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      Visual attention is not deployed at the endpoint of averaging saccades

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      PLoS Biology
      Public Library of Science

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          Abstract

          The premotor theory of attention postulates that spatial attention arises from the activation of saccade areas and that the deployment of attention is the consequence of motor programming. Yet attentional and oculomotor processes have been shown to be dissociable at the neuronal level in covert attention tasks. To investigate a potential dissociation at the behavioral level, we instructed human participants to move their eyes (saccade) towards 1 of 2 nearby, competing saccade targets. The spatial distribution of visual attention was determined using oriented visual stimuli presented either at the target locations, between them, or at several other equidistant locations. Results demonstrate that accurate saccades towards one of the targets were associated with presaccadic enhancement of visual sensitivity at the respective saccade endpoint compared to the nonsaccaded target location. In contrast, averaging saccades, landing between the 2 targets, were not associated with attentional facilitation at the saccade endpoint. Rather, attention before averaging saccades was equally deployed at the 2 target locations. Taken together, our results reveal that visual attention is not obligatorily coupled to the endpoint of a subsequent saccade. Rather, our results suggest that the oculomotor program depends on the state of attentional selection before saccade onset and that saccade averaging arises from unresolved attentional selection.

          Author summary

          The premotor theory of attention postulates that spatial visual attention is a consequence of the brain activity that controls eye movement. Indeed, attention and eye movement share overlapping brain networks, and attention is deployed at the target of an eye movement (saccade) even before the eyes start to move. But is attention always deployed at the endpoint of saccades? Here, we measured visual attention before accurate saccades and before saccades that landed in between 2 targets (averaging saccades). While accurate saccades were associated with a selective enhancement of visual sensitivity at their endpoint, no such enhancement was found at the endpoint of averaging saccades. Rather, visual sensitivity was evenly distributed across the 2 saccade targets, suggesting that saccade averaging arises from unresolved attentional selection. Overall, our results reveal that attention is not always coupled to the endpoint of saccades, arguing against a simplistic view of the premotor theory of attention at the behavioral level. Instead, we propose that saccadic responses depend on the state of attentional selection at saccade onset.

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          Most cited references76

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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, intention, and priority in the parietal lobe.

              For many years there has been a debate about the role of the parietal lobe in the generation of behavior. Does it generate movement plans (intention) or choose objects in the environment for further processing? To answer this, we focus on the lateral intraparietal area (LIP), an area that has been shown to play independent roles in target selection for saccades and the generation of visual attention. Based on results from a variety of tasks, we propose that LIP acts as a priority map in which objects are represented by activity proportional to their behavioral priority. We present evidence to show that the priority map combines bottom-up inputs like a rapid visual response with an array of top-down signals like a saccade plan. The spatial location representing the peak of the map is used by the oculomotor system to target saccades and by the visual system to guide visual attention.
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                Author and article information

                Contributors
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: InvestigationRole: MethodologyRole: Project administrationRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: ConceptualizationRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SupervisionRole: Writing – review & editing
                Role: ConceptualizationRole: Data curationRole: Formal analysisRole: Funding acquisitionRole: MethodologyRole: Project administrationRole: ResourcesRole: SoftwareRole: SupervisionRole: ValidationRole: VisualizationRole: Writing – review & editing
                Role: Academic Editor
                Journal
                PLoS Biol
                PLoS Biol
                plos
                plosbiol
                PLoS Biology
                Public Library of Science (San Francisco, CA USA )
                1544-9173
                1545-7885
                25 June 2018
                June 2018
                25 June 2018
                : 16
                : 6
                : e2006548
                Affiliations
                [1 ] Allgemeine und Experimentelle Psychologie, Ludwig-Maximilians-Universität München, Munich, Germany
                [2 ] Graduate School of Systemic Neurosciences, Ludwig-Maximilians-Universität München, Planegg-Martinsried, Germany
                [3 ] Department of Cognitive Psychology, Vrije Universiteit Amsterdam, Amsterdam, the Netherlands
                McGill University, Canada
                Author notes

                The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-3874-7949
                Article
                pbio.2006548
                10.1371/journal.pbio.2006548
                6034887
                29939986
                50678bd4-5250-4ae0-8393-8e495a4a83a0
                © 2018 Wollenberg et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 26 January 2018
                : 6 June 2018
                Page count
                Figures: 4, Tables: 0, Pages: 23
                Funding
                DFG, German Research Foundation www.dfg.de/en (grant number SZ343/1). received by Martin Szinte (M.S.). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. DFG, German Research Foundation www.dfg.de/en (grant number RTG 2175). received by Heiner Deubel (H.D.). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. DFG, German Research Foundation www.dfg.de/en (grant number DE336/5-1). received by Heiner Deubel (H.D.). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript. Marie Skłdowska-Curie Actions (Individual Fellowship) https://ec.europa.eu/research/mariecurieactions/actions/individual-fellowships_en (grant number 704537). received by Martin Szinte (M.S.). The funder had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
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