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Cited by 203Visual perception and processing mechanismsVisual Attention and Saliency DetectionMultisensory perception and integration

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Attention Modulates the Responses of Simple Cells in Monkey Primary Visual Cortex

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McAdams, Carrie J., Reid, R. Clay·2005·The Journal of Neuroscience
DOI 10.1523/jneurosci.2904-05.2005PMC PMC6725881
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Abstract

Spatial attention has long been postulated to act as a spotlight that increases the salience of visual stimuli at the attended location. We examined the effects of attention on the receptive fields of simple cells in primary visual cortex (V1) by training macaque monkeys to perform a task with two modes. In the attended mode, the stimuli relevant to the animal's task overlay the receptive field of the neuron being recorded. In the unattended mode, the animal was cued to attend to stimuli outside the receptive field of that neuron. The relevant stimulus, a colored pixel, was briefly presented within a white-noise stimulus, a flickering grid of black and white pixels. The receptive fields of the neurons were mapped by correlating spikes with the white-noise stimulus in both attended and unattended modes. We found that attention could cause significant modulation of the visually evoked response despite an absence of significant effects on the overall firing rates. On further examination of the relationship between the strength of the visual stimulation and the firing rate, we found that attention appears to cause multiplicative scaling of the visually evoked responses of simple cells, demonstrating that attention reaches back to the initial stages of visual cortical processing.

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Figures

Figure 1 Stimulus configuration and behavioral protocol. The animal fixated on the central spot and had previously been cued to direct his attention to one of the two stimulus grids. The blue dashed circle represents the receptive field of the recorded neuron and was not present on thescreen.Trials in which the animal's attention was directed to the grid overlying the receptive field were defined as attended, whereas those trials in which his attention was directed to the other grid were defined as unattended. A small colored patch (in this example, follow the dashed blue arrow to a red square in the top left stimulus grid) was visible for 250 -350 ms, during which time all of the other pixels in the stimulus continued to change luminance randomly. If the animal's attention had been cued to the grid on the top left, the correct response wouldbeasaccadetotheredtarget,illustratedbythesolidbluearrow.Iftheanimal'sattention had been directed to the stimulus grid on the bottom right (no colored patch shown in this example), the correct response would have been to maintain fixation. Such catch trials ended after a random interval ranging from 260 to 3300 ms.
Figure 1 Stimulus configuration and behavioral protocol. The animal fixated on the central spot and had previously been cued to direct his attention to one of the two stimulus grids. The blue dashed circle represents the receptive field of the recorded neuron and was not present on thescreen.Trials in which the animal's attention was directed to the grid overlying the receptive field were defined as attended, whereas those trials in which his attention was directed to the other grid were defined as unattended. A small colored patch (in this example, follow the dashed blue arrow to a red square in the top left stimulus grid) was visible for 250 -350 ms, during which time all of the other pixels in the stimulus continued to change luminance randomly. If the animal's attention had been cued to the grid on the top left, the correct response wouldbeasaccadetotheredtarget,illustratedbythesolidbluearrow.Iftheanimal'sattention had been directed to the stimulus grid on the bottom right (no colored patch shown in this example), the correct response would have been to maintain fixation. Such catch trials ended after a random interval ranging from 260 to 3300 ms.CC-BY-NC-SA · From the PDF
Figure 2 A , The spatiotemporal receptive-field map of a single neuron in the unattended mode (top) and attended mode (bottom). Blue indicates regions in which black pixels tended to precede spikes (off responses, negative values), and red indicates regions in which white pixels preceded spikes (on responses, positive values). Brighter colors indicate more responsive areas of the receptive field. Intersections in the grid lines correspond to centers of the stimulus pixels. Response values were interpolated betweenpixels. The unattended maps were generated from 2473 spikes and 5260 frames over 108 correct trials, and the attended maps were generated from 2438 spikes and 5160 frames over 108 correct trials. B , The spatial receptive-field (RF) maps were extracted from the spatiotemporal maps by averaging the time frames near the peak response and selecting pixels meeting threshold levels and contiguous with other strong pixels (see Materials and Methods). This was done independently for the primary(column2)andsecondary(column3)subfieldsandforbothbehavioralmodes(redandwhitepixels).However,onlythose pixels that overlapped in the two behavioral modes were included in the comparison (white pixels). C , The time courses of the responses for the receptive-field subfields, summed over all white pixels defined in B . Attended modes are shown in red, and unattended modes are in blue. The gray lines show ± 3 SDs of the noise (pixel variability times the square root of the number of pixels composing the spatial receptive-field subregion) in the response. The asterisks along the x -axis indicate those time bins in which the responses were > 3 SDs of the noise for both the attended and unattended modes and were summed to determine the total visual responses for each mode and each subregion.
Figure 2 A , The spatiotemporal receptive-field map of a single neuron in the unattended mode (top) and attended mode (bottom). Blue indicates regions in which black pixels tended to precede spikes (off responses, negative values), and red indicates regions in which white pixels preceded spikes (on responses, positive values). Brighter colors indicate more responsive areas of the receptive field. Intersections in the grid lines correspond to centers of the stimulus pixels. Response values were interpolated betweenpixels. The unattended maps were generated from 2473 spikes and 5260 frames over 108 correct trials, and the attended maps were generated from 2438 spikes and 5160 frames over 108 correct trials. B , The spatial receptive-field (RF) maps were extracted from the spatiotemporal maps by averaging the time frames near the peak response and selecting pixels meeting threshold levels and contiguous with other strong pixels (see Materials and Methods). This was done independently for the primary(column2)andsecondary(column3)subfieldsandforbothbehavioralmodes(redandwhitepixels).However,onlythose pixels that overlapped in the two behavioral modes were included in the comparison (white pixels). C , The time courses of the responses for the receptive-field subfields, summed over all white pixels defined in B . Attended modes are shown in red, and unattended modes are in blue. The gray lines show ± 3 SDs of the noise (pixel variability times the square root of the number of pixels composing the spatial receptive-field subregion) in the response. The asterisks along the x -axis indicate those time bins in which the responses were > 3 SDs of the noise for both the attended and unattended modes and were summed to determine the total visual responses for each mode and each subregion.CC-BY-NC-SA · From the PDF
Figure 3 Spatiotemporal receptive-field maps (unattended, left; attended, right) and time courses of the responses of the receptive-field (RF) subfields (primary, top; secondary, bottom) for two single neurons that showed modest effects of attention. For the neuron in A , the unattended maps were generated from 1370 spikes and 4573 frames over 108 correct trials, and the attended maps were generated from 1559 spikes and 4991 frames over 108 correct trials. For the neuron in B , the unattended mapsweregeneratedfrom2170spikesand5924framesover144correcttrials,andtheattendedmapsweregeneratedfrom2539 spikes and 5526 frames over 144 correct trials.
Figure 3 Spatiotemporal receptive-field maps (unattended, left; attended, right) and time courses of the responses of the receptive-field (RF) subfields (primary, top; secondary, bottom) for two single neurons that showed modest effects of attention. For the neuron in A , the unattended maps were generated from 1370 spikes and 4573 frames over 108 correct trials, and the attended maps were generated from 1559 spikes and 4991 frames over 108 correct trials. For the neuron in B , the unattended mapsweregeneratedfrom2170spikesand5924framesover144correcttrials,andtheattendedmapsweregeneratedfrom2539 spikes and 5526 frames over 144 correct trials.CC-BY-NC-SA · From the PDF
Figure 4 Histograms of the attentional modulation index for the primary subfield ( A ) and the secondary subfield ( B ). The attentional modulation index was defined as the attended response minus the unattended response divided by their mean. Cells shown in black had individually statistically significant effects of attention.
Figure 4 Histograms of the attentional modulation index for the primary subfield ( A ) and the secondary subfield ( B ). The attentional modulation index was defined as the attended response minus the unattended response divided by their mean. Cells shown in black had individually statistically significant effects of attention.CC-BY-NC-SA · From the PDF
Figure 5 Spatial and temporal receptive fields calculated with and without correction for eye position. Two different neurons are shown in A and B . For each, the spatial receptive fields (RF) in the unattended, attended, and the pixels chosen for analysis of the primary subfield are shown on the left. The time course of the responses in those pixels is shown on the right. The top row for each neuron are the original (uncorrected) maps, and the bottom row are the maps after adjusting for the actual eye position relative to the white-noise stimulus, at a resolution of a quarter of each pixel, at the time of the spikes. Both neurons had individually significant effects of attention both with and without eye correction. Neuron A is the same neuron shown in Figure 2. The attentional index value for each condition is displayed on the top left of the time response function.
Figure 5 Spatial and temporal receptive fields calculated with and without correction for eye position. Two different neurons are shown in A and B . For each, the spatial receptive fields (RF) in the unattended, attended, and the pixels chosen for analysis of the primary subfield are shown on the left. The time course of the responses in those pixels is shown on the right. The top row for each neuron are the original (uncorrected) maps, and the bottom row are the maps after adjusting for the actual eye position relative to the white-noise stimulus, at a resolution of a quarter of each pixel, at the time of the spikes. Both neurons had individually significant effects of attention both with and without eye correction. Neuron A is the same neuron shown in Figure 2. The attentional index value for each condition is displayed on the top left of the time response function.CC-BY-NC-SA · From the PDF
Figure6 A , Histogram of the attentional modulation index of the primary subfield (as in Fig. 4), calculated with the correction for eye position. The 13 cells shown in black had individually statistically significant effects of attention. B , The attentional index for the primary subfield without the correction for eye position is plotted against the attentional index with the correction for eye position. The diagonal x = y is plotted as well. Filled symbols indicate cells with significant effects: filled circles indicate effects only without eye correction (3 cells); filled squares indicate effects only after eye correction (3 cells); and filled triangles indicate effects in both cases (10 cells).
Figure6 A , Histogram of the attentional modulation index of the primary subfield (as in Fig. 4), calculated with the correction for eye position. The 13 cells shown in black had individually statistically significant effects of attention. B , The attentional index for the primary subfield without the correction for eye position is plotted against the attentional index with the correction for eye position. The diagonal x = y is plotted as well. Filled symbols indicate cells with significant effects: filled circles indicate effects only without eye correction (3 cells); filled squares indicate effects only after eye correction (3 cells); and filled triangles indicate effects in both cases (10 cells).CC-BY-NC-SA · From the PDF
Figure7 A , The time course of the responses for the 12 neurons with individually significant positive effects of attention were constructed by normalizing each cell to its peak response in theunattendedmodeandthenshiftingeachfunctionsothatthepeakresponsesofeachneuron were aligned in time. The attended mode is in black, the unattended mode in dark gray, and their difference is shown with a dashed black line. B , The attentional index for the peak of the primary subfield is plotted against the attentional index for the peak of the antagonistic subfield. The diagonal x = y is plotted as well. Filled symbols indicate cells with significant differences between the attentional states: filled circles indicate an effect on the primary subfield only (10 cells); filled squares indicate an effect on the secondary subfield only (3 cells); and filled triangles indicate the cells with effects on both subfields (3 cells).
Figure7 A , The time course of the responses for the 12 neurons with individually significant positive effects of attention were constructed by normalizing each cell to its peak response in theunattendedmodeandthenshiftingeachfunctionsothatthepeakresponsesofeachneuron were aligned in time. The attended mode is in black, the unattended mode in dark gray, and their difference is shown with a dashed black line. B , The attentional index for the peak of the primary subfield is plotted against the attentional index for the peak of the antagonistic subfield. The diagonal x = y is plotted as well. Filled symbols indicate cells with significant differences between the attentional states: filled circles indicate an effect on the primary subfield only (10 cells); filled squares indicate an effect on the secondary subfield only (3 cells); and filled triangles indicate the cells with effects on both subfields (3 cells).CC-BY-NC-SA · From the PDF
Figure 8 A , Histograms of the attentional modulation index for the overall firing rate in response to the stimulus. The attentional modulation index was defined as the spike rate in the attended mode minus the spike rate in the unattended mode divided by their mean. No cells showed individually significant changes in spike rate. B , The attentional index for the primary subfield is plotted against the attentional index for the overall spike rate in response to all stimuli. The 13 cells with significant effects on the primary subfield are shown as filled circles.
Figure 8 A , Histograms of the attentional modulation index for the overall firing rate in response to the stimulus. The attentional modulation index was defined as the spike rate in the attended mode minus the spike rate in the unattended mode divided by their mean. No cells showed individually significant changes in spike rate. B , The attentional index for the primary subfield is plotted against the attentional index for the overall spike rate in response to all stimuli. The 13 cells with significant effects on the primary subfield are shown as filled circles.CC-BY-NC-SA · From the PDF
Figure9 Computationofthetwo-stagemodel:alinearfilterfollowedbyanonlinearoutput function. First row, Schematic representation of four successive stimulus frames, with additional frames indicated by black dots. Second row, The receptive field of a single neuron is convolved with the stimulus sequence to provide a single numerical value representing the result of the linear first stage (the 'linear input'). Third row, A portion of the calculated output of the linear first stage, arbitrarily scaled from -1to1;the x -axis is time and covers 40 different stimulus frames at 23.5 ms/frame. The open circle is the value derived from the stimuli illustrated in the first row; the neighboring black dots indicate the values for the adjacent stimulus frame sequences. Fourth row, A simple form of output nonlinearity: a rectifier that converts all negative inputs to zero and linearly scales positive inputs. Fifth row, Green, The predicted firing rate, derived by passing the result of the linear stage through the output function. The lines shownin red, on the bottom axis, are the actual spikes of the neuron, which varied from zero to three spikes per frame within this specific sequence and up to five spikes per frame overall. The neuron fired more spikes when the predicted firing rate function is high and few or no spikes when the predicted firing rate is low.
Figure9 Computationofthetwo-stagemodel:alinearfilterfollowedbyanonlinearoutput function. First row, Schematic representation of four successive stimulus frames, with additional frames indicated by black dots. Second row, The receptive field of a single neuron is convolved with the stimulus sequence to provide a single numerical value representing the result of the linear first stage (the 'linear input'). Third row, A portion of the calculated output of the linear first stage, arbitrarily scaled from -1to1;the x -axis is time and covers 40 different stimulus frames at 23.5 ms/frame. The open circle is the value derived from the stimuli illustrated in the first row; the neighboring black dots indicate the values for the adjacent stimulus frame sequences. Fourth row, A simple form of output nonlinearity: a rectifier that converts all negative inputs to zero and linearly scales positive inputs. Fifth row, Green, The predicted firing rate, derived by passing the result of the linear stage through the output function. The lines shownin red, on the bottom axis, are the actual spikes of the neuron, which varied from zero to three spikes per frame within this specific sequence and up to five spikes per frame overall. The neuron fired more spikes when the predicted firing rate function is high and few or no spikes when the predicted firing rate is low.CC-BY-NC-SA · From the PDF
Image 10
CC-BY-NC-SA · From the PDF

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Metadata

Authors
McAdams, C. J., & Reid, R. C.
Affiliations
Harvard University (US)
ORCID
Venue
The Journal of Neuroscience
Publisher
Society for Neuroscience
Published
2005-11-23
Volume
25
Issue
47
Pages
11023-11033
ISSN
  • 0270-6474 (ISSN-L)
  • 1529-2401
DOI
10.1523/jneurosci.2904-05.2005
PMC
PMC6725881
OpenAlex
W1964026607
Cited by
203
References
43
Citations by year
2026: 8 · 2025: 5 · 2024: 5 · 2023: 7 · 2022: 8 · 2021: 23 · 2020: 10 · 2019: 4 · 2018: 7 · 2017: 9 · 2016: 7 · 2015: 7 · 2014: 9 · 2013: 11 · 2012: 10
FWCI
6.29
Type
journal article
Language
en
Open access
Licence
Locations
  • Journal of Neuroscience (publishedVersion, cc-by-nc-sa)
  • Europe PMC (PubMed Central) (publishedVersion)
  • PubMed Central (publishedVersion)
  • PubMed (publishedVersion)
Funders
  • National Institutes of Health
  • U.S. Public Health Service (P30 12196)
  • National Eye Institute (R01 EY12815, R01EY012815)
  • National Institute of Neurological Disorders and Stroke (T32-NS07484, T32NS007484)
Topics
  • Life Sciences › Neuroscience › Cognitive Neuroscience › Visual perception and processing mechanisms
  • Physical Sciences › Computer Science › Computer Vision and Pattern Recognition › Visual Attention and Saliency Detection
  • Social Sciences › Psychology › Experimental and Cognitive Psychology › Multisensory perception and integration
Keywords
spatial attention, simple cells, primary visual cortex, receptive fields, visual evoked potentials, attentional modulation, macaque, early visual processing
MeSH terms
Acoustic Stimulation, Action Potentials, Animals, Attention, Behavior, Animal, Brain Mapping, Cues, Electrophysiology, Evoked Potentials, Visual, Macaca fascicularis, Macaca mulatta, Neurons, Photic Stimulation, Space Perception, Visual Cortex

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