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Articles, Systems/Circuits

Modulation of Neuronal Responses by Exogenous Attention in Macaque Primary Visual Cortex

Feng Wang, Minggui Chen, Yin Yan, Li Zhaoping and Wu Li
Journal of Neuroscience 30 September 2015, 35 (39) 13419-13429; DOI: https://doi.org/10.1523/JNEUROSCI.0527-15.2015
Feng Wang
1State Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, and Center for Collaboration and Innovation in Brain and Learning Sciences, Beijing Normal University, Beijing 100875, China, and
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Minggui Chen
1State Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, and Center for Collaboration and Innovation in Brain and Learning Sciences, Beijing Normal University, Beijing 100875, China, and
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Yin Yan
1State Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, and Center for Collaboration and Innovation in Brain and Learning Sciences, Beijing Normal University, Beijing 100875, China, and
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Li Zhaoping
1State Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, and Center for Collaboration and Innovation in Brain and Learning Sciences, Beijing Normal University, Beijing 100875, China, and
2Department of Computer Science, University College London, London WC1E 6BT, United Kingdom
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Wu Li
1State Key Laboratory of Cognitive Neuroscience and Learning, IDG/McGovern Institute for Brain Research, and Center for Collaboration and Innovation in Brain and Learning Sciences, Beijing Normal University, Beijing 100875, China, and
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Abstract

Visual perception is influenced by attention deployed voluntarily or triggered involuntarily by salient stimuli. Modulation of visual cortical processing by voluntary or endogenous attention has been extensively studied, but much less is known about how involuntary or exogenous attention affects responses of visual cortical neurons. Using implanted microelectrode arrays, we examined the effects of exogenous attention on neuronal responses in the primary visual cortex (V1) of awake monkeys. A bright annular cue was flashed either around the receptive fields of recorded neurons or in the opposite visual field to capture attention. A subsequent grating stimulus probed the cue-induced effects. In a fixation task, when the cue-to-probe stimulus onset asynchrony (SOA) was <240 ms, the cue induced a transient increase of neuronal responses to the probe at the cued location during 40–100 ms after the onset of neuronal responses to the probe. This facilitation diminished and disappeared after repeated presentations of the same cue but recurred for a new cue of a different color. In another task to detect the probe, relative shortening of monkey's reaction times for the validly cued probe depended on the SOA in a way similar to the cue-induced V1 facilitation, and the behavioral and physiological cueing effects remained after repeated practice. Flashing two cues simultaneously in the two opposite visual fields weakened or diminished both the physiological and behavioral cueing effects. Our findings indicate that exogenous attention significantly modulates V1 responses and that the modulation strength depends on both novelty and task relevance of the stimulus.

SIGNIFICANCE STATEMENT Visual attention can be involuntarily captured by a sudden appearance of a conspicuous object, allowing rapid reactions to unexpected events of significance. The current study discovered a correlate of this effect in monkey primary visual cortex. An abrupt, salient, flash enhanced neuronal responses, and shortened the animal's reaction time, to a subsequent visual probe stimulus at the same location. However, the enhancement of the neural responses diminished after repeated exposures to this flash if the animal was not required to react to the probe. Moreover, a second, simultaneous, flash at another location weakened the neuronal and behavioral effects of the first one. These findings revealed, beyond the observations reported so far, the effects of exogenous attention in the brain.

  • awake monkey
  • cueing effects
  • exogenous attention
  • habituation
  • primary visual cortex
  • reaction time
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The Journal of Neuroscience: 35 (39)
Journal of Neuroscience
Vol. 35, Issue 39
30 Sep 2015
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Modulation of Neuronal Responses by Exogenous Attention in Macaque Primary Visual Cortex
Feng Wang, Minggui Chen, Yin Yan, Li Zhaoping, Wu Li
Journal of Neuroscience 30 September 2015, 35 (39) 13419-13429; DOI: 10.1523/JNEUROSCI.0527-15.2015

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Modulation of Neuronal Responses by Exogenous Attention in Macaque Primary Visual Cortex
Feng Wang, Minggui Chen, Yin Yan, Li Zhaoping, Wu Li
Journal of Neuroscience 30 September 2015, 35 (39) 13419-13429; DOI: 10.1523/JNEUROSCI.0527-15.2015
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Keywords

  • awake monkey
  • cueing effects
  • exogenous attention
  • habituation
  • primary visual cortex
  • reaction time

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