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      Perceptual Oscillation of Audiovisual Time Simultaneity

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          Abstract

          Action and perception are tightly coupled systems requiring coordination and synchronization over time. How the brain achieves synchronization is still a matter of debate, but recent experiments suggest that brain oscillations may play an important role in this process. Brain oscillations have been also proposed to be fundamental in determining time perception. Here, we had subjects perform an audiovisual temporal order judgment task to investigate the fine dynamics of temporal bias and sensitivity before and after the execution of voluntary hand movement (button-press). The reported order of the audiovisual sequence was rhythmically biased as a function of delay from hand action execution. Importantly, we found that it oscillated at a theta range frequency, starting ∼500 ms before and persisting ∼250 ms after the button-press, with consistent phase-locking across participants. Our results show that the perception of cross-sensory simultaneity oscillates rhythmically in synchrony with the programming phase of a voluntary action, demonstrating a link between action preparation and bias in temporal perceptual judgments.

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          Most cited references50

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          The phase of ongoing EEG oscillations predicts visual perception.

          Oscillations are ubiquitous in electrical recordings of brain activity. While the amplitude of ongoing oscillatory activity is known to correlate with various aspects of perception, the influence of oscillatory phase on perception remains unknown. In particular, since phase varies on a much faster timescale than the more sluggish amplitude fluctuations, phase effects could reveal the fine-grained neural mechanisms underlying perception. We presented brief flashes of light at the individual luminance threshold while EEG was recorded. Although the stimulus on each trial was identical, subjects detected approximately half of the flashes (hits) and entirely missed the other half (misses). Phase distributions across trials were compared between hits and misses. We found that shortly before stimulus onset, each of the two distributions exhibited significant phase concentration, but at different phase angles. This effect was strongest in the theta and alpha frequency bands. In this time-frequency range, oscillatory phase accounted for at least 16% of variability in detection performance and allowed the prediction of performance on the single-trial level. This finding indicates that the visual detection threshold fluctuates over time along with the phase of ongoing EEG activity. The results support the notion that ongoing oscillations shape our perception, possibly by providing a temporal reference frame for neural codes that rely on precise spike timing.
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            Neuronal oscillations and multisensory interaction in primary auditory cortex.

            Recent anatomical, physiological, and neuroimaging findings indicate multisensory convergence at early, putatively unisensory stages of cortical processing. The objective of this study was to confirm somatosensory-auditory interaction in A1 and to define both its physiological mechanisms and its consequences for auditory information processing. Laminar current source density and multiunit activity sampled during multielectrode penetrations of primary auditory area A1 in awake macaques revealed clear somatosensory-auditory interactions, with a novel mechanism: somatosensory inputs appear to reset the phase of ongoing neuronal oscillations, so that accompanying auditory inputs arrive during an ideal, high-excitability phase, and produce amplified neuronal responses. In contrast, responses to auditory inputs arriving during the opposing low-excitability phase tend to be suppressed. Our findings underscore the instrumental role of neuronal oscillations in cortical operations. The timing and laminar profile of the multisensory interactions in A1 indicate that nonspecific thalamic systems may play a key role in the effect.
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              Perceptual Cycles.

              Brain function involves oscillations at various frequencies. This could imply that perception and cognition operate periodically, as a succession of cycles mirroring the underlying oscillations. This age-old notion of discrete perception has resurfaced in recent years, fueled by advances in neuroscientific techniques. Contrary to earlier views of discrete perception as a unitary sampling rhythm, contemporary evidence points not to one but several rhythms of perception that may depend on sensory modality, task, stimulus properties, or brain region. In vision, for example, a sensory alpha rhythm (∼10Hz) may coexist with at least one more rhythm performing attentional sampling at around 7Hz. How these multiple periodic functions are orchestrated, and how internal sampling rhythms coordinate with overt sampling behavior, remain open questions.
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                Author and article information

                Journal
                eNeuro
                eNeuro
                eneuro
                eneuro
                eNeuro
                eNeuro
                Society for Neuroscience
                2373-2822
                21 May 2018
                25 May 2018
                May-Jun 2018
                : 5
                : 3
                : ENEURO.0047-18.2018
                Affiliations
                [1 ]Dipartimento Di Ricerca Traslazionale e Delle Nuove Tecnologie in Medicina e Chirurgia, Università Di Pisa , via San Zeno 31, Pisa, 56123, Italy
                [2 ]Istituto Di Neuroscienze, Consiglio Nazionale Delle Ricerche (CNR) , via Moruzzi 1, Pisa, 56124, Italy
                [3 ]Dipartimento Di Psicologia, Farmacologia e Salute Del Bambino (NEUROFARBA), Università Di Firenze , via San Salvi 12, Firenze, 50135, Italy
                [4 ]IRCCS Stella-Maris , Viale Del Tirreno 331, Pisa, 56018, Italy Calambrone
                Author notes

                The authors declare no competing financial interests.

                Author contributions: A.B. performed research. All authors designed research, analyzed data, and wrote the paper.

                This work was supported by the European Research Council (FP7 ECSPLAIN Grant 338866 to M.C.M.).

                Correspondence should be addressed to Maria Concetta Morrone, Department of Translational Research on New Technologies in Medicines and Surgery, University of Pisa, via San Zeno 31, 56123 Pisa, Italy. E-mail: concetta@ 123456in.cnr.it .
                Author information
                http://orcid.org/0000-0002-9713-1300
                http://orcid.org/0000-0003-1541-8832
                http://orcid.org/0000-0002-1025-0316
                Article
                eN-NWR-0047-18
                10.1523/ENEURO.0047-18.2018
                5969321
                acaa6c56-fddf-445f-9b74-f863d1f3c978
                Copyright © 2018 Benedetto et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

                History
                : 29 January 2018
                : 9 March 2018
                : 17 March 2018
                Page count
                Figures: 5, Tables: 0, Equations: 22, References: 71, Pages: 12, Words: 7844
                Funding
                Funded by: ERC | European Research Council
                Award ID: 338866
                Categories
                8
                8.1
                New Research
                Sensory and Motor Systems
                Custom metadata
                May/June 2018

                audiovisual,behavioral oscillations,decision bias,simultaneity,theta,time perception

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