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      Perisaccadic Updating of Visual Representations and Attentional States: Linking Behavior and Neurophysiology

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          Abstract

          During natural vision, saccadic eye movements lead to frequent retinal image changes that result in different neuronal subpopulations representing the same visual feature across fixations. Despite these potentially disruptive changes to the neural representation, our visual percept is remarkably stable. Visual receptive field remapping, characterized as an anticipatory shift in the position of a neuron’s spatial receptive field immediately before saccades, has been proposed as one possible neural substrate for visual stability. Many of the specific properties of remapping, e.g., the exact direction of remapping relative to the saccade vector and the precise mechanisms by which remapping could instantiate stability, remain a matter of debate. Recent studies have also shown that visual attention, like perception itself, can be sustained across saccades, suggesting that the attentional control system can also compensate for eye movements. Classical remapping could have an attentional component, or there could be a distinct attentional analog of visual remapping. At this time we do not yet fully understand how the stability of attentional representations relates to perisaccadic receptive field shifts. In this review, we develop a vocabulary for discussing perisaccadic shifts in receptive field location and perisaccadic shifts of attentional focus, review and synthesize behavioral and neurophysiological studies of perisaccadic perception and perisaccadic attention, and identify open questions that remain to be experimentally addressed.

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          Most cited references249

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          Visual attention: the past 25 years.

          This review focuses on covert attention and how it alters early vision. I explain why attention is considered a selective process, the constructs of covert attention, spatial endogenous and exogenous attention, and feature-based attention. I explain how in the last 25 years research on attention has characterized the effects of covert attention on spatial filters and how attention influences the selection of stimuli of interest. This review includes the effects of spatial attention on discriminability and appearance in tasks mediated by contrast sensitivity and spatial resolution; the effects of feature-based attention on basic visual processes, and a comparison of the effects of spatial and feature-based attention. The emphasis of this review is on psychophysical studies, but relevant electrophysiological and neuroimaging studies and models regarding how and where neuronal responses are modulated are also discussed. Copyright © 2011 Elsevier Ltd. All rights reserved.
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            Saccade target selection and object recognition: evidence for a common attentional mechanism.

            The spatial interaction of visual attention and saccadic eye movements was investigated in a dual-task paradigm that required a target-directed saccade in combination with a letter discrimination task. Subjects had to saccade to locations within horizontal letter strings left and right of a central fixation cross. The performance in discriminating between the symbols "E" and "E", presented tachistoscopically before the saccade within the surrounding distractors was taken as a measure of visual attention. The data show that visual discrimination is best when discrimination stimulus and saccade target refer to the same object; discrimination at neighboring items is close to chance level. Also, it is not possible, in spite of prior knowledge of discrimination target position, to direct attention to the discrimination target while saccading to a spatially close saccade target. The data strongly argue for an obligatory and selective coupling of saccade programming and visual attention to one common target object. The results favor a model in which a single attentional mechanism selects objects for perceptual processing and recognition, and also provides the information necessary for motor action.
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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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                Author and article information

                Contributors
                Journal
                Front Syst Neurosci
                Front Syst Neurosci
                Front. Syst. Neurosci.
                Frontiers in Systems Neuroscience
                Frontiers Media S.A.
                1662-5137
                05 February 2016
                2016
                : 10
                : 3
                Affiliations
                [1] 1Interdepartmental Neuroscience Program, Yale University New Haven, CT, USA
                [2] 2Medical Scientist Training Program, Yale University School of Medicine New Haven, CT, USA
                [3] 3Department of Neurobiology, Yale University School of Medicine New Haven, CT, USA
                [4] 4Department of Psychology, Yale University New Haven, CT, USA
                Author notes

                Edited by: Marc Zirnsak, Stanford University, USA

                Reviewed by: Marc A. Sommer, Duke University, USA; Sebastiaan Mathôt, Aix-Marseille Université, France

                *Correspondence: James A. Mazer james.mazer@ 123456yale.edu
                Article
                10.3389/fnsys.2016.00003
                4743436
                26903820
                15cd3a18-4865-4d79-83b0-b0b29a9739b0
                Copyright © 2016 Marino and Mazer.

                This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution and reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

                History
                : 05 October 2015
                : 15 January 2016
                Page count
                Figures: 4, Tables: 3, Equations: 0, References: 270, Pages: 21, Words: 18877
                Funding
                Funded by: National Eye Institute 10.13039/100000053
                Award ID: R01EY025103
                Funded by: National Institute of Mental Health 10.13039/100000025
                Award ID: F30MH102010
                Funded by: National Institutes of Health 10.13039/100000002
                Award ID: T32GM007205
                Categories
                Neuroscience
                Review

                Neurosciences
                saccades,visual attention,neurophysiology,visual psychophysics,visual perception,receptive fields,receptive field remapping

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