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      Spatial attention enhances network, cellular and subthreshold responses in mouse visual cortex

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          Abstract

          Internal brain states strongly modulate sensory processing during behaviour. Studies of visual processing in primates show that attention to space selectively improves behavioural and neural responses to stimuli at the attended locations. Here we develop a visual spatial task for mice that elicits behavioural improvements consistent with the effects of spatial attention, and simultaneously measure network, cellular, and subthreshold activity in primary visual cortex. During trial-by-trial behavioural improvements, local field potential (LFP) responses to stimuli detected inside the receptive field (RF) strengthen. Moreover, detection inside the RF selectively enhances excitatory and inhibitory neuron responses to task-irrelevant stimuli and suppresses noise correlations and low frequency LFP fluctuations. Whole-cell patch-clamp recordings reveal that detection inside the RF increases synaptic activity that depolarizes membrane potential responses at the behaviorally relevant location. Our study establishes that mice display fundamental signatures of visual spatial attention spanning behavioral, network, cellular, and synaptic levels, providing new insight into rapid cognitive enhancement of sensory signals in visual cortex.

          Abstract

          Extensive research in primates shows that attention to space improves behavioural performance as well as neural responses to stimuli in that location. Here, the authors establish a visual spatial attention task in mice and report on attentional modulation of behaviour, as well as neural correlates from subthreshold responses in single cells to spikes and LFP at network level.

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          Most cited references57

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          Modulation of Oscillatory Neuronal Synchronization by Selective Visual Attention

          P. Fries (2001)
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            Attention improves performance primarily by reducing interneuronal correlations

            Visual attention can dramatically improve behavioural performance by allowing observers to focus on the important information in a complex scene. Attention also typically increases the firing rates of cortical sensory neurons. Rate increases improve the signal-to-noise ratio of individual neurons, and this improvement has been assumed to underlie attention-related improvements in behaviour. We recorded dozens of neurons simultaneously in visual area V4 and found that changes in single neurons accounted for only a small fraction of the improvement in the sensitivity of the population. Instead, over 80% of the attentional improvement in the population signal was caused by decreases in the correlations between the trial-to-trial fluctuations in the responses of pairs of neurons. These results suggest that the representation of sensory information in populations of neurons and the way attention affects the sensitivity of the population may only be understood by considering the interactions between neurons.
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              The normalization model of attention.

              Attention has been found to have a wide variety of effects on the responses of neurons in visual cortex. We describe a model of attention that exhibits each of these different forms of attentional modulation, depending on the stimulus conditions and the spread (or selectivity) of the attention field in the model. The model helps reconcile proposals that have been taken to represent alternative theories of attention. We argue that the variety and complexity of the results reported in the literature emerge from the variety of empirical protocols that were used, such that the results observed in any one experiment depended on the stimulus conditions and the subject's attentional strategy, a notion that we define precisely in terms of the attention field in the model, but that has not typically been completely under experimental control.
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                Author and article information

                Contributors
                bilal.haider@bme.gatech.edu
                Journal
                Nat Commun
                Nat Commun
                Nature Communications
                Nature Publishing Group UK (London )
                2041-1723
                24 January 2020
                24 January 2020
                2020
                : 11
                : 505
                Affiliations
                ISNI 0000 0001 2097 4943, GRID grid.213917.f, Georgia Institute of Technology & Emory University, ; Atlanta, GA USA
                Author information
                http://orcid.org/0000-0001-9238-1696
                Article
                14355
                10.1038/s41467-020-14355-4
                6981183
                31980628
                27bc075c-23aa-42d8-b7b5-5b338f1563b2
                © The Author(s) 2020

                Open Access This article is licensed under a Creative Commons Attribution 4.0 International License, which permits use, sharing, adaptation, distribution and reproduction in any medium or format, as long as you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. The images or other third party material in this article are included in the article’s Creative Commons license, unless indicated otherwise in a credit line to the material. If material is not included in the article’s Creative Commons license and your intended use is not permitted by statutory regulation or exceeds the permitted use, you will need to obtain permission directly from the copyright holder. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/.

                History
                : 31 May 2019
                : 2 January 2020
                Funding
                Funded by: FundRef https://doi.org/10.13039/100000065, U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (NINDS);
                Award ID: NS109978
                Award ID: NS107968
                Award Recipient :
                Funded by: FundRef https://doi.org/10.13039/100001391, Whitehall Foundation (Whitehall Foundation, Inc.);
                Funded by: FundRef https://doi.org/10.13039/100000879, Alfred P. Sloan Foundation;
                Funded by: U.S. Department of Health & Human Services | NIH | National Institute of Neurological Disorders and Stroke (NINDS)
                Categories
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                © The Author(s) 2020

                Uncategorized
                neural circuits,sensory processing,striate cortex
                Uncategorized
                neural circuits, sensory processing, striate cortex

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