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      Predicting the Multisensory Consequences of One’s Own Action: BOLD Suppression in Auditory and Visual Cortices

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          Abstract

          Predictive mechanisms are essential to successfully interact with the environment and to compensate for delays in the transmission of neural signals. However, whether and how we predict multisensory action outcomes remains largely unknown. Here we investigated the existence of multisensory predictive mechanisms in a context where actions have outcomes in different modalities. During fMRI data acquisition auditory, visual and auditory-visual stimuli were presented in active and passive conditions. In the active condition, a self-initiated button press elicited the stimuli with variable short delays (0-417ms) between action and outcome, and participants had to detect the presence of a delay for auditory or visual outcome (task modality). In the passive condition, stimuli appeared automatically, and participants had to detect the number of stimulus modalities (unimodal/bimodal). For action consequences compared to identical but unpredictable control stimuli we observed suppression of the blood oxygen level depended (BOLD) response in a broad network including bilateral auditory and visual cortices. This effect was independent of task modality or stimulus modality and strongest for trials where no delay was detected (undetected<detected). In bimodal vs. unimodal conditions we found activation differences in the left cerebellum for detected vs. undetected trials and an increased cerebellar-sensory cortex connectivity. Thus, action-related predictive mechanisms lead to BOLD suppression in multiple sensory brain regions. These findings support the hypothesis of multisensory predictive mechanisms, which are probably conducted in the left cerebellum.

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          Most cited references55

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          Anterior cingulate conflict monitoring and adjustments in control.

          Conflict monitoring by the anterior cingulate cortex (ACC) has been posited to signal a need for greater cognitive control, producing neural and behavioral adjustments. However, the very occurrence of behavioral adjustments after conflict has been questioned, along with suggestions that there is no direct evidence of ACC conflict-related activity predicting subsequent neural or behavioral adjustments in control. Using the Stroop color-naming task and controlling for repetition effects, we demonstrate that ACC conflict-related activity predicts both greater prefrontal cortex activity and adjustments in behavior, supporting a role of ACC conflict monitoring in the engagement of cognitive control.
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            Central cancellation of self-produced tickle sensation.

            A self-produced tactile stimulus is perceived as less ticklish than the same stimulus generated externally. We used fMRI to examine neural responses when subjects experienced a tactile stimulus that was either self-produced or externally produced. More activity was found in somatosensory cortex when the stimulus was externally produced. In the cerebellum, less activity was associated with a movement that generated a tactile stimulus than with a movement that did not. This difference suggests that the cerebellum is involved in predicting the specific sensory consequences of movements, providing the signal that is used to cancel the sensory response to self-generated stimulation.
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              Multisensory Interplay Reveals Crossmodal Influences on ‘Sensory-Specific’ Brain Regions, Neural Responses, and Judgments

              Although much traditional sensory research has studied each sensory modality in isolation, there has been a recent explosion of interest in causal interplay between different senses. Various techniques have now identified numerous multisensory convergence zones in the brain. Some convergence may arise surprisingly close to low-level sensory-specific cortex, and some direct connections may exist even between primary sensory cortices. A variety of multisensory phenomena have now been reported in which sensory-specific brain responses and perceptual judgments concerning one sense can be affected by relations with other senses. We survey recent progress in this multisensory field, foregrounding human studies against the background of invasive animal work and highlighting possible underlying mechanisms. These include rapid feedforward integration, possible thalamic influences, and/or feedback from multisensory regions to sensory-specific brain areas. Multisensory interplay is more prevalent than classic modular approaches assumed, and new methods are now available to determine the underlying circuits.
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                Author and article information

                Contributors
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                6 January 2017
                2017
                : 12
                : 1
                : e0169131
                Affiliations
                [1 ]Philipps-University Marburg, Department of Psychiatry and Psychotherapy, Marburg, Germany
                [2 ]Justus-Liebig University, Department of Experimental Psychology, Giessen, Germany
                [3 ]AWO Centre of Psychiatry Halle, Clinic for Psychiatry and Psychotherapy, Halle, Germany
                [4 ]York University, Centre for Vision Research and Department of Psychology, Ontario, Canada
                Harvard Medical School, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                • Conceptualization: BS TK KF DTL LRH.

                • Data curation: BMvK BEA.

                • Formal analysis: BS BMvK.

                • Funding acquisition: BS TK KF DTL.

                • Investigation: BMvK BEA.

                • Methodology: BMvK BEA DTL.

                • Project administration: BS BMvK TK.

                • Resources: BS TK.

                • Software: BMvK BEA DTL.

                • Supervision: BS TK LRH.

                • Validation: BMvK BEA.

                • Visualization: BS BMvK.

                • Writing – original draft: BS.

                • Writing – review & editing: BS BMvK BEA LRH KF TK.

                Author information
                http://orcid.org/0000-0002-9837-0944
                Article
                PONE-D-16-33656
                10.1371/journal.pone.0169131
                5218407
                28060861
                69b80417-f923-496a-9aff-65eabf84316a
                © 2017 Straube 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
                : 23 August 2016
                : 12 December 2016
                Page count
                Figures: 6, Tables: 2, Pages: 25
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: INST 162/445-1; Subproject A3
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001659, Deutsche Forschungsgemeinschaft;
                Award ID: STR 1146/8-1
                Award Recipient :
                This work was supported by the “Deutsche Forschungsgemeinschaft” ( http://www.dfg.de/en/, grant numbers: SFB/TRR 135 INST 162/445-1, IRTG 1901 to BEA and STR-1146/8-1 to BS) and the Natural Sciences and Engineering Research Council (NSERC, http://www.nserc-crsng.gc.ca) of Canada to LRH. The funders had no role in study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Neuroscience
                Sensory Perception
                Vision
                Biology and Life Sciences
                Psychology
                Sensory Perception
                Vision
                Social Sciences
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                Sensory Perception
                Vision
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                Anatomy
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                Cerebral Cortex
                Cerebellum
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                Custom metadata
                Data are available from the Zenodo repository at the following URL: https://doi.org/10.5281/zenodo.202094.

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