1Division of Neuroscience and 2Howard Hughes Medical Institute, Baylor College of Medicine, Houston, Texas 77030
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ABSTRACT |
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McAdams, Carrie J. and John H. R. Maunsell. Attention to Both Space and Feature Modulates Neuronal Responses in Macaque Area V4. J. Neurophysiol. 83: 1751-1755, 2000. Attention is the mechanism with which we select specific aspects of our environment for processing. Psychological experiments have shown that attention can be directed to a spatial location or to a particular object. Electrophysiological studies in trained macaque monkeys have found that attention can strengthen the responses of neurons in cortical area V4. Some of these studies have attributed these effects to spatial attention, whereas others have suggested that feature-directed attention may modulate the neuronal response. Here we report that neuronal correlates for both spatial and feature-directed attention exist in individual neurons in area V4 of behaving rhesus monkeys.
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INTRODUCTION |
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Attention can be directed at different attributes of the environment. We can perform many tasks which seem to require different types of stimulus processing. Clearly, catching a flying object and determining what object is flying are different tasks. Catching the object requires computations of its velocity and trajectory. Determining the identity of the object requires a comparison of the visual attributes of the object with the attributes of other stimuli.
Experiments examining reaction times in human subjects suggest that
attention may be directed to either or both stimulus location or
feature. Maljkovic and Nakayama (1994, 1996
)
examined reaction times in pop-out tasks. They found that reaction
times decreased when either the feature that defined the target or the
location of the target was the same on consecutive trials.
Additionally, the improvements in reaction time showed summation,
suggesting that feature and position may use different attentional
mechanisms. Baylis and Driver (1992)
demonstrated that
the ability of distractors to interfere with recognition of the target
depends on both the spatial proximity of the distractors to the target
and whether the target and distractor are the same color. They
suggested that attentional allocation depends on the similarity of the
target and distractors, because the visual scene is parsed according to
Gestalt principles of perceptual organization.
Neuronal correlates of attention have also been measured in many
different cortical areas using electrophysiological recordings from
single neurons in behaving monkeys. Neurons throughout extrastriate visual cortex show increased responses when the animal's attention is
directed to stimuli that are in the receptive field of the neuron being
recorded (Bushnell et al. 1981; Connor et al.
1996
, 1997
; Mountcastle et al. 1987
; Sato
1988
; Treue and Maunsell 1996
). Increased
neuronal responses have also been found when attention is allocated on
the basis of stimulus feature (Haenny et al. 1988
; Maunsell et al. 1991
; Motter 1994a
,b
).
However two important issues remain. Is the neuronal input that results
in a modulation in a spatial attention task different from the input
that causes modulation in a feature-directed attention task? Are the
same neurons involved in performing both spatial and feature-directed attention tasks?
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METHODS |
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All experimental procedures and care of the animals were carried out in compliance with guidelines established by the National Institutes of Health.
Behavioral paradigms
We examined the effects of attention by recording from neurons
in monkeys while they performed a task that required them to shift
their attention to stimuli at different locations in visual field. Data
were collected from two male rhesus monkeys (Macaca mulatta). Water intake was controlled and each animal was trained to perform a behavioral task using operant conditioning with a juice
reward. Partway through training, an aseptic surgery was performed to
implant a head post and scleral search coil (Judge et al.
1980). The animal was required to fixate within 0.7° of a
fixation point throughout each trial using the scleral search coil to
monitor eye position (Robinson 1963
). Eye positions were analyzed to ensure that differences in the neuronal responses could not
be attributed to differences in fixation position. The median fixation
difference for the two tasks for both animals was <0.10°.
The monkeys were trained to do a delayed match-to-sample task with two versions (Fig. 1). In both versions, visual stimuli were presented at two locations on each trial: one inside the receptive field of the neuron being recorded from and one outside that neuron's receptive field. The animal was required to report whether the sample and test stimuli shown at one location were the same or different. In the spatial attention task, the visual stimuli at both locations were Gabor stimuli (Space, Fig. 1A). The animal's task was to report whether the orientation of the sample and test at one location were the same. In one mode, attended, the animal had to report on the stimuli inside the receptive field of the neuron being recorded. In the other mode, unattended, the animal had to report on the stimuli outside that neuron's receptive field. This task variant was called the spatial attention task because the neuronal correlate for attention that we were measuring depended on the difference between the animal attending to equivalent stimuli at different locations.
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Another task involved both spatial and feature-directed attention (Space and Feature, Fig. 1B). In this task, the visual stimuli in the receptive field were again Gabors, but those outside the receptive field were isoluminant, colored, 2-D Gaussians. As in the spatial task in the attended mode, the animal reported whether the orientation of the stimuli in the receptive field matched. However, in the unattended mode, the animal reported whether the colors of the stimuli outside the neuron's receptive field matched. This was called the space-and-feature attention task because the neuronal correlate for attention that we measured could depend on either the animal shifting its attention between different locations or different features (color or orientation).
Because only some neurons in area V4 have clear attentional modulation,
we selected those cells that showed attentional modulation during the
space-and-feature attention task (McAdams and Maunsell 1999). For these neurons, data were collected in blocks of one task (spatial or space-and-feature) and one behavioral state (attended or unattended). The animal was instructed to attend to stimuli at only
one location using instruction trials in which visual stimuli appeared
at only one location. After the animal performed two instruction trials
correctly, the other stimuli returned. He continued to direct his
attention to the instructed location until a new instruction trial was
provided. The initial condition was randomly selected and the 4 conditions were performed in blocks of 16 correct trials, with at least
2 cycles of each condition obtained for each neuron. Trials were
balanced within each task so that each of the four stimulus-behavioral
combinations was equally likely. Trials were aborted if the animal
broke fixation or released the lever before the stimulus appeared.
Neuronal Recording and Data Collection
Data were collected from area V4 in both animals using
recording chambers (20 mm diam) that were implanted on intact skull over V4. One animal received a second V4 chamber so that data were
collected from three hemispheres in two animals. Transdural recordings
were made using Pt/Ir recording electrodes of 1-2 M at 1 kHz.
Signals from the microelectrode were amplified, filtered, and monitored
on an oscilloscope and an audio monitor. Histological reconstructions
of the recording areas showed that all recordings were in V4 in the
anterior part of the prelunate gyrus, dorsal to the end of the inferior
occipital sulcus.
One stimulus was centered in the receptive field of the neuron being recorded and the other stimulus was placed at equal eccentricity diametrically across the fovea. The contrast of the Gabors was temporally counterphased at 4 Hz with a sinusoidal profile. The receptive field centers of the V4 neurons were located between 1.2° and 5° eccentricity. Receptive fields were plotted using a task in which the animal maintained fixation on a central spot of light while the experimenter moved a small bright bar while listening to the neuronal response on the audio monitor. Stimuli were generally larger than the receptive fields of the neurons. The oriented patches were adjusted in spatial frequency, color, and size to produce optimized responses. The unattended oriented patches had the same parameter values as the attended oriented patches.
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RESULTS |
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We examined the effects of these tasks on 71 isolated neurons in
area V4 in 2 monkeys. Most of the neurons showed significant attention
effects [62/71 cells; three-factor analysis of variance (ANOVA);
P < 0.05] and most were orientation-selective (60/71 cells; three-factor ANOVA; P < 0.05). The specific task the
animal performed significantly affected the firing rate of 31% of the neurons (22/71 cells; three-factor ANOVA; P < 0.05). We
found relatively few cells with individually statistically significant interactions between attention and task (7/71 cells), task and stimulus
orientation (8/71 cells), and attention, task, and stimulus orientation
(6/71 cells). However, 48% of the neurons (34/71 cells) showed an
interaction between attention and stimulus orientation. We have
previously reported that attention causes a proportional increase in
the responses of these neurons, using different orientations to elicit
different response levels (McAdams and Maunsell 1999). Because small absolute effects of attention were found at orientations away from the peak of the tuning curve, the rest of this analysis was
restricted to the data obtained when the preferred orientation of the
neuron was in the receptive field.
The responses of two single units are plotted in Fig. 2. The visual stimulation of each neuron was the same within each task and the receptive field stimulus was the same in all conditions, but the stimulus outside the neuron's receptive field differed between the two tasks. Each unit responded more strongly when the animal was attending to the stimulus in the receptive field. Although the unit in Fig. 2A responded more strongly overall during the spatial task, it was more modulated by attention in the space-and-feature task. This neuron appeared to receive feature-dependent attentional modulation as well as spatial attentional modulation. The unit in Fig. 2B showed the same amount of attentional modulation in both tasks, presumably reflecting spatial attention alone.
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We calculated an attention index, (attended response unattended
response)/(attended response + unattended response), for each neuron in
each task. The population of neurons showed consistently more
modulation in the space-and-feature attention task than in the spatial
attention task (Wilcoxon signed rank test, P < 0.001). The
median attention index during the spatial attention task was 0.13, corresponding to a 31% increase in activity and the median attention
index during the space-and-feature attention task was 0.21, corresponding to a 54% increase in activity. Although we selected
cells showing attention effects in the space-and-feature attention
task, we could have found neurons without attention effects in the
spatial attention task. Notably, every neuron that we recorded with a
positive attention effect in the space-and-feature attention task also
had a positive attention effect in the spatial attention task, although
not all of these effects were statistically significant. This suggests
that appreciable attentional modulation for features may not occur in
isolation under these conditions.
Although the same stimulus appeared inside the receptive field in all conditions, the distant stimulus differed between the two task modes. That stimulus was far outside the classical receptive field of the neuron being recorded but might have affected the responses between conditions. To examine this possibility, we compared the responses to the attended modes in both tasks. In both of the "attended" conditions, the animal attended to an oriented stimulus inside the receptive field and only the distant unattended stimulus differed. Responses were not significantly different between these conditions (Fig. 3A) suggesting that the distant retinal stimulus was not a factor by itself (median space response 23.6 spike/s; median space-and-feature response 24.5 spike/s; Wilcoxon signed rank test, P > 0.99). When the animal attended to the distant site, however, the feature being attended did affect responses (Fig. 3B). In the unattended modes, attention was directed to orientation during the spatial task and attention was directed to color during the space-and-feature task. Responses were significantly greater in the spatial attention task than in the space-and-feature attention task (median space response 16.4 spikes/s; median space-and-feature response 14.8 spikes/s; Wilcoxon signed rank test, P < 0.001). Thus the change in attentional modulation was a result of the differences in the behavioral requirements in the unattended mode, which resulted in decreased neuronal responses to the oriented grating when the animal was performing the color task, relative to the neuronal responses to the oriented grating when the animal was performing the orientation task on a different grating.
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An alternative explanation for these results is that the animal might
have been less challenged and therefore less vigilant when matching
color compared with matching orientation. This could cause the weaker
responses during the unattended mode of the space-and-feature task
which we observed. One way to assess whether task difficulty has
significantly affected the neuronal responses is to examine whether the
magnitude of the neurophysiological attentional modulation is
correlated with the magnitude of differences in the behavioral performance between the attended and unattended conditions during the
space-and-feature task. We assessed behavioral performance based on the
accuracy of the animal's responses to completed trials. The behavioral
performance of the two animals during the space-and-feature task ranged
from 77% to 91%, with a median of 84%. We calculated a behavioral
performance index, (attended performance unattended performance)/(attended performance + unattended performance), for each
cell. We then examined whether there was any significant correlation
between the neurophysiological attentional index, as previously
described, and the behavioral performance index. We found no
significant correlations between these indices (r =
0.33; P > 0.75), suggesting that the neurophysiological
difference observed is unlikely a result of a difference in difficulty
in performing the two types of tasks.
As a more direct test of the effects of task difficulty, we recorded from 23 neurons in 1 animal using 2 versions of the spatial attention task, which differed in the difficulty of the orientation matching. In one version, the task was easy because the nonmatching stimuli differed in orientation by 90° and the animal's performance was high, 89% correct. The other version of the task was more difficult because the nonmatching stimuli differed in orientation by 30° and the animal's performance was worse, 75% correct. However, there was no significant difference between attentional effects measured for these cells in the easy and difficult variants (Wilcoxon signed rank test, P = 0.98) despite the fact that these cells did show significant attention effects in both the easy and difficult tasks (Wilcoxon signed rank test, P < 0.05). These results support the interpretation that the increased attentional modulations seen in the space-and-feature attention task relative to the spatial attention task were due to the difference in attending to different stimulus features rather than a difference in task difficulty.
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DISCUSSION |
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These experiments contribute to understanding how different forms
of attention interact in visual processing. They show that spatial
attention and feature attention coexist in a relatively early stage of
visual processing, cortical area V4. This finding is consistent with
the demonstrations of attentional modulations in area V4 both by tasks
requiring spatial attention (Connor et al. 1996, 1997
;
Moran and Desimone 1985
; Motter 1993
) and
by tasks that require feature-directed attention (Haenny and
Schiller 1988
; Haenny et al. 1988
;
Maunsell and Hochstein 1991
; Maunsell et al. 1991
; Motter 1994a
,b
). Further, they indicate
that the same neuron can receive multiple types of attentional inputs.
We have also suggested that when attention is directed to an
oriented stimulus at a particular location, oriented neurons with
receptive fields throughout the visual field show a relative increase
in activity. Motter (1994a) has previously shown that V4
neuronal responses can be enhanced when the color or luminance of the
neuronal stimulus in the receptive field matches the color or luminance
of a cue. However, in that experiment, the stimulus in the receptive
field could become the target. In our experiment, the process of
attending to orientation affected the signals of neurons throughout the
visual field even when those neurons appear to be irrelevant to the
task. An alternative explanation is that attention to the colored
stimuli suppresses the responses of neurons to oriented stimuli. Either
interpretation shows that directing attention to a stimulus feature
might modulate the responses of neurons throughout the visual field.
These results provide neurophysiological evidence that visual attention
may be allocated by a segmentation of the scene consistent with Gestalt
principles of perceptual organization: the neuronal responses to the
distractor grating are increased when attention is directed to another
grating than when attention is directed to a color patch.
Recently, Treue and Trujillo (1999) reported that
neurons in area MT could be modulated by both spatial and
feature-directed attention. They presented two random dot stimuli, one
inside and one outside of the receptive field of the neuron being
recorded. The monkeys were cued to attend to a particular location.
They then examined the effects of changing the direction of the motion of the stimulus outside the receptive field on the neuronal responses to the stimulus in the receptive field. They found no effect of changing the stimulus outside the receptive field unless the animal was
attending to it, just as we have reported for V4 neurons in this
experiment. In their task, when the animal attended to the stimulus
outside the receptive field and it was moving in the preferred
direction for the neuron being recorded, the neuron's responses were
13% greater than when the stimulus outside the receptive field was
moving in the null direction. In our analogous condition, we found an
11% increase in response when the animal attended to the orientation
of the stimulus outside the receptive field rather than its color. Both
of these results suggest that processing features even of a specific
target may require dynamic comparisons using information obtained from
other stimuli in the visual field.
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ACKNOWLEDGMENTS |
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We thank C. E. Boudreau, J. DiCarlo, and E. Cook for helpful comments on preliminary versions of the manuscript. We also thank C. E. Boudreau, R. Diaz, and B. Noerager for help with training the animals and other technical assistance.
This work was supported by National Institutes of Health Grants RO1 EY-05911, T32 EY-07001, T32 GM-07330, and T32 GM-08507 to C. J. McAdams. J.H.R. Maunsell is a Howard Hughes Medical Institute Investigator.
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FOOTNOTES |
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Address for reprint requests: J.H.R. Maunsell, Division of Neuroscience, Baylor College of Medicine, One Baylor Plaza, S-603, Houston, TX 77030.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 8 September 1999; accepted in final form 3 December 1999.
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REFERENCES |
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