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      Conflict-sensitive neurons gate interocular suppression in human visual cortex

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          Abstract

          Neural suppression plays an important role in cortical function, including sensory, memory, and motor systems. It remains, however, relatively poorly understood. A paradigmatic case arises when conflicting images are presented to the two eyes. These images can compete for awareness, and one is usually strongly suppressed. The mechanisms that resolve such interocular conflict remain unclear. Suppression could arise solely from “winner-take-all” competition between neurons responsive to each eye. Alternatively, suppression could also depend upon neurons detecting interocular conflict. Here, we provide physiological evidence in human visual cortex for the latter: suppression depends upon conflict-sensitive neurons. We recorded steady-state visual evoked potentials (SSVEP), and used the logic of selective adaptation. The amplitude of SSVEP responses at intermodulation frequencies strengthened as interocular conflict in the stimulus increased, suggesting the presence of neurons responsive to conflict. Critically, adaptation to conflict both reduced this SSVEP effect, and increased the amount of conflict needed to produce perceptual suppression. The simplest account of these results is that interocular-conflict-sensitive neurons exist in human cortex: adaptation likely reduced the responsiveness of these neurons which in turn raised the amount of conflict required to produce perceptual suppression. Similar mechanisms may be used to resolve other varieties of perceptual conflict.

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          Most cited references36

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          Neural bases of binocular rivalry.

          During binocular rivalry, conflicting monocular images compete for access to consciousness in a stochastic, dynamical fashion. Recent human neuroimaging and psychophysical studies suggest that rivalry entails competitive interactions at multiple neural sites, including sites that retain eye-selective information. Rivalry greatly suppresses activity in the ventral pathway and attenuates visual adaptation to form and motion; nonetheless, some information about the suppressed stimulus reaches higher brain areas. Although rivalry depends on low-level inhibitory interactions, high-level excitatory influences promoting perceptual grouping and selective attention can extend the local dominance of a stimulus over space and time. Inhibitory and excitatory circuits considered within a hybrid model might account for the paradoxical properties of binocular rivalry and provide insights into the neural bases of visual awareness itself.
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            What is rivalling during binocular rivalry?

            When different images are presented to the two eyes, they compete for perceptual dominance, such that one image is visible while the other is suppressed. This binocular rivalry is thought to reflect competition between monocular neurons within the primary visual cortex. However, neurons whose activity correlates with perception during rivalry are found mainly in higher cortical areas, and respond to input from both eyes. Thus rivalry may involve competition between alternative perceptual interpretations at a higher level of analysis. To investigate this, we tested the effect of rapidly alternating the rival stimuli between the two eyes. Under these conditions, the perceptual alternations exhibit the same temporal dynamics as with static patterns, and a single phase of perceptual dominance can span multiple alternations of the stimuli. Thus neural representations of the two stimuli compete for visual awareness independently of the eye through which they reach the higher visual areas. This finding places binocular rivalry in the general category of multistable phenomena, such as ambiguous figures, and provides a new way to study the neural cause and resolution of perceptual ambiguities.
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              Computational evidence for a rivalry hierarchy in vision.

              Cortical-form vision comprises multiple, hierarchically arranged areas with feedforward and feedback interconnections. This complex architecture poses difficulties for attempts to link perceptual phenomena to activity at a particular level of the system. This difficulty has been especially salient in studies of binocular rivalry alternations, where there is seemingly conflicting evidence for a locus in primary visual cortex or alternatively in higher cortical areas devoted to object perception. Here, I use a competitive neural model to demonstrate that the data require at least two hierarchic rivalry stages for their explanation. This model demonstrates that competitive inhibition in the first rivalry stage can be eliminated by using suitable stimulus dynamics, thereby revealing properties of a later stage, a result obtained with both spike-rate and conductance-based model neurons. This result provides a synthesis of competing rivalry theories and suggests that neural competition may be a general characteristic throughout the form-vision hierarchy.
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                Author and article information

                Contributors
                sucharit.katyal@inserm.fr
                Journal
                Sci Rep
                Sci Rep
                Scientific Reports
                Nature Publishing Group UK (London )
                2045-2322
                19 January 2018
                19 January 2018
                2018
                : 8
                Affiliations
                [1 ]ISNI 0000000419368657, GRID grid.17635.36, Department of Psychology, , University of Minnesota Twin Cities, ; Minneapolis, MN 55455 USA
                [2 ]ISNI 0000000419368657, GRID grid.17635.36, Department of Biomedical Engineering, , University of Minnesota Twin Cities, ; Minneapolis, MN 55455 USA
                Article
                19809
                10.1038/s41598-018-19809-w
                5775389
                29352155
                ba0a743a-b59f-4f28-83d1-b46db4be7c1b
                © The Author(s) 2018

                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/.

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