Falkner et al. (2010) Surround suppression sharpens the priority map in the lateral intraparietal area

Falkner et al. (2010) Surround suppression sharpens the priority map in the lateral intraparietal area
The Journal of Neuroscience, September 22, 2010 • 30(38):12787–12797 • 12787
Behavioral/Systems/Cognitive
Surround Suppression Sharpens the Priority Map in the
Lateral Intraparietal Area
Annegret L. Falkner,1,5* B. Suresh Krishna,1,5,6* and Michael E. Goldberg1,2,3,4,5
1
Mahoney Center for Brain and Behavior, Department of Neuroscience, and Departments of 2Neurology, 3Psychiatry, and 4Ophthalmology, Columbia
University College of Physicians and Surgeons, and 5New York State Psychiatric Institute, New York, New York 10032, and 6Bernstein Center for
Computational Neuroscience and German Primate Center, Goettingen, Germany 37077
In the visual world, stimuli compete with each other for allocation of the brain’s limited processing resources. Computational models
routinely invoke wide-ranging mutually suppressive interactions in spatial priority maps to implement active competition for attentional
and saccadic allocation, but such suppressive interactions have not been physiologically described, and their existence is controversial.
Much evidence implicates the lateral intraparietal area as a candidate priority map in the macaque (Macaca mulatta). Here, we demonstrate that the responses of neurons in the lateral intraparietal area (LIP) to a task-irrelevant distractor are strongly suppressed when the
monkey plans saccades to locations outside their receptive fields. Suppression can be evoked both by flashed visual stimuli and by a
memorized saccade plan. The suppressive surrounds of LIP neurons are spatially tuned and wide ranging. Increasing the monkey’s
motivation enhances target– distractor discriminability by enhancing both distractor suppression and the saccade goal representation;
these changes are accompanied by correlated improvements in behavioral performance.
Introduction
In the visual world, stimuli are in constant competition for allocation of the brain’s limited processing resources. Salient stimuli
are often not relevant to the task at hand, but can nevertheless
transiently capture attention and result in disadvantageous behaviors (Egeth and Yantis, 1997; Bisley and Goldberg, 2003b;
Peck et al., 2009). For example, a jungle predator may have difficulty monitoring his elusive prey when there is a distracting insect
flying in his field of view. It would be disadvantageous for this
predator to lose focus on the location of the prey, either through
an eye movement or a shift of attention to the location of the
insect. Human subjects can reduce the capture of attention by an
abruptly appearing, task-irrelevant stimulus by attending to a
different, task-relevant location before the distractor appears
(Egeth and Yantis, 1997). This reduction in attentional capture
could be achieved in the brain by enhancing the neural activity
encoding the location of the task-relevant stimulus or by suppressing the neural activity associated with the location of the
task-irrelevant stimulus. In principle, an efficient neural strategy
Received May 6, 2010; revised July 19, 2010; accepted July 22, 2010.
M.E.G. was supported by National Eye Institute Grants R24EY015634, R01EY01497, and R01EY017039, and the
Kavli, Keck, Dana, and Zegar Foundations. A.L.F. was supported by the National Science Foundation Graduate
Research Fellowship and the Ruth L. Kirschstein National Research Service Award. B.S.K. was supported by the
German Ministry for Education and Science Grant BMBF 01GQ0433 to the Bernstein Center for Computational
Neuroscience, and by a Gatsby Foundation award. We are grateful to Drs. Mo Osman, Moshe Shalev, and Girma
Asfaw for veterinary care, Yana Pavlova for veterinary assistance, John Caban for machining, Glen Duncan for
electronics, and Latoya Palmer for facilitating everything.
*A.L.F. and B.S.K. contributed equally.
Correspondence should be addressed to either of the following: Annegret L. Falkner, 1051 Riverside Drive, Unit
87, New York, NY 10027, E-mail: alf2111@columbia.edu; or B. Suresh Krishna, German Primate Center, 4 Kellnerweg, 37077 Goettingen, Germany, E-mail: skrishna@dpz.eu.
DOI:10.1523/JNEUROSCI.2327-10.2010
Copyright © 2010 the authors 0270-6474/10/3012787-11$15.00/0
might incorporate both mechanisms simultaneously, though
how such interactions occur is not yet understood.
Many models of attentional and saccadic processing posit that
the allocation of visual attention and the selection of saccade
targets are both based on the dynamically evolving peak of activity in a map-like representation of spatial priority (Schall, 1995;
Gold and Shadlen, 2000; Itti and Koch, 2000; Fecteau and Munoz,
2006; Goldberg et al., 2006; Serences and Yantis, 2007; Armstrong
et al., 2009). Current evidence suggests that such priority-map
representations exist in several interconnected brain regions, including the lateral intraparietal area (LIP), the frontal eye field
(FEF), and the superior colliculus (SC) (Keller and McPeek,
2002; Thompson and Bichot, 2005; Goldberg et al., 2006). It is
commonly theorized that different spatial locations on this map
mutually suppress each other over large distances to facilitate the
evolution of a clear peak of activity that can serve as the focus of
visual attention and select the target for saccadic eye movements
(Koch and Ullman, 1985; Itti and Koch, 2001; Deco et al., 2002;
Constantinidis and Wang, 2004). Such mutual suppression is
also considered crucial for maintaining a localized and persistent
focus of attention that is resistant to abruptly appearing distractors (Constantinidis and Wang, 2004; Wong et al., 2007), and for
the programming of sequential saccades (Xing and Andersen,
2000). Long-ranging interactions across the priority map may
also be necessary for the global computations of relative reward
value that are known to affect the priority map in LIP (Dorris and
Glimcher, 2004; Sugrue et al., 2004).
Despite this theoretical interest, suppression has never been
explicitly studied in LIP (or any other priority map area), and its
very existence is controversial. Surround suppression has been
postulated to explain the decrease in activity with increasing set
size in a visual search task (Balan et al., 2008), but it has also been
Falkner et al. • Surround Suppression, Motivation, and the LIP Map
12788 • J. Neurosci., September 22, 2010 • 30(38):12787–12797
A
C
B
D
E
F
Figure 1. Task design. A, Target-mapping task: monkeys fixated for 500 ms, after which a target appeared at a location randomly chosen from a 40 ⫻ 40° grid of locations in the visual field, with
5° spacing in most cases (C). After 500 ms, a distractor was flashed briefly (⬍50 ms) at the RF center. After a 550 ms delay, the fixation spot was turned off, and the monkey made a saccade to the
target to obtain the reward. B, The no-saccade control task was otherwise identical, except that the fixation spot was never turned off, and monkeys maintained fixation throughout the trial to obtain
the reward. C, Grid of potential target locations. D, Suppression of example LIP neuron by a saccade plan to the surround. Grayscale map of response to the distractor (average firing rate from 30 to
300 ms after distractor onset) as a function of saccade target location with respect to the central fixation point. Target locations with yellow/cyan dots are significantly suppressed (yellow) or
enhanced (cyan) relative to the no-saccade control ( p ⬍ 0.05, t test with Bonferroni correction for 80 simultaneous comparisons). Boxed locations indicate saccade target locations defined as the
RF (magenta) and Smax (red) for the rasters and PSTHs in E. X at ⫺20, 20 indicates distractor location. E, PSTHs and rasters from the example neuron, aligned to distractor onset: saccade plan to the
Smax leads to a reduced distractor response (red) compared to both the no-saccade control response (blue) and the response when saccade is planned to the RF (magenta). Rasters are sorted by trial
type. Dashed vertical lines indicate time of saccade target onset (left), distractor onset (middle), and time of saccade go-cue (right). F, Distractor response varies with distance of saccade target from
the RF center. An example neuron’s distractor response during the target-mapping task (minus the response during the no-saccade control, horizontal dashed line at 0) is plotted as a function of the
distance between the saccade target and the RF center. Error bars show SEMs (n ⫽ number of locations contributing to each data point).
recently argued that LIP has no surround suppression (Churchland
et al., 2008). In this study, we demonstrate that the priority map
in LIP is, in fact, powerfully influenced by surround suppression.
Surround suppression in LIP possesses novel properties that have
not been demonstrated before in other visual areas.
Materials and Methods
We used three male rhesus monkeys (Macaca mulatta) weighing 8 –12 kg
in this experiment. All experimental protocols were approved by the
Animal Care and Use Committees at Columbia University and the New
York State Psychiatric Institute, and complied with the guidelines established by the Public Health Service Guide for the Care and Use of Laboratory Animals. We located the intraparietal sulcus in each monkey using
a T1 volume scan obtained on a GE Signa 1.5 T magnet. Using standard
sterile surgical techniques and endotracheal isoflurane general anesthesia, we made a 2 cm trephine hole over the intraparietal sulcus and
implanted 12–16 titanium screws in the monkey’s skull and used them to
anchor an acrylic cap in which we placed a head-holding device, the
recording chamber, and the plug for subconjunctival search coils for eye
position recording. We used three recording cylinders: (monkey D, left
hemisphere; monkey I, right hemisphere; monkey Z, right hemisphere).
Data collection and task design. We used the REX/MEX/VEX system
developed at the National Eye Institute’s Laboratory for Sensorimotor
Research for behavioral control, visual stimulus display and data collection using Dell Optiplex PCs running QNX (REX and MEX) and Win-
dows 2000 (VEX). The monkeys sat in a dimly illuminated room with their
head fixed and viewed a screen that stood 75 cm away. Visual stimuli were
back-projected onto the screen using a LCD projector (Hitachi CP-X275)
with a refresh rate of 75 Hz. We used a photodiode to register the actual times
for stimulus onsets and offsets. Fixation point and saccade target stimuli
were 0.3°-wide colored squares and distractors were 1.5°-wide white squares.
We introduced the electrodes through a guide tube positioned in a 1 mm
grid (Crist Instrument). We recorded single units from area LIP with glassinsulated tungsten electrodes (Alpha Omega Engineering) while the monkeys performed a passive fixation task as white spots flashed sequentially at
different locations in the visual field. We amplified, filtered, and discriminated action potentials using an amplitude window discriminator (MEX
software). Only well isolated single neurons were studied.
We considered neurons to be in LIP if they showed consistent visual,
delay-period, and/or saccade-related response during the memoryguided saccade task or were located between such neurons in that electrode penetration. Of 98 neurons tested, 52 (53.06%) responded
significantly more during the delay period of a memory-guided delayed
saccade task (t test, one-tailed p ⬍ 0.05, average of 49.84 trials per neuron) than at baseline. Every neuron responded to the abrupt onset of a
visual stimulus in its receptive field (RF).
Task details. For each neuron we isolated, we identified the center of
the RF using flashed spots at 400 ms intervals (4 per trial, located on a
40 ⫻ 40° grid with 5° spacing, ⬍50 ms duration) during passive fixation
(Fig. 1C). We defined the center of the RF as the spatial location of the
Falkner et al. • Surround Suppression, Motivation, and the LIP Map
flashed spot that elicited the maximum activity. We then ran a nosaccade control, where the monkeys fixated a central red fixation spot for
2050 ms. One thousand milliseconds after the monkey achieved fixation,
a brief white spot flashed for ⬍50 ms (2–3 video frames in 90% of trials;
1 video frame on the remaining trials) in the center of the RF. The
duration of the distractor was independent of all other task parameters,
including stimulus locations, timing, and reward size. The no-saccade
control was identical to the target-mapping task (below), except that no
saccade target appeared and the monkey had to maintain fixation
throughout the trial to get his reward. After ⬃50 trials of the no-saccade
control task, we had the monkey perform several variants of the delayed
saccade paradigm. We ran each task only on a subset of neurons, depending on the neuron’s isolation quality and the monkey’s satiety.
The target-mapping task began with the appearance of a central red
fixation spot; 500 ms after the monkey fixated the central spot, a saccade
target appeared at a location randomly chosen from 80 possibilities (on a
40 ⫻ 40° grid with 5° spacing). Occasionally, for some neurons, we
sampled from a slightly different set of locations, varying either the sampling or the spatial extent of the grid to more closely sample particular
regions of space or to ensure sufficient data collection within the limited
recording time available. A distractor flashed briefly for ⬍50 ms (two or
three video frames in ⬃90% of trials) at the center of the RF 500 ms after
the saccade target appeared. When the center of the RF coincided with
one of the 80 target locations, the distractor flashed on top of the (much
smaller) saccade target. The fixation spot disappeared 550 ms after distractor onset; this was the cue for the monkey to make the saccade (gocue). Monkeys had to keep their eyes within a 3 ⫻ 3° window until the cue
to make the saccade appeared. The mean SD of eye position during the
fixation period was ⬍0.25° for all sessions. Monkeys had 400 ms after the
go-cue to make a saccade to a 4.5 ⫻ 4.5° window around the saccade goal.
If the monkey’s eye was in the window for 100 ms from 400 to 500 ms
after the go-cue, he received a drop of water or juice as reward. In ⬍5% of
randomly interleaved trials on this task, no saccade target appeared and
the monkey was rewarded for maintaining fixation throughout the trial
(interleaved no-saccade control). The distractor-mapping task was similar to the target-mapping task, except that the saccade target location
was fixed at the RF center while the distractor location was varied over a
40 ⫻ 40° grid. In another task variant of the target-mapping task, we also
had the monkey make a memory-guided saccade to an effective location
in the suppressive surround, while the distractor appeared at the RF
center (⬃75 trials). We typically used this task after ⬃500 trials on the
target-mapping task, after which an effective location could be identified.
Finally, we measured neuronal properties on the cued-reward task,
where we cued either a large or a small reward randomly on each trial by
the saccade target color. For most neurons, we first ran a control task
where the saccade target could be one of two different colors, but each
was associated with the same reward (⬃50 trials with distractor at RF
center and saccade to suppressive surround, and ⬃50 trials with saccade
to RF center and distractor in the suppressive surround). Next, the monkeys performed the cued-reward task, where the two chosen saccade
target colors was associated with different reward sizes. In the first block,
the distractor appeared at the RF center and the saccade was made to the
suppressive surround (⬃200 trials) and in the second block, the saccade
was made to the RF center and the distractor appeared in the suppressive
surround (⬃50 trials). Actual reward magnitudes were chosen daily
based on the monkey’s satiety level and his behavioral sensitivity to the
difference in reward sizes. The reward ratio between small and large
rewards was ⬃1:6 on average, and ranged from 1:3 to 1:10 for all but two
neurons (for which we used higher ratios of 1:20 and 1:50, respectively).
The apparently large range of reward ratios is explained by the fact that
ratios are very sensitive to changes in the denominator when the denominator is small.
On a given trial, the monkey’s eye had to remain within a 4.5 ⫻ 4.5°
window around the saccade goal from 400 to 500 ms after the go-cue for
reward delivery. The monkey’s eye usually entered this window with the
first saccade after the go-cue: for example, in the cued-reward task, in
96.5% of trials, the first saccade after the go-cue landed within this window. Counting only saccades at least 1.5° in amplitude, the monkeys
J. Neurosci., September 22, 2010 • 30(38):12787–12797 • 12789
usually made only one (92.9%) or two (6.8%) saccades during the period
between the go-cue and the reward.
Data analysis. All data analysis programs were written in MATLAB
(MathWorks). For the target-mapping task, we verified that a given saccade target location lay outside the RF by comparing the response to the
onset of the saccade target to the pretarget response (response 30 –230 ms
after target onset compared to response ⫺170 to 30 ms relative to target
onset; t test, one-tailed p ⬍ 0.05). This insured that the suppression of the
distractor response as a result of the saccade plan could not be simply
attributed to response adaptation as the result of an excitatory response
to the target. We computed population-averaged peristimulus time histograms (PSTHs) by first obtaining PSTHs from each neuron and then
finding the mean of these PSTHs. We used ANOVAs to quantify the
spatial properties of the surround. To have a sufficient number of trials
for these analyses, we first pooled the saccade target locations into nine
10 ⫻ 10° clusters before performing the ANOVA. When we computed
the Smax (defined as the 10 ⫻ 10° cluster of saccade targets associated with
the minimum distractor response), we found that in 2/72 neurons there
were two such clusters that were associated with the minimum distractor
response. In these two ambiguous cases, we picked one cluster at random
as the Smax. In the remaining 70 neurons, our algorithm identified a
unique Smax and there was no ambiguity. We defined the angular position of the target with respect to the RF as the angle between a line
connecting the saccade target to the RF center and a horizontal line
passing through the RF center. We used t tests wherever applicable rather
than alternatives like the Wilcoxon signed-rank test or the rank-sum test
because we consistently observed that whenever there was an occasional
discrepancy between the t test and the alternatives (which do assume that
the underlying distribution is symmetrical), it was the t test that agreed
with the results of permutation tests based on repeated simulations. For
the analyses of proportions and latencies, the underlying distributions
were very skewed, and we therefore used a permutation test that compared the z-statistic for the paired difference between large- and smallreward trials with the null distribution for the paired difference obtained
by 10,000 random shuffles of the two distributions being compared.
Error classification. On error trials, the monkeys usually made one
(70.5%), two (20.8%), or three (5.7%) saccades from a time beginning
350 ms after distractor appearance. For categorizing error trials, we first
classified each saccade in these trials as (1) target directed (if its endpoint
lay within 5° of the saccade goal), (2) distractor directed (if its endpoint
lay within 5° of the distractor goal), or (3) elsewhere directed (if it was
neither target directed nor distractor directed). We then used the
following scheme to categorize a given error trial: If there were no
target-directed or distractor-directed saccades, it was classified as an
elsewhere-directed error trial. If only target-directed saccades were
present, it was a target-directed error trial, and similarly, if only
distractor-directed saccades were present, it was a distractor-directed
error trial. If both target-directed and distractor-directed saccades
were present, then we classified the trial as target or distractor directed depending on which saccade was earlier.
In 24.5% of error trials, REX truncated data collection of the eye position signal before the end of the final saccade, and so the saccade endpoint could not be determined directly; in these cases, we classified
saccades whose mean direction was within 0.35 radians (20°) of the line
joining the fixation point to the saccade target as target-directed saccades, and saccades that were not target directed and whose mean direction was within 0.35 radians of the line joining the fixation point to the
distractor location as distractor-directed saccades.
Results
We studied the effect of surround suppression on the visual responses of a total of 105 LIP neurons LIP in three monkeys (43 in
monkey Z, 26 in monkey D, 36 in monkey I). Our dataset consists
of LIP neurons with systematically mapped RFs based on their
clear visual response to a briefly flashed spot (see Materials and
Methods). We considered neurons to be in LIP if they showed
consistent visual, delay-period, and/or saccade-related responses
during the memory-guided saccade task or were located between
12790 • J. Neurosci., September 22, 2010 • 30(38):12787–12797
such neurons in that electrode penetration. A categorical breakdown of the number of neurons contributing to each task type is
shown in supplemental Table 1 (available at www.jneurosci.org
as supplemental material).
LIP neurons show clear surround suppression by a
planned saccade
We looked for evidence of surround suppression of LIP neural
responses by systematically mapping the effect of a visually
guided delayed saccade plan on the response to a task-irrelevant
distractor in a subset of 72 neurons. In this task (the targetmapping task, Fig. 1 A), the monkey fixated the central fixation
point and a small red target appeared at a location chosen randomly on each trial from the grid (Fig. 1C). Five hundred milliseconds later, a large, white, salient but task-irrelevant distractor
flashed in the center of the RF for ⬍50 ms The fixation point
disappeared 550 ms later, which served as a cue for the monkey to
make a saccade to the target within 400 ms to earn a reward. We
compared the neuronal response in the target-mapping task to
the response in a control task (the no-saccade control task, Fig.
1 B) run in a separate block, in which the monkey was rewarded
for maintaining fixation and no saccade target appeared. The
no-saccade control task was otherwise identical to the targetmapping task. We also ran a small proportion of no-saccade
control trials interleaved within the target-mapping task: the
distractor response in this condition was not significantly different from that in the blocked version (mean difference ⫾
SEM ⫽ 1.16 ⫾ 1.73 spikes/s, t test p ⫽ 0.5027, n ⫽ 72 neurons)
(supplemental Fig. 1 A, B, available at www.jneurosci.org as
supplemental material).
In the target-mapping task, a saccade plan to locations in the
visual field outside the RF suppressed the response to the distractor flashed at the RF center relative to the distractor response in
the no-saccade control task (Fig. 1). Suppression could be evoked
from a range of spatial locations. The degree of suppression varied markedly as a function of saccade target location (example
response map in Fig. 1 D). To quantify the maximal amount of
suppression for each neuron, we identified a 10° ⫻ 10° region
outside the RF (Smax, red square in Fig. 1 D) from which the
saccade plan maximally suppressed the distractor response. We
used a randomly selected two-thirds of trials to define the location of the Smax for each neuron. Locations were considered to be
outside the RF if the appearance of the saccade target did not elicit
a significant response from the neuron (see Materials and Methods). We then cross-validated, using the remaining one-third of
trials to estimate the magnitude of the suppression evoked by the
saccade plan to locations within Smax. When the monkey planned
a saccade to regions within Smax, the distractor response was reduced compared to the no-saccade control (see example neuron,
Fig. 1 E). This reduction was strongly present in our LIP population: in 66 of 72 neurons (91.7%), planning a saccade to locations
within Smax reduced the neuron’s response to the distractor relative to the no-saccade control (Fig. 2 B) (two-sample t test, onetailed p ⬍ 0.05, n ⫽ number of trials in the session). Across the
population, the distractor response was strongly reduced compared to the no-saccade control task when planning a saccade to
locations within Smax (mean reduction ⫾ SEM ⫽ 14.14 ⫾ 1.46
spikes/s, p ⬍ 0.0001, n ⫽ 72 neurons). In addition, the net distractor response (calculated by subtracting the pre-distractor firing rate 240 ms before to 30 ms after distractor onset) was also
significantly suppressed when the monkey planned a saccade to
locations within Smax compared to the no-saccade control task
Falkner et al. • Surround Suppression, Motivation, and the LIP Map
(mean reduction ⫾ SEM ⫽ 8.27 ⫾ 1.19 spikes/s, p ⬍ 0.0001, n ⫽
72 neurons).
Suppression emerged in the background activity even before
the distractor appeared, beginning 100 ms after the appearance of
the saccade target, and continuing through the trial until the
go-cue (Fig. 2 A) (n ⫽ 72 neurons). The pre-distractor baseline
response (⫺500 to 30 ms around distractor onset) when the
monkey planned a saccade to locations within Smax was significantly reduced compared to the no-saccade control task (mean
reduction ⫾ SEM ⫽ 3.43 ⫾ 1.15 spikes/s; p ⫽ 0.0037, n ⫽ 72
neurons). When we recalculated the Smax based on the predistractor baseline response itself, rather than basing it on the
distractor response (supplemental Fig. 1 E, F, available at www.
jneurosci.org as supplemental material), an even larger effect on
the pre-distractor baseline response was visible (mean reduction ⫾ SEM ⫽ 7.09 ⫾ 1.07 spikes/s, p ⬍ 0.0001, n ⫽ 72 neurons).
Surround suppression is long ranging and radially symmetric
in the population
Suppressive surrounds from individual neurons in LIP had a
wide variety of shapes, similar to reports of surround suppression
from lower visual areas (Orban, 2008). The amount of suppression elicited by a saccade target varied significantly with its spatial
location in 57/72 neurons (Kruskal–Wallis ANOVA, p ⬍ 0.05).
Surround suppression extends over long distances: the farthest
location from which significant suppression could be elicited lay
⬎21.2° from the excitatory receptive field center in all 66 neurons
that showed significant surround suppression. The mean farthest
location was 35°. Smax lay further than 10° from the RF center in
65/72 neurons (90.3%).
Although individual neurons showed diverse surround
shapes, surround suppression averaged across the population
was radially symmetric and showed a systematic dependence
upon the distance of the saccade target from the RF center. For
each neuron, we plotted the average activity from the targetmapping task for each target location (minus the activity in the
no-saccade control task) as a function of the distance between the
distractor and target locations (example neuron in Figs. 1 F, 2C).
On average, suppression reached a maximum between 12° and
35° from the RF center, and remained significant up to 40° away
from the RF center. A similar distance dependence was seen for
the baseline response (supplemental Fig. 2 B, available at www.
jneurosci.org as supplemental material). To evaluate the radial
symmetry of the surround around the excitatory receptive field
center, we plotted the average activity from the target-mapping
task at each location outside the RF (minus the activity in the
no-saccade control task) as a function of the angular locations of
the target with respect to the RF center (Fig. 2 D, black). The
population-averaged surround was radially symmetric around
the RF center, and showed no significant dependence upon the
angular location of the saccade target with respect to the RF center (Kruskal–Wallis ANOVA, p ⫽ 0.8732).
Individual neurons, however, did not in general have circularly symmetric surrounds. When we replotted the data in the
blue trace in Figure 2 D after rotating the location of Smax so that
it always lay at 0°, thereby aligning the locations with the maximum amount of suppression, the average response showed a
clear dependence upon angular location of the saccade target
with respect to the excitatory receptive field center (gray trace,
Kruskal–Wallis ANOVA, p ⬍ 0.0001). In accordance with this
result, the degree of suppression in individual neurons along a
ring passing through Smax (with the RF as center) depended significantly upon the angular location of the saccade target in 33/72
Falkner et al. • Surround Suppression, Motivation, and the LIP Map
A
B
C
D
J. Neurosci., September 22, 2010 • 30(38):12787–12797 • 12791
to a saccade target that flashed briefly for
50 ms at a single location within the suppressive surround. The task was otherwise
identical to the target-mapping task (Figs.
1 A, 3A). We briefly flashed a distractor in
the RF center 500 ms after the saccade target appeared. The fixation point disappeared 550 ms after the distractor
disappeared, and the monkey was rewarded for making a saccade to the spatial
location of the vanished stimulus. For 40
of the 48 neurons, the neuronal response
to the distractor that appeared during the
delay period was significantly suppressed
relative to the no-saccade control (83.3%;
two-sample t test, one-tailed p ⬍ 0.05)
(Fig. 3B). Suppression was strongly significant across the population of sampled
neurons (mean reduction ⫾ SEM ⫽
16.09 ⫾ 2.33 spikes/s, p ⬍ 0.0001, n ⫽ 48
neurons) (Fig. 3C). Suppression by a
memory-guided saccade, like suppression
by a visually guided saccade, began 100 ms
after the saccade target appeared and continued until the go-cue (Fig. 3B) (n ⫽ 48
neurons).
A distractor in the surround transiently
suppresses the response to the
saccade target
Figure 2. A, Population average PSTH reveals significant suppression of both baseline and distractor response when a saccade In a subset of neurons (n ⫽ 37), we looked
is planned to the Smax (red) compared to the no-saccade control (blue). Only the one-third of trials that were not used to calculate to see whether a flashed distractor in the
the Smax contribute to the response in red. Black crosses mark the centers of non-overlapping 100 ms time bins with a significant
surround would have a suppressive effect
difference between responses (paired t test, p ⬍ 0.05, n ⫽ 72 neurons). B, Scatter plot of each neuron’s response to the distractor
on the maintained activity during a
(30 –300 ms after distractor onset, gray bar in A) during the no-saccade control (abscissa) and the saccade plan to Smax condition
(ordinate). Paired t test: p ⬍ 0.0001, n ⫽ 72. Green, black, and magenta circles indicate neurons from monkeys I, D, and Z, planned saccade to the excitatory receprespectively. C, Distractor response varies with distance of saccade target from the RF center. Population-averaged distractor tive field (Fig. 4 A). In this task (the
response during the target-mapping task (minus the response during the no-saccade control, horizontal dashed line at 0) is plotted distractor-mapping task), a variant of the
as a function of the distance between the saccade target and the RF center. Averaged tuning curves were first calculated for each target-mapping task, the saccade target alneuron and then averaged together to produce the population average. Error bars show SEMs. n ⫽ number of neurons contrib- ways appeared at the RF center, while the
uting to each data point. D, Population-averaged suppression extends in all directions from the RF. A polar plot shows average level spatial location of the distractor (rather
of suppression in 8 binned angular directions (bin size ⫽ 45°) around the RF center. Polar tuning plots were first computed for each than the saccade target) was randomized.
neuron and then averaged together. Error bars are as in C. The magnitude of suppression (spikes/s) is plotted as a function of The distractor-mapping task was otherabsolute direction around the RF center (black), and after rotating all target angles so that the center of Smax lies at 0° (gray). The
wise identical to the target-mapping task.
four circles in the polar plot lie at ⫺15, ⫺10, ⫺5, and 0 spikes/s. See also supplemental Figures 1 and 2 (available at www.
As a control, during a small number of
jneurosci.org as supplemental material).
interleaved trials, no distractor appeared
during the delay period (the no-distractor
neurons (45.8%, Kruskal–Wallis ANOVA, p ⬍ 0.05). Finally,
control). Again we used half the trials to determine the 10 ⫻ 10°
though the RF centers were all in the contralateral visual field or
region where the distractor evoked maximal suppression (DSmax)
and then used the remaining trials to estimate the effect of a
along the midline, the locations of the Smax for each cell showed
only a small tendency to lie in the contralateral hemifield: 18/25
distractor flashed within DSmax. A distractor flashed within DSneurons (72.0%) in monkey Z and 15/22 neurons (68.2%) in
max caused a significant transient suppression of the maintained
delay-period response of the neuron. This effect was significant
monkey D lay in the contralateral hemifield ( p ⫽ 0.0455 and p ⫽
for two consecutive 100 ms bins following distractor onset (Fig.
0.1356, respectively, test of proportions), but only 9/19 (47.4%)
4 B for the population average) (n ⫽ 37 neurons). The response
neurons in monkey I did ( p ⬇ 1, test of proportions).
30 –300 ms following the distractor flashed within Smax was significantly lower than the response in the same period in the noSuppression can be maintained without the presence of the
distractor control (Fig. 4C) (mean decrease ⫾ SEM ⫽ 3.00 ⫾ 1.07
visual target
spikes/s, p ⫽ 0.0075, n ⫽ 37). In addition, the saccadic latency on
LIP neurons show enhanced activity throughout the delay pethese trials (where distractor appeared within DSmax) was signifriod of the memory-guided delayed saccade task (Gnadt and
icantly longer compared to the interleaved no-distractor control
Andersen, 1988). We tested whether this was also true for surtrials, despite the fact that the distractor appeared 550 ms before
round suppression in a subset of 48 neurons by modifying the
the go signal (Fig. 4 D) (mean increase ⫾ SEM ⫽ 13.07 ⫾ 2.85 ms,
target-mapping task. Instead of a visually guided delayed saccade,
p ⬍ 0.0001, n ⫽ 37), confirming that the distractor had a disruptwe asked the monkey to make a memory-guided delayed saccade
Falkner et al. • Surround Suppression, Motivation, and the LIP Map
12792 • J. Neurosci., September 22, 2010 • 30(38):12787–12797
A
B
C
Figure 3. Suppressioncanbemaintainedwithoutthepresenceofthesaccadetarget.A,Taskdesign:Identicaltothetarget-mappingtask,exceptthatmonkeysplannedamemory-guidedsaccadetoasingle
fixedlocationwithinthesurround.ThedistractorwasflashedattheRFcenter.B,PopulationaveragePSTHrevealssignificantsuppressionofbothbaselineanddistractorresponsewhenamemory-guidedsaccade
isplannedtothesurround(red)comparedtotheno-saccadecontrol(blue).Binwidth⫽15ms.C,Scatterplotofeachneuron’sresponsetothedistractor(graybarinB)duringtheno-saccadecontrol(abscissa)
comparedtothesaccadeplantothesurround(ordinate).Onepoint(controlresponse⫽131.70,saccadeplan⫽59.64)wasomittedforvisibility.Pairedttest:p⬍0.0001,n⫽48.ThefigureformatforBand
C is otherwise identical to Figure 2, A and B, respectively.
ing effect on the monkey’s saccade plan. Saccade latencies are also
longer when averaged across all possible distractor locations
(not just the DSmax; mean increase ⫾ SEM ⫽ 12.35 ⫾ 3.42 ms,
p ⬍ 0.0001, n ⫽ 37) (Fig. 4 D).
Increasing expected reward increases the response to the
target and decreases the response to the distractor
We studied the effect of motivation on surround suppression on
a subset of neurons in LIP (n ⫽ 48) using a variant of the targetmapping task. We cued the monkey to expect a large or a small
reward using the color of the saccade target to indicate the upcoming reward (cued-reward task). We used two specific spatial
configurations (always in separate blocks): to measure the distractor response, we presented the distractor at the RF center
(and the saccade target at a fixed location in the suppressive surround), and to measure the target response, we presented the
saccade target at the RF center (and the distractor at a fixed location within the suppressive surround). The cued-reward task was
otherwise identical to the target-mapping task. We randomly assigned color pairings with large and small rewards during each
recording session. Large- and small-reward targets were interleaved within each block of trials. The monkeys learned the reward contingencies associated with the color of the saccade target
within a few trials, as indicated by significantly faster saccade
latencies and significantly fewer distractor-directed saccades on
the large-reward trials than on the small-reward trials (Roesch
and Olson, 2003; Hikosaka et al., 2006).
On large-reward trials, the three monkeys never made an error
saccade directed toward the distractor. However, on smallreward trials, all three monkeys made a very small, but significant
proportion of error saccades directed toward the distractor (permutation p ⬍ 0.0001 in each monkey, mean proportion ⫾ SEM
in monkey: Z, 2.08 ⫾ 1.07%, n ⫽ 8; D, 1.77 ⫾ 0.41%, n ⫽ 19; I,
2.82 ⫾ 0.76%, n ⫽ 21). Monkeys Z and I also made significantly
shorter latency saccades to the saccade targets associated with the
large reward than to those associated with the small reward
(mean decrease ⫾ SEM in monkey: Z, 83.46 ⫾ 12.86 ms, p ⫽
0.0002, n ⫽ 8; D, 10.21 ⫾ 7.54 ms, p ⫽ 0.1813, n ⫽ 19; I, 22.80 ⫾
9.70 ms, p ⫽ 0.0258, n ⫽ 21). These results indicate that the
monkeys could assess the reward value of the trial based on the
saccade target color and were more highly motivated during
large-reward trials.
The relative magnitude of the cued reward affected the responses to both the distractor (when the monkey planned a sac-
cade to the surround and the distractor appeared at the RF
center) and the target (when the target and distractor locations
were reversed). The neuronal response to the distractor flashed at
the RF center on large-reward trials was significantly lower than
the response on small-reward trials in three consecutive 100 ms
periods following distractor onset (Fig. 5A) (n ⫽ 46 neurons).
This reduction was significant in 31 of the 46 neurons taken
individually (67.4%; two-sample t test, one-tailed p ⬍ 0.05). In
the population, the reduced distractor response on large-reward
trials was highly significant (Fig. 5B) (mean decrease ⫾ SEM ⫽
10.36 ⫾ 1.83 spikes/s, p ⬍ 0.0001, n ⫽ 46 neurons).
The neuronal response to the saccade target appearing at the
RF center was greater when the monkey expected a large reward
instead of a small reward. In the population, the enhanced target
response (400 ms before distractor onset to 30 ms after distractor
onset) on large-reward trials was highly significant (Fig. 5C)
(mean increase ⫾ SEM ⫽ 11.15 ⫾ 2.27 spikes/s, p ⬍ 0.0001, n ⫽
38 neurons). The target response was significantly higher on
large-reward trials in 22 of the 38 neurons taken individually
(57.9%; two-sample t test, one-tailed p ⬍ 0.05). The enhanced
target response, averaged across monkeys, was significant
throughout the trial from 100 ms after saccade target onset until
the go-cue (Fig. 5D) (n ⫽ 38 neurons). The duration of the enhanced target response was variable across monkeys. Monkey D
showed an enhanced target response only during the early part of
the trial, while the other two monkeys showed an enhanced response throughout the trial until the go-cue (supplemental Fig.
3C–H, available at www.jneurosci.org as supplemental material).
To ensure that the effects of varying expected reward were not
due simply to a systematic (though unlikely) overlap of the chosen reward associations with LIP color selectivity, we performed a
control experiment in a subset of the neurons recorded in the
cued-reward task (supplemental Fig. 3 A, B, available at www.
jneurosci.org as supplemental material). Before associating different reward sizes with different colors, we recorded the
responses of LIP neurons with both target colors associated with
the same reward size, sampling both spatial configurations (distractor at RF center and target in suppressive surround in one
block and target at RF center and distractor in suppressive surround in another block). We found no significant behavioral
differences (n ⫽ 38 neurons) between trials with the two saccade
target colors in the total percentage of errors (mean difference ⫾
SEM ⫽ 0.37 ⫾ 0.67%, p ⫽ 0.58), the percentage of distractordirected error saccades (mean difference ⫾ SEM ⫽ 0.036 ⫾ 0.060%,
Falkner et al. • Surround Suppression, Motivation, and the LIP Map
J. Neurosci., September 22, 2010 • 30(38):12787–12797 • 12793
Distractor in surround (ms)
Activity (sp/s)
B
Distractor in DS max (sp/s)
Distractor and saccade target responses
are correlated with saccade latency
40
RF
We looked for correlations between the
neuronal response and the monkeys’ saccade latency in the cued-reward task. For
small-reward trials, the distractor response
was positively correlated with saccade laNo-distractor
tency on a trial-by-trial basis: increased
control
Distractor in
distractor responses were associated with
DS max
longer-latency saccades when the distractor
10
was flashed at the RF center. The average
0
500
1000
Time after target onset (ms)
correlation coefficient (Spearman’s ␳) between trial-by-trial neuronal activity 30 –
C
D
300 ms after distractor onset and saccadic
Saccade latency
Activity at distractor onset
latency was significantly greater than zero
(Fig. 5E) (mean ⫾ SEM ⫽ 0.088 ⫾ 0.024,
80 Monkey Z
300
p ⫽ 0.0006, n ⫽ 46). Conversely, the target
Monkey D
response was negatively correlated with saccade latency on a trial-by-trial basis: increased target responses were associated
with shorter-latency saccades when the tar200
get appeared at the RF center. The average
correlation coefficient between trial-by-trial
neuronal activity 300 –500 ms after distractor response and saccadic latency was
significantly negative (mean ⫾ SEM ⫽
0
100
80
⫺0.14 ⫾ 0.04 ms/Hz, p ⫽ 0.0005, n ⫽ 38).
100
0
300
200
In large-reward trials, there was a similar
No-distractor control (sp/s)
No-distractor control (ms)
negative correlation coefficient when the
Figure4. Aflasheddistractorelicitssuppression.A,Distractor-mappingtask:identicaltothetarget-mappingtask(Fig.1A),exceptthat target lay at the RF center (mean ⫾ SEM ⫽
thesaccadetargetlocationwasfixedattheRFcenter,andthedistractorlocationwaschosenrandomlyoneachtrialfromthe40⫻40°grid ⫺0.069 ⫾ 0.027 ms/Hz, p ⫽ 0.0132, n ⫽
of locations (Fig. 1C). In interleaved no-distractor controls, the distractor was not flashed. B, Distractor onset in the surround evokes 38), but not when the distractor was flashed
transient suppression. Population average PSTHs show the no-distractor control (blue) and the population average response when the at the RF center (mean ⫾ SEM ⫽ 0.033 ⫾
distractor was flashed within DSmax calculated from the bottom-up response map (red). Trials used to calculate DSmax not included in the 0.027 ms/Hz, p ⫽ 0.2266, n ⫽ 46). Since the
PSTH. PSTHs are aligned to saccade target onset. Black crosses are as in Figure 2A. Bin width ⫽ 25 ms. C, Scatter plot of each neuron’s reduced distractor response on largeresponsetothedistractorduringtheno-distractorcontrol(abscissa)comparedtotheresponsewiththedistractorwithinDSmax (ordinate). reward trials is accompanied by a reduced
Paired t test: p ⫽ 0.007, n ⫽ 37. Two points (control response ⫽ 176.02, 134.35 and saccade plan ⫽ 189.92, 123.28) were omitted for variance (mean decrease ⫾ SEM ⫽ 8.59 ⫾
visibility. D, Distractor appearance leads to slowed saccadic latencies: scatter plot of mean saccadic latency during the no-distractor control
2.43 Hz 2, p ⫽ 0.0002, n ⫽ 46), we interpret
(abscissa)versusthemeansaccadiclatencywiththedistractorflashedeitherwithinDSmax (ordinate,filledcircles)oranywhereinthevisual
this
result as reflecting that once distractor
field (ordinate, plus signs). Each point represents data from the recording of one neuron. Paired t tests for both comparisons: p ⬍ 0.0001,
responses
are highly suppressed (as in the
n ⫽ 37. The figure format for B and C is otherwise identical to Figure 2, A and B, respectively.
large-reward trials), their reduced residual
trial-by-trial variability contributes less to
p ⫽ 0.50), or saccadic latency (mean difference ⫾ SEM ⫽ 1.44 ⫾
the overall variation in saccadic latency.
2.24 ms, p ⫽ 0.53). Before reward association, we also found no
significant differences between the two colors in either the disThe distractor response in LIP predicts erroneous saccades
tractor response (mean difference ⫾ SEM ⫽ 0.22 ⫾ 0.67 spikes/s,
The monkeys had an error rate of only 5.0% on average during
p ⫽ 0.74, n ⫽ 35) or the target response (mean difference ⫾
large-reward trials. But because they usually made far more errors
SEM ⫽ 2.12 ⫾ 2.32 spikes/s, p ⫽ 0.36, n ⫽ 31).
on small-reward trials (mean error rate ⫽ 31.5%), we were able to
On large-reward trials, the three monkeys never made an error
use the small-reward trials to test whether there was any correlasaccade directed toward the distractor. However, on smalltion between the distractor response in LIP and the monkey’s
reward trials, all three monkeys made a very small but significant
saccadic behavior. To eliminate any contamination of the distracproportion of error saccades directed toward the distractor (pertor response (30 –300 ms following distractor onset) from
mutation p ⬍ 0.0001 in each monkey, mean proportion ⫾ SEM
saccade-related signals, we included only error trials where the
in monkey: Z, 2.08 ⫾ 1.07%, n ⫽ 8; D, 1.77 ⫾ 0.41%, n ⫽ 19; I,
monkey made an erroneous saccade after 350 ms following the
2.82 ⫾ 0.76%, n ⫽ 21). Monkeys Z and I also made significantly
distractor onset. We divided error trials into three types dependshorter latency saccades to the saccade targets associated with the
ing on whether the erroneous saccade was directed toward the
large reward than to those associated with the small reward
distractor (distractor-directed error trials), preemptively toward
(mean decrease ⫾ SEM in monkey: Z, 83.46 ⫾ 12.86 ms, p ⫽
the target (target-directed error trials), or toward neither the
0.0002, n ⫽ 8; D, 10.21 ⫾ 7.54 ms, p ⫽ 0.1813, n ⫽ 19; I, 22.80 ⫾
distractor nor the target (elsewhere-directed error trials). The dis9.70 ms, p ⫽ 0.0258, n ⫽ 21). These results indicate that the
tractor response in LIP was significantly enhanced on distractormonkeys could assess the reward value of the trial based on the
directed error trials compared to correct trials (Fig. 6C) (mean
saccade target color and were more highly motivated during
increase ⫾ SEM ⫽ 15.80 ⫾ 3.54 spikes/s, p ⫽ 0.0003, n ⫽ 18
large-reward trials.
neurons). The population average PSTH on distractor-directed
A
Falkner et al. • Surround Suppression, Motivation, and the LIP Map
12794 • J. Neurosci., September 22, 2010 • 30(38):12787–12797
Discussion
Our results show, for the first time, that
LIP neurons have strong suppressive surrounds that influence and sharpen the LIP
priority map. By systematically characterizing these effects, we find that suppression of LIP responses is wide-ranging and
can therefore link the representations of
stimuli that are distant from each other in
physical space.
A
B
20
−500
Distractor Response
80
Small Reward
Large Reward
Large reward (sp/s)
100
Average activity (sp/s)
0
500
C
Small Reward
Large Reward
80
20
−500
0
500
Time after distractor onset (ms)
E
Spearman’s rho
error trials (Fig. 6 B, red PSTH) was significantly different from the PSTH on correct trials (Fig. 6 B, blue PSTH) from 100
to 300 ms following distractor onset (n ⫽
18 neurons). The enhancement of the distractor response was specific to distractordirected error trials and was not present
for the other two types of error trials. There
was no significant difference between the
distractor response on elsewhere-directed
error trials and correct trials (mean difference ⫾ SEM ⫽ 2.75 ⫾ 1.99 spikes/s, p ⫽
0.1691, n ⫽ 35 neurons). Similarly, the distractor response on target-directed error
trials was actually significantly lower than
that on correct trials (mean decrease ⫾
SEM ⫽ 4.60 ⫾ 2.48 spikes/s, p ⫽ 0.0270,
n ⫽ 35 neurons). The enhanced distractor
response therefore predicted the impending
erroneous saccade toward the distractor.
There was no significant difference in
the target response (from 400 ms before to
300 ms after distractor onset) between
distractor-directed error trials and elsewhere-directed error trials (mean difference ⫾ SEM ⫽ 2.29 ⫾ 3.81 spikes/s, p ⫽
0.5405, n ⫽ 9 neurons); we therefore
pooled these two types of trials together as
error trials with saccades directed away
from the target. The target response on
these trials (Fig. 6 E, red PSTH) was significantly higher than that on correct trials
(Fig. 6 E, blue PSTH) (mean increase ⫾
SEM ⫽ 10.03 ⫾ 1.55 spikes/s, p ⬍ 0.0001,
n ⫽ 31 neurons, Fig. 6 F). Thus, a lower
target response predicts error trials where
the monkey saccades away from the target. On these error trials, a higher distractor response predicts a distractor-directed
saccade.
Monkey I
Monkey D
Monkey Z
0
0
80
D
Target Response
120
0
0
Small reward (sp/s)
120
0.2 Small Reward
Large reward
0
-0.2
**
*
**
* p<0.05
** p<0.005
Target
response
Distractor
response
Figure 5. Increasing motivation enhances suppression. A, Distractor response is lower during large-reward trials: With distractor in RF and target in the suppressive surround, population average PSTH shows reduced distractor response in large-reward trials
(red), compared to small-reward trials (blue). Black crosses are as in Figure 2 A. B, Scatter plot of each neuron’s response to the
distractor during small-reward (abscissa) and large-reward (ordinate) trials. Paired t test: p ⬍ 0.0001, n ⫽ 46. One point (smallreward: 105.63, large-reward: 79.00) was omitted for visibility. C, Target response is larger during large-reward trials: With target
in RF and distractor in the suppressive surround, population average PSTH shows enhanced target response in large-reward trials
(red), compared to small-reward trials (blue). Black crosses are as in Figure 2 A. D, Scatter plot of each neuron’s response to the
target (⫺400 to 30 ms after distractor onset, gray bar in C) during small-reward (abscissa) and large-reward (ordinate) trials.
Paired t test: p ⬍ 0.0001, n ⫽ 38. PSTH bin widths: 15 ms. Two points (small-reward: 150.26 and 153.30, large-reward: 184.38,
149.44) were omitted for visibility. The figure format for PSTHs and scatter plots is as in Figure 2. E, Correlates of LIP neurons with
saccadic behavior in the cued-reward task: Larger LIP neuronal responses are associated with faster saccades to the RF and slower
saccades to the surround. In the small-reward condition (blue bars), correlation coefficients were significantly negative (paired t
test: p ⫽ 0.0005, n ⫽ 38) with target in RF and distractor in the surround, while slopes were significantly positive with distractor
in RF and target in the surround (paired t test: p ⫽ 0.0006, n ⫽ 46). Effect sizes were smaller in the large-reward condition (red
bars) and only significant with the target in RF (paired t test: p ⫽ 0.0132, n ⫽ 38) and not with the distractor in the RF (paired t test:
p ⫽ 0.2266, n ⫽ 46). See also supplemental Figure 3 (available at www.jneurosci.org as supplemental material).
Surround suppression in LIP is affected
by cognitive influences
Surround suppression evoked by visual stimuli is a ubiquitous
neural strategy and has been reported in many visual areas, including the retina and lateral geniculate nucleus (Alitto and Usrey,
2008), area V1 (Angelucci and Bressloff, 2006), MT and MST
(Allman et al., 1985; Eifuku and Wurtz, 1998; Orban, 2008), and
V4 (Desimone et al., 1985, 1993). However the surround suppression we report here in LIP has several unique properties not
seen in other visual areas. Most importantly, surround suppression observed in LIP is affected by cognitive processes that are not
dependent upon the presence of a particular visual stimulus. We
demonstrated this in two ways: first, suppression of LIP responses
can be maintained by the memory of a visual stimulus, which will
guide a future saccade, whereas the surround suppression demonstrated in lower visual areas was evoked and maintained by a
visual stimulus itself. Second, suppression of LIP responses is
enhanced when the monkey expects a larger reward as a result of
a learned association with a visual stimulus. Increased motivation
enhanced the representation of the saccade goal and suppressed
the representation of the distractor. The enhancement of the tar-
Falkner et al. • Surround Suppression, Motivation, and the LIP Map
A
J. Neurosci., September 22, 2010 • 30(38):12787–12797 • 12795
Distractor response:
Error to distractor
RF
B
100
C
150
Correct trials
Error trials
Monkey I
Monkey D
Monkey Z
100
D
Target response:
Error away from target
RF
0
−500
0
300
E
80
Error trials (sp/s)
Smax
Average activity (sp/s)
50
0
0
50
100
150
F
150
100
50
Smax
Correct trials
Error trials
20
−500
0
300
Time after distractor (ms)
0
0
50
100
150
Correct trials (sp/s)
Figure 6. Target and distractor responses predict saccadic targeting during small-reward error trials. A lower target response predicts saccades away from the target. A higher distractor response
on such trials predicts a distractor-directed saccade. A, Schematic depicting distractor-directed error trials. B, Population average PSTH shows larger distractor responses on distractor-directed error
trials (red) than on correct trials (blue). C, Scatter plot of each neuron’s response to the distractor during correct trials (abscissa) and distractor-directed error trials (ordinate). Paired t test: p ⫽ 0.0003,
n ⫽ 18 neurons. D, Schematic depicting small-reward error trials where monkey saccades away from the target. E, Population average PSTH shows reduced target responses on these error trials (red)
compared to correct trials (blue). Black crosses are as in Figure 2 A. F, Scatter plot of each neuron’s response to the target (⫺400 to 300 ms relative to distractor onset, gray bar in E) during correct
trials (abscissa) and error trials (ordinate). Paired t test: p ⬍ 0.0001, n ⫽ 31 neurons. PSTH bin widths ⫽ 25 ms. Only errors made at least 350 ms after distractor onset included. Figure format for
PSTHs and scatter plots as in Figure 2.
get response in our single-target task conflicts with prior claims
based on data from game-based choice tasks (Dorris and Glimcher,
2004), but is entirely consistent with reports from various other
parts of the brain, including the dorsolateral prefrontal cortex,
frontal and supplementary eye fields, the basal ganglia, and the
SC (Ikeda and Hikosaka, 2003; McCoy and Platt, 2005; Hikosaka
et al., 2006; Watanabe, 2007).
Spatial attention has been shown to suppress distractor responses through center-surround interactions in the nearsurround of V4 neurons (Sundberg et al., 2009) and from
locations far outside the RF in V1 neurons, especially at higher
task difficulties (Chen et al., 2008). We suggest based on our
results that the center-surround interactions measured in V1 reflect long-range suppressive effects established in another cortical
area like LIP, especially if enhancement of surround suppression
by higher task difficulty is based on the same circuitry as the
enhancement of surround suppression by higher reward expectation (Maunsell, 2004).
Surround suppression in priority maps
Given the ubiquity of surround suppression in the visual system,
it is surprising that the existence of surround suppression in LIP
has been controversial (Churchland et al., 2008). Data from other
putative priority map areas in the brain has also been inconclusive. Data from FEF during a visual search task indicate only
spatially local suppressive effects in less than one-third of neurons that extend on average up to 4 – 6° outside the RF at 10°
eccentricity (Schall et al., 1995, 2004). In the SC, distractors
flashed at locations distant from the excitatory RF evoke shortlatency suppression of pretarget activity in a gap-saccade task in
some neurons (Dorris et al., 2007). In dorsolateral prefrontal
cortex (DLPFC), a memory-guided saccade plan has been shown
to slightly suppress baseline neuronal responses opposite to the
saccade goal (Constantinidis et al., 2002). Our characterization of
surround suppression goes well beyond these prior descriptions
by unequivocally demonstrating the spatially wide-ranging,
strong, and ubiquitous influence of surround suppression of LIP
responses and by illustrating several important and novel properties that have not been previously reported from other areas
(using tasks that were not explicitly designed to study surround
suppression).
The suppressive effects we have measured in LIP may not
necessarily be mediated by direct suppressive effects upon LIP
neurons, and could instead reflect suppressive interactions in
other areas that are then relayed to LIP. This is of course also true
for every other response property measured from LIP neurons to
date: there is not a single known response property of LIP neurons that is known to be definitively established within LIP itself.
However, we do know that inhibitory inputs exert a strong influence on LIP neurons, since the majority of LIP neurons respond
with dramatically increased firing after iontophoretic injection of
bicuculline hydrochloride, a GABAA receptor antagonist, and decreased responses after injection of GABA (Zhang et al., 2007).
Because LIP surround suppression can be maintained by a
memory-guided saccade plan, it is likely to emerge from one or
more “priority-map” brain areas active during the delay period of
the memory-guided saccade task like LIP itself (Sereno and Amador,
2006) FEF, DLPFC, and SC. These areas also contain neurons
whose activity is enhanced when a larger reward is expected following a saccade into the neuron’s RF (Watanabe, 2007), in turn
Falkner et al. • Surround Suppression, Motivation, and the LIP Map
12796 • J. Neurosci., September 22, 2010 • 30(38):12787–12797
leading to enhanced suppression of neurons representing competing locations. The reward-cue signal that mediates the effects
of motivation on surround suppression could emerge from a
range of areas, including the amygdala, striatum, and the perirhinal, entorhinal, orbitofrontal, and insular cortices (Salzman et al.,
2005; Simmons et al., 2007).
Implications of LIP surround suppression for behavior
LIP represents a priority map whose peak can be used by the
visual system for the allocation of visual attention (Bisley and
Goldberg, 2003a) and the oculomotor system for the generation
of saccades when saccades are appropriate (Ipata et al., 2006).
Network models of priority maps often posit that global inhibitory interactions enable the emergence of a peak of activity on the
priority map (Koch and Ullman, 1985; Itti and Koch, 2001) and
are critical for the maintenance of stable, localized persistent activity that is resistant to perturbation from external distractors
(Constantinidis and Wang, 2004). Mutually suppressive push–
pull interactions in LIP have also been postulated to be critical for
the programming of sequential saccades (Xing and Andersen,
2000).
Studies of perceptual decision making in LIP often model the
decision process as a race to a threshold between competing alternatives (Gold and Shadlen, 2007). Our data supports models
of perceptual decision making that incorporate mutual inhibition between competing choices (Usher and McClelland, 2001)
and argues against models of the decision process as independent
random walks toward a threshold. Specifically, our finding that
surround suppression can strongly suppress visually driven LIP
responses suggests that surround suppression could explain the
recently reported large reductions in LIP responses to stimulus
onset in a four-choice task compared to a two-choice task
(Churchland et al., 2008). Surround suppression of LIP responses
also provides a mechanism for the baseline resetting that is part of
models for evidence accumulation toward a saccadic decision in
LIP (Seung et al., 2000; Roitman and Shadlen, 2002). The reward
modulation of surround suppression immediately provides a
possible mechanism for the global computations of normalized
reward value that have been hypothesized to underlie saccadic
choice decisions in LIP (Sugrue et al., 2004).
Converging physiological evidence indicates that the firingrates of neurons in priority maps in FEF, LIP, and SC are tightly
linked to attentional allocation (Bisley and Goldberg, 2003b;
Armstrong et al., 2009). Our findings provide a mechanism by
which spatial locations can compete with each other for attentional priority: the higher firing-rates associated with LIP neurons representing a particular location (in this case, the saccade
goal) lead to lower firing rates in neurons representing other
competing locations. Consistent with the tight linkage between
LIP activity and spatial attention, this mechanism correlates with
a reduction of attentional allocation to the RF when the RF location competes with the saccade goal outside the RF for attentional
priority.
It could be argued that attention is the cause of the reduced
responses to the distractor in LIP in the presence of the saccade
plan to a competing spatial location. This argument posits that
the distractor response is lower in the presence of a saccade plan
because the distractor is less likely to capture attention than the
distractor in the no-saccade control condition. However, attention is a psychophysical construct and cannot cause neural effects. Instead, it is the neural implementation of attention that
must cause the measured effects in LIP, not attention itself.
Therefore, this argument is identical to one discussed above
where the suppressive effects measured in LIP reflect suppressive
interactions in other areas that are then relayed to LIP. The surround suppression we measure in LIP, whether it is implemented
in LIP or elsewhere, provides a mechanism that could underlie
the ability of focused attention to modulate attentional capture
by an abruptly appearing irrelevant stimulus in human subjects
(Egeth and Yantis, 1997). In keeping with the broad extent of the
suppressive surrounds we find in LIP, a human patient with bilateral parietal lesions had difficulty filtering distractors even over
large distances (Friedman-Hill et al., 2003). The increased suppression of distractor responses in LIP when a higher reward is
cued provides a physiological basis for possible improvements in
attentional focusing and distractor suppression as a function of
the cognitive demands of the task.
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Supplemental Table and Figures
Supplemental Table 1
MemoryTarget
Number of
Distractor
guided
Mapping
Cued Reward
neurons in
Mapping
suppression
category
+
12
+
+
9
+
+
+
+
+
+
+
+
+
+
+
10
+
2
+
26
+
13
+
7
25
1
Categorical breakdown of the number of neurons contributing to each task
type. Each row is a different category of neurons, defined by the tasks on which
their properties were measured (marked by + signs). The final column indicates
the number of neurons in the category.
0
0
500
C
D
0
500
0
0
150
Interleaved control (sp/s)
Saccade to
baseline S max (sp/s)
F
50
100
0
−500
0
500
G
0
−500
0
500
I
0
−500
150
0
500
Time after distractor (ms)
C,D) Identical to 2A,B except that the interleaved No-Saccade
control is used instead of the No-Saccade control run in a separate
block. Clear suppression is visible when monkey plans a saccade
to Smax: mean difference between saccade and control responses
= 17.29 ± 1.55 sp/s, p<0.0001, n=72 neurons.
E,F) We calculated a baseline Smax based on the baseline response
(-500 to 30 ms relative to distractor onset) instead of the distractor
response, using 2/3 of the trials. The baseline response was clearly
reduced when planning a saccade to the baseline Smax in the
remaining 1/3 of trials compared to the No-Saccade control (mean
difference ± SEM = 7.09 ± 1.07 sp/s, p<0.0001, n=72 neurons). One
point at (control response = 66.19, saccade plan = 34.59) omitted
for visibility.
I,J) Suppression varies over a large range for different outside-RF
locations. Tuning depth from outside the RF: figure identical to
2A,B except that trials with a saccade to Smax (red PSTH, ordinate
in J) are compared to trials with a saccade to a 10x10 degree
square outside the RF that evokes the minimum suppression; i.e.
the maximum distractor response (Smin, blue PSTH, abscissa in J).
0
We used a conservative definition for the RF (p<0.5) instead of our
0
350
usual p<0.05 criterion (see Methods) to further ensure that Smin
No-Saccade Control (sp/s) lay outside the RF. 2/3 of the trials were used to calculate Smax and
Smin; the remaining 1/3 of trials were used for this plot. Mean
J
difference ± SEM = 12.19 ± 1.75 sp/s, p<0.0001, n=72 neurons.
350
Saccade to
within-RF S max (sp/s)
125
Figure format in each pair of left and right panels is identical to
those in Figures 2A,B respectively.
A,B) No-Saccade Control response is similar whether run in a
separate block (blue PSTH in A, abscissa in B) or interleaved with
Target Mapping trials (red PSTH in A, ordinate in B) Mean difference between blocked and interleaved control responses = 1.16 ±
1.73 sp/s, p=0.5027, n=72 neurons.
G,H) Distractor suppression is also evoked by a saccade plan to
within-RF locations. We calculated an Smax for saccade-target
locations within the RF using 2/3 of trials: there is clear reduction
of the response 30 to 100 ms following distractor onset in the
0
remaining 1/3 of trials (mean difference ± SEM = 36.24 ± 5.51 sp/s,
0
50
p<0.0001, n=63 neurons, 9 neurons had less than 3 contiguous
No-Saccade Control (sp/s)
within-RF locations and were ineligible for Smax calculation).
H
Saccade to Smax (sp/s)
Average Activity (sp/s)
E
100
0
150
Blocked control (sp/s)
150
100
0
−500
Supplementary Figure 1:
150
Interleaved
control (sp/s)
0
−500
B
Saccade to Smax (sp/s)
125
A
0
0
150
Saccade to Smin (sp/s)
Activity relative to
No-Saccade control (sp/s)
A
B
10
40
30
0
−20
20
10
0
0
25
50
0
10
20
30
40
50
Saccade target - ERF distance
(degrees)
Supplementary Figure 2:
A) Since suppression is not radially symmetric (Figure 2D), we re-evaluated
the dependence of the degree of suppression upon the distance of the
saccade target from the RF center. Identical to Figure 2C, except that instead
of averaging data from all saccade target locations, we averaged data from
saccade targets that were outside the RF and lay within 10 degrees of a line
running from the RF center to the Smax. Suppression is clearly visible and
dependent on the distance of the saccade target from the RF center. B)
Identical to Figure 2C, except that the baseline response is used instead of
the distractor response. The baseline response (-500 to 30 ms following
distractor onset) also shows a clear dependence upon the distance of the
saccade target from the RF center.
Future large-reward color (sp/s)
B
A
75
150
50
100
25
50
0
0
0
50
75
0
50 100
Future small-reward color (sp/s)
25
80
70
Average activity (sp/s)
0
500
0
45
55
0
500
15
0
H
G
105
30
20
F
E
10
−500
150
D
C
10
−500
Supplementary Figure 3:
75
−500
0
500
Time after distractor (ms)
15
0
Time after saccade (ms)
A,B) Effects of saccade target color are not significant
before reward association. Both the distractor
response (A, distractor at RF center) and the target
response (B, target at RF center) are not significantly
different when the saccade target has the future
small-reward color (abscissa) or large-reward color
(ordinate). A: mean difference ± SEM = 0.22 ± 0.67
sp/s, p=0.7423, n=35 neurons. B: mean difference ±
SEM = 2.12 ± 2.32 sp/s, p=0.36, n=31 neurons. The
effects of saccade color were not explicitly measured
prior to reward association in the remaining neurons.
One point in B at (small-reward color response =
155.57, large-reward color response = 94.09) omitted
for visibility.
C,E,G) Same data and format as in Figure 5C, but
separately for the 3 monkeys Z (in C), D (in E) and I
(in G). All 3 monkeys show greater responses to the
target in large-reward trials during the early part of
the trial. However, from about 100 ms before
distractor onset, monkey D no longer shows an
enhanced target response.
D,F,H) Same format as in C,E and G, except the PSTH
is aligned to saccade onset. The difference between
monkeys in the effect of absolute reward on the late
delay response is visible. The absence of statistical
significance for the effects in monkey Z is likely due
to the small number of neurons recorded from this
monkey (N=8).
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