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J Neurosci. 2019 Feb 6;39(6):1066-1076. doi: 10.1523/JNEUROSCI.2164-18.2018. Epub 2018 Dec 12.

Attention Enhances the Efficacy of Communication in V1 Local Circuits.

Author information

1
Physiology & Neurobiology Department, Geisel School of Medicine at Dartmouth, Lebanon, New Hampshire 03756.
2
Program in Experimental and Molecular Medicine, Dartmouth College, Hanover, New Hampshire 03755.
3
Ernest J. Del Monte Institute for Neuroscience, University of Rochester School of Medicine, Rochester, New York 14642.
4
Center for Neuroscience, University of California at Davis, Davis, California 95618.
5
Ernest J. Del Monte Institute for Neuroscience, University of Rochester School of Medicine, Rochester, New York 14642, farran_briggs@urmc.rochester.edu.
6
Department of Neuroscience, University of Rochester School of Medicine, Rochester, New York 14642.
7
Department of Brain and Cognitive Sciences, University of Rochester, Rochester, New York 14627, and.
8
Center for Visual Science, University of Rochester, Rochester, New York 14627.

Abstract

Attention is a critical component of visual perception; however, the mechanisms of attention at the granular level are poorly understood. One possible mechanism by which attention modulates neuronal activity is to control the efficacy of communication between connected neurons; however, it is unclear whether attention alters communication efficacy across a variety of neuronal circuits. In parallel, attentional modulation of neuronal firing rate is not uniform but depends upon the match between neuronal feature selectivity and the feature required for successful task completion. Here we tested whether modulation of communication efficacy is a viable mechanism of attention by assessing whether it is consistent across a variety of neuronal circuits and dependent upon the type of information conveyed in each circuit. We identified monosynaptically connected pairs of V1 neurons through cross-correlation of neuronal spike trains recorded in adult female macaque monkeys performing attention-demanding contrast-change detection tasks. Attention toward the stimulus in the receptive field of recorded neurons significantly facilitated the efficacy of communication among connected pairs of V1 neurons. The amount of attentional enhancement depended upon neuronal physiology, with larger facilitation for circuits conveying information about task-relevant features. Furthermore, presynaptic activity was more determinant of attentional enhancement of communication efficacy than postsynaptic activity, and feedforward local circuits often displayed the largest facilitation with attention. Together, these findings highlight attentional modulation of communication efficacy as a generalized mechanism of attention and demonstrate that attentional modulation at the granular level depends on the relevance of feature-specific information conveyed by neuronal circuits.SIGNIFICANCE STATEMENT How we pay attention to objects and locations in the visual environment has a profound impact on visual perception. Individual neurons in the visual cortex are similarly regulated by shifts in visual attention; however, the rules that govern whether and how attention alters neuronal activity are not known. In this study, we explored whether attention regulates communication between connected pairs of neurons in the primary visual cortex. We observed robust attentional facilitation of communication among these circuits. Furthermore, the extent to which the circuits were facilitated by attention depended on whether the information they conveyed was relevant for the particular attention task.

KEYWORDS:

V1; attention; efficacy; monosynaptic connection; receptive field properties

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