 |
||||
|
||||
|
||||
|
||||
Previous Article | Next Article
The Journal of Neuroscience, March 1, 1999, 19(5):1736-1753
Competitive Mechanisms Subserve Attention in Macaque Areas V2 and V4
John H. Reynolds1, Leonardo Chelazzi2, and Robert Desimone1 1 Laboratory of Neuropsychology, National Institute of Mental Health, National Institutes of Health, Bethesda, Maryland 20892-4415, and 2 Dipartimento di Scienze Neurologiche e della Visione, Sezione di Fisiologia, University of Verona, Verona, Italy
It is well established that attention modulates visual processing in extrastriate cortex. However, the underlying neural mechanisms are unknown. A consistent observation is that attention has its greatest impact on neuronal responses when multiple stimuli appear together within a cell's receptive field. One way to explain this is to assume that multiple stimuli activate competing populations of neurons and that attention biases this competition in favor of the attended stimulus. In the absence of competing stimuli, there is no competition to be resolved. Accordingly, attention has a more limited effect on the neuronal response to a single stimulus. To test this interpretation, we measured the responses of neurons in macaque areas V2 and V4 using a behavioral paradigm that allowed us to isolate automatic sensory processing mechanisms from attentional effects. First, we measured each cell's response to a single stimulus presented alone inside the receptive field or paired with a second receptive field stimulus, while the monkey attended to a location outside the receptive field. Adding the second stimulus typically caused the neuron's response to move toward the response that was elicited by the second stimulus alone. Then, we directed the monkey's attention to one element of the pair. This drove the neuron's response toward the response elicited when the attended stimulus appeared alone. These findings are consistent with the idea that attention biases competitive interactions among neurons, causing them to respond primarily to the attended stimulus. A quantitative neural model of attention is proposed to account for these results.
Key words: spatial attention; monkey; extrastriate cortex; V2; V4; model
Copyright © 1999 Society for Neuroscience 0270-6474/99/1951736-18$05.00/0
This article has been cited by other articles:
L. B. Ekstrom, P. R. Roelfsema, J. T. Arsenault, G. Bonmassar, and W. Vanduffel
Bottom-Up Dependent Gating of Frontal Signals in Early Visual Cortex
Science, July 18, 2008; 321(5887): 414 - 417.
[Abstract] [Full Text] [PDF]
C. Kayser, C. I. Petkov, and N. K. Logothetis
Visual Modulation of Neurons in Auditory Cortex
Cereb Cortex, July 1, 2008; 18(7): 1560 - 1574.
[Abstract] [Full Text] [PDF]
J. Poort and P. R. Roelfsema
Noise Correlations Have Little Influence on the Coding of Selective Attention in Area V1
Cereb Cortex, June 13, 2008; (2008) bhn103v1.
[Abstract] [Full Text] [PDF]
M. Kouh and T. Poggio
A Canonical Neural Circuit for Cortical Nonlinear Operations
Neural Comput., June 1, 2008; 20(6): 1427 - 1451.
[Abstract] [Full Text] [PDF]
G. M. Ghose and J. H. R. Maunsell
Spatial Summation Can Explain the Attentional Modulation of Neuronal Responses to Multiple Stimuli in Area V4
J. Neurosci., May 7, 2008; 28(19): 5115 - 5126.
[Abstract] [Full Text] [PDF]
C. I. Buia and P. H. Tiesinga
Role of Interneuron Diversity in the Cortical Microcircuit for Attention
J Neurophysiol, May 1, 2008; 99(5): 2158 - 2182.
[Abstract] [Full Text] [PDF]
P. Fries, T. Womelsdorf, R. Oostenveld, and R. Desimone
The Effects of Visual Stimulation and Selective Visual Attention on Rhythmic Neuronal Synchronization in Macaque Area V4
J. Neurosci., April 30, 2008; 28(18): 4823 - 4835.
[Abstract] [Full Text] [PDF]
C. de Hemptinne, P. Lefevre, and M. Missal
Neuronal Bases of Directional Expectation and Anticipatory Pursuit
J. Neurosci., April 23, 2008; 28(17): 4298 - 4310.
[Abstract] [Full Text] [PDF]
W. K. Page and C. J. Duffy
Cortical Neuronal Responses to Optic Flow Are Shaped by Visual Strategies for Steering
Cereb Cortex, April 1, 2008; 18(4): 727 - 739.
[Abstract] [Full Text] [PDF]
D. Zoccolan, M. Kouh, T. Poggio, and J. J. DiCarlo
Trade-Off between Object Selectivity and Tolerance in Monkey Inferotemporal Cortex
J. Neurosci., November 7, 2007; 27(45): 12292 - 12307.
[Abstract] [Full Text] [PDF]
G. L. Shulman, S. V. Astafiev, M. P. McAvoy, G. d'Avossa, and M. Corbetta
Right TPJ Deactivation during Visual Search: Functional Significance and Support for a Filter Hypothesis
Cereb Cortex, November 1, 2007; 17(11): 2625 - 2633.
[Abstract] [Full Text] [PDF]
A. A. Stevens, M. Snodgrass, D. Schwartz, and K. Weaver
Preparatory Activity in Occipital Cortex in Early Blind Humans Predicts Auditory Perceptual Performance
J. Neurosci., October 3, 2007; 27(40): 10734 - 10741.
[Abstract] [Full Text] [PDF]
S. A. McMains, H. M. Fehd, T.-A. Emmanouil, and S. Kastner
Mechanisms of Feature- and Space-Based Attention: Response Modulation and Baseline Increases
J Neurophysiol, October 1, 2007; 98(4): 2110 - 2121.
[Abstract] [Full Text] [PDF]
C. Cadieu, M. Kouh, A. Pasupathy, C. E. Connor, M. Riesenhuber, and T. Poggio
A Model of V4 Shape Selectivity and Invariance
J Neurophysiol, September 1, 2007; 98(3): 1733 - 1750.
[Abstract] [Full Text] [PDF]
S. Ardid, X.-J. Wang, and A. Compte
An Integrated Microcircuit Model of Attentional Processing in the Neocortex
J. Neurosci., August 8, 2007; 27(32): 8486 - 8495.
[Abstract] [Full Text] [PDF]
D. Marinazzo, H. J. Kappen, and S. C. A. M. Gielen
Input-Driven Oscillations in Networks with Excitatory and Inhibitory Neurons with Dynamic Synapses.
Neural Comput., July 1, 2007; 19(7): 1739 - 1765.
[Abstract] [Full Text] [PDF]
M. J. Dubin and C. J. Duffy
Behavioral Influences on Cortical Neuronal Responses to Optic Flow
Cereb Cortex, July 1, 2007; 17(7): 1722 - 1732.
[Abstract] [Full Text] [PDF]
S. Jaramillo and B. A. Pearlmutter
Optimal Coding Predicts Attentional Modulation of Activity in Neural Systems
Neural Comput., May 1, 2007; 19(5): 1295 - 1312.
[Abstract] [Full Text] [PDF]
J. C. Alvarado, J. W. Vaughan, T. R. Stanford, and B. E. Stein
Multisensory Versus Unisensory Integration: Contrasting Modes in the Superior Colliculus
J Neurophysiol, May 1, 2007; 97(5): 3193 - 3205.
[Abstract] [Full Text] [PDF]
C. Jacques and B. Rossion
Electrophysiological Evidence for Temporal Dissociation between Spatial Attention and Sensory Competition during Human Face Processing
Cereb Cortex, May 1, 2007; 17(5): 1055 - 1065.
[Abstract] [Full Text] [PDF]
T. Serre, A. Oliva, and T. Poggio
A feedforward architecture accounts for rapid categorization
PNAS, April 10, 2007; 104(15): 6424 - 6429.
[Abstract] [Full Text] [PDF]
A. Maier, N. K. Logothetis, and D. A. Leopold
Context-dependent perceptual modulation of single neurons in primate visual cortex
PNAS, March 27, 2007; 104(13): 5620 - 5625.
[Abstract] [Full Text] [PDF]
M. Fallah, G. R. Stoner, and J. H. Reynolds
Stimulus-specific competitive selection in macaque extrastriate visual area V4
PNAS, March 6, 2007; 104(10): 4165 - 4169.
[Abstract] [Full Text] [PDF]
B. Rossion, D. Collins, V. Goffaux, and T. Curran
Long-term Expertise with Artificial Objects Increases Visual Competition with Early Face Categorization Processes.
J. Cogn. Neurosci., March 1, 2007; 19(3): 543 - 555.
[Abstract] [Full Text] [PDF]
N. W. Roach and J. H. Hogben
Impaired filtering of behaviourally irrelevant visual information in dyslexia
Brain, March 1, 2007; 130(3): 771 - 785.
[Abstract] [Full Text] [PDF]
J. T. Serences and S. Yantis
Spatially Selective Representations of Voluntary and Stimulus-Driven Attentional Priority in Human Occipital, Parietal, and Frontal Cortex
Cereb Cortex, February 1, 2007; 17(2): 284 - 293.
[Abstract] [Full Text] [PDF]
M. A. Silver, D. Ress, and D. J. Heeger
Neural Correlates of Sustained Spatial Attention in Human Early Visual Cortex
J Neurophysiol, January 1, 2007; 97(1): 229 - 237.
[Abstract] [Full Text] [PDF]
J. J. Geng, E. Eger, C. C. Ruff, A. Kristjansson, P. Rotshtein, and J. Driver
On-Line Attentional Selection From Competing Stimuli in Opposite Visual Fields: Effects on Human Visual Cortex and Control Processes
J Neurophysiol, November 1, 2006; 96(5): 2601 - 2612.
[Abstract] [Full Text] [PDF]
W. Suzuki, K. Matsumoto, and K. Tanaka
Neuronal Responses to Object Images in the Macaque Inferotemporal Cortex at Different Stimulus Discrimination Levels
J. Neurosci., October 11, 2006; 26(41): 10524 - 10535.
[Abstract] [Full Text] [PDF]
P. F Balan and J. Gottlieb
Integration of Exogenous Input into a Dynamic Salience Map Revealed by Perturbing Attention
J. Neurosci., September 6, 2006; 26(36): 9239 - 9249.
[Abstract] [Full Text] [PDF]
A. P. Sripati and K. O. Johnson
Dynamic Gain Changes During Attentional Modulation
Neural Comput., August 1, 2006; 18(8): 1847 - 1867.
[Abstract] [Full Text] [PDF]
S. Shomstein and M. Behrmann
Cortical systems mediating visual attention to both objects and spatial locations
PNAS, July 25, 2006; 103(30): 11387 - 11392.
[Abstract] [Full Text] [PDF]
T. Williford and J. H. R. Maunsell
Effects of spatial attention on contrast response functions in macaque area v4.
J Neurophysiol, July 1, 2006; 96(1): 40 - 54.
[Abstract] [Full Text] [PDF]
E. Shin, M. Fabiani, and G. Gratton
Multiple levels of stimulus representation in visual working memory.
J. Cogn. Neurosci., May 1, 2006; 18(5): 844 - 858.
[Abstract] [Full Text] [PDF]
A. C. Nobre, A. Rao, and L. Chelazzi
Selective attention to specific features within objects: behavioral and electrophysiological evidence.
J. Cogn. Neurosci., April 1, 2006; 18(4): 539 - 561.
[Abstract] [Full Text] [PDF]
X. Li, B. Kim, and M. A. Basso
Transient Pauses in Delay-Period Activity of Superior Colliculus Neurons
J Neurophysiol, April 1, 2006; 95(4): 2252 - 2264.
[Abstract] [Full Text] [PDF]
J.-M. Hopf, S. J. Luck, K. Boelmans, M. A. Schoenfeld, C. N. Boehler, J. Rieger, and H.-J. Heinze
The neural site of attention matches the spatial scale of perception.
J. Neurosci., March 29, 2006; 26(13): 3532 - 3540.
[Abstract] [Full Text] [PDF]
P. De Weerd, E. Smith, and P. Greenberg
Effects of Selective Attention on Perceptual Filling-in.
J. Cogn. Neurosci., March 1, 2006; 18(3): 335 - 347.
[Abstract] [Full Text] [PDF]
M. Bauer, R. Oostenveld, M. Peeters, and P. Fries
Tactile Spatial Attention Enhances Gamma-Band Activity in Somatosensory Cortex and Reduces Low-Frequency Activity in Parieto-Occipital Areas
J. Neurosci., January 11, 2006; 26(2): 490 - 501.
[Abstract] [Full Text] [PDF]
X. Li and M. A. Basso
Competitive Stimulus Interactions within Single Response Fields of Superior Colliculus Neurons
J. Neurosci., December 7, 2005; 25(49): 11357 - 11373.
[Abstract] [Full Text] [PDF]
P. H. E. Tiesinga
Stimulus Competition by Inhibitory Interference
Neural Comput., November 1, 2005; 17(11): 2421 - 2453.
[Abstract] [Full Text] [PDF]
J. E. Rollenhagen and C. R. Olson
Low-Frequency Oscillations Arising From Competitive Interactions Between Visual Stimuli in Macaque Inferotemporal Cortex
J Neurophysiol, November 1, 2005; 94(5): 3368 - 3387.
[Abstract] [Full Text] [PDF]
S. Moldakarimov, J. E. Rollenhagen, C. R. Olson, and C. C. Chow
Competitive Dynamics in Cortical Responses to Visual Stimuli
J Neurophysiol, November 1, 2005; 94(5): 3388 - 3396.
[Abstract] [Full Text] [PDF]
J. Hung, J. Driver, and V. Walsh
Visual Selection and Posterior Parietal Cortex: Effects of Repetitive Transcranial Magnetic Stimulation on Partial Report Analyzed by Bundesen's Theory of Visual Attention
J. Neurosci., October 19, 2005; 25(42): 9602 - 9612.
[Abstract] [Full Text] [PDF]
J.-D. Haynes, J. Tregellas, and G. Rees
Attentional integration between anatomically distinct stimulus representations in early visual cortex
PNAS, October 11, 2005; 102(41): 14925 - 14930.
[Abstract] [Full Text] [PDF]
E. P. Merriam and C. L. Colby
Active Vision in Parietal and Extrastriate Cortex
Neuroscientist, October 1, 2005; 11(5): 484 - 493.
[Abstract] [PDF]
D. Zoccolan, D. D. Cox, and J. J. DiCarlo
Multiple Object Response Normalization in Monkey Inferotemporal Cortex
J. Neurosci., September 7, 2005; 25(36): 8150 - 8164.
[Abstract] [Full Text] [PDF]
K. Taylor, S. Mandon, W.A. Freiwald, and A.K. Kreiter
Coherent Oscillatory Activity in Monkey Area V4 Predicts Successful Allocation of Attention
Cereb Cortex, September 1, 2005; 15(9): 1424 - 1437.
[Abstract] [Full Text] [PDF]
G. Deco and E. T. Rolls
Neurodynamics of Biased Competition and Cooperation for Attention: A Model With Spiking Neurons
J Neurophysiol, July 1, 2005; 94(1): 295 - 313.
[Abstract] [Full Text] [PDF]
I. Opris, A. Barborica, and V. P. Ferrera
Microstimulation of the Dorsolateral Prefrontal Cortex Biases Saccade Target Selection
J. Cogn. Neurosci., June 1, 2005; 17(6): 893 - 904.
[Abstract] [Full Text] [PDF]
S. Schwartz, P. Vuilleumier, C. Hutton, A. Maravita, R. J. Dolan, and J. Driver
Attentional Load and Sensory Competition in Human Vision: Modulation of fMRI Responses by Load at Fixation during Task-irrelevant Stimulation in the Peripheral Visual Field
Cereb Cortex, June 1, 2005; 15(6): 770 - 786.
[Abstract] [Full Text] [PDF]
C. Borgers, S. Epstein, and N. J. Kopell
Background gamma rhythmicity and attention in cortical local circuits: A computational study
PNAS, May 10, 2005; 102(19): 7002 - 7007.
[Abstract] [Full Text] [PDF]
B. Krekelberg and T. D. Albright
Motion Mechanisms in Macaque MT
J Neurophysiol, May 1, 2005; 93(5): 2908 - 2921.
[Abstract] [Full Text] [PDF]
N. P. Bichot, A. F. Rossi, and R. Desimone
Parallel and Serial Neural Mechanisms for Visual Search in Macaque Area V4
Science, April 22, 2005; 308(5721): 529 - 534.
[Abstract] [Full Text] [PDF]
F. H. Hamker
The Reentry Hypothesis: The Putative Interaction of the Frontal Eye Field, Ventrolateral Prefrontal Cortex, and Areas V4, IT for Attention and Eye Movement
Cereb Cortex, April 1, 2005; 15(4): 431 - 447.
[Abstract] [Full Text] [PDF]
E. A. Buffalo, G. Bertini, L. G. Ungerleider, and R. Desimone
Impaired Filtering of Distracter Stimuli by TE Neurons following V4 and TEO Lesions in Macaques
Cereb Cortex, February 1, 2005; 15(2): 141 - 151.
[Abstract] [Full Text] [PDF]
C. Constantinidis and M. A. Steinmetz
Posterior Parietal Cortex Automatically Encodes the Location of Salient Stimuli
J. Neurosci., January 5, 2005; 25(1): 233 - 238.
[Abstract] [Full Text] [PDF]
J. B. Rowe, K. E. Stephan, K. Friston, R. S.J. Frackowiak, and R. E. Passingham
The Prefrontal Cortex shows Context-specific Changes in Effective Connectivity to Motor or Visual Cortex during the Selection of Action or Colour
Cereb Cortex, January 1, 2005; 15(1): 85 - 95.
[Abstract] [Full Text] [PDF]
J. T. Serences, S. Yantis, A. Culberson, and E. Awh
Preparatory Activity in Visual Cortex Indexes Distractor Suppression During Covert Spatial Orienting
J Neurophysiol, December 1, 2004; 92(6): 3538 - 3545.
[Abstract] [Full Text] [PDF]
S. Shomstein and S. Yantis
Control of Attention Shifts between Vision and Audition in Human Cortex
J. Neurosci., November 24, 2004; 24(47): 10702 - 10706.
[Abstract] [Full Text] [PDF]
