the correlation is imperfect, it may be phenomena such as
surround suppression that will most reflect the difference.
Arguably, the fact that our BOLD signals mostly decrease in
circumstances in which single-unit activity is typically reduced
suggests that inhibition reduces, rather than increases, the
BOLD signal.
Relationship between fMRI and neuronal activity
Mechanisms of surround modulation
The interpretation of our results is predicated on the assumption that a change in the BOLD response measured in fMRI
experiments is tightly coupled to the level of neural activity in
the region measured. This is controversial, although it is becoming less so, and the debate is now moving toward which
aspects of the neural response are reflected in the BOLD
response (Logothetis et al. 2001). Of particular importance
here, since suppression is suggestive of inhibition from neurons responsive to the surround, is the question of whether
inhibitory synaptic activity reduces the BOLD response (because it reduces net activity) or increases it (because it makes
metabolic demands, including consumption of oxygen). Logothetis et al. (2001) have suggested that BOLD reflects neural
input and intracortical processing rather than the spiking output
of neurons. But their conclusion is based on a correlation with
the spectral power of local field potentials, which could perhaps be changed in either direction by inhibition. Scannell and
Young (1999) have argued that, although neural metabolic
Of prime interest is the origin and purpose of the modulatory
signals whose influence is evident in changes in perceived
contrast and fMRI signal. Various purposes have been suggested, including low-level operations such as contrast gain
control and more sophisticated processes such as object segmentation. Some have suggested that multiple mechanisms
may be involved (e.g., Ido et al. 2000). An important clue to
their nature must lie in the extent to which interactions are local
(intracortical horizontal connections) or involve feedback to
the visual cortex from higher cortical areas. Several studies
suggest the latter. Zipser et al. (1996) recorded responses from
monkey V1 neurons and found that facilitatory contextual
modulation appears only after 80 –100 ms, suggesting feedback
from other areas. Similarly, Hupé et al. (1998) showed that
cooling MT in monkeys reduces the influence of context on
responses to moving bars in V1–V3. At the same time, some
cortical interactions may well be local. Certainly contextual
effects are sufficiently complex to support more than one
J Neurophysiol • VOL
Influence of adaptation effects
In our experiments, the center stimulus that provides the
substrate for contextual modulation is present continuously.
Inevitably, adaptation occurs during the measurement period,
resulting in reduced perceived contrast and possibly reduced
cortical activation. The quantitative accuracy of our data could
be compromised by this fact. However, any such effects can
only be secondary. A fall in stimulus-related activity will have
no effect on activation as we measure it, since we measure only
modulation that is correlated with the appearance of the surround. Only if the modulatory effect of a surround varies with
the adaptation state of the recipient cortical region will our
measurements be affected. This is quite possible, but any such
effects should be similar in all conditions, since we used
similar center stimuli throughout.
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study is perhaps no more definitive than any other, it does
present a coherent picture and there are many commonalities,
both between their stimuli and ours and between their perceptual results and our fMRI findings. In line with previous
authors, they find a predominance of suppression, but facilitation by low-contrast surrounds. Suppression is markedly reduced when the center and surround gratings are orthogonal.
The only substantial difference between their perceptual results
and our neuroimaging data is that they find no effect of the
spatial phase of parallel center/surround gratings, whereas we
find a marked effect (Experiment 2). Interestingly, however,
they suggest a way of resolving the conflict in the literature on
this point. Their stimuli had a small gap between center and
surround, so that the two zones were always clearly demarcated, and they suggest that this may be important since previous studies reporting an effect of phase have not used a gap.
It may be that when the combined stimulus is perceived as a
single grating (in-phase stimuli), global or high-level factors
come into play, giving a different result. One possibility is that
when the two stimuli are not separated, phase-dependent
brightness induction effects occur (Ejima and Takahashi 1985;
Yu et al. 2001). It should be noted that in both our study and
that of Xing and Heeger (2001), the surround was close to the
center and had a limited spatial extent. At least one study (Polat
1999) suggests that, while local interactions may be predominantly suppressive, facilitation is the norm when there is a
large separation between target and inducers.
Press et al. (2001) have recently reported fMRI results that
are equivalent to one of our conditions, namely foveal stimulation with a parallel surround in the same spatial phase as the
center stimulus. They measured spatial summation, i.e., they
defined a small region of interest and stimulated it with patches
of grating of various sizes. They report that, in V1, V2, and V3,
extending the stimulus beyond the measured region resulted in
60 –90% suppression but that, in V3A, V3B, and V7 there was
no such suppression. It is not clear how reliably they separated
these areas in the foveal representation, which we did not
attempt. But our results, in which we pooled the retinotopic
areas and obtained ⱕ76% suppression with in-phase stimuli, is
in line with the mean of their results.
EFFECTS OF VISUAL CONTEXT IN HUMAN VISUAL CORTEX
mechanism and purpose. Because of poor temporal resolution,
fMRI data do not enable us to study feedback-related delays
and so other strategies will be required.
This work was supported by a research grant to A. T. Smith and K. D. Singh
from the Wellcome Trust. We are grateful to Prof. Neil Roberts, University of
Liverpool, for arranging scanner access.
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