Natural asynchronies in audiovisual communication signals regulate neuronal multisensory interactions in voice-sensitive cortex

Perrodin, C., Kayser, C., Logothetis, N. K. and Petkov, C. I. (2015) Natural asynchronies in audiovisual communication signals regulate neuronal multisensory interactions in voice-sensitive cortex. Proceedings of the National Academy of Sciences of the United States of America, 112(1), pp. 273-278. (doi: 10.1073/pnas.1412817112) (PMID:25535356) (PMCID:PMC4291635)

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Publisher's URL: http://dx.doi.org/10.1073/pnas.1412817112

Abstract

When social animals communicate, the onset of informative content in one modality varies considerably relative to the other, such as when visual orofacial movements precede a vocalization. These naturally occurring asynchronies do not disrupt intelligibility or perceptual coherence. However, they occur on time scales where they likely affect integrative neuronal activity in ways that have remained unclear, especially for hierarchically downstream regions in which neurons exhibit temporally imprecise but highly selective responses to communication signals. To address this, we exploited naturally occurring face- and voice-onset asynchronies in primate vocalizations. Using these as stimuli we recorded cortical oscillations and neuronal spiking responses from functional MRI (fMRI)-localized voice-sensitive cortex in the anterior temporal lobe of macaques. We show that the onset of the visual face stimulus resets the phase of low-frequency oscillations, and that the face–voice asynchrony affects the prominence of two key types of neuronal multisensory responses: enhancement or suppression. Our findings show a three-way association between temporal delays in audiovisual communication signals, phase-resetting of ongoing oscillations, and the sign of multisensory responses. The results reveal how natural onset asynchronies in cross-sensory inputs regulate network oscillations and neuronal excitability in the voice-sensitive cortex of macaques, a suggested animal model for human voice areas. These findings also advance predictions on the impact of multisensory input on neuronal processes in face areas and other brain regions.

Item Type:Articles
Status:Published
Refereed:Yes
Glasgow Author(s) Enlighten ID:Kayser, Professor Christoph
Authors: Perrodin, C., Kayser, C., Logothetis, N. K., and Petkov, C. I.
College/School:College of Medical Veterinary and Life Sciences > School of Psychology & Neuroscience
Journal Name:Proceedings of the National Academy of Sciences of the United States of America
Publisher:National Academy of Sciences
ISSN:0027-8424
ISSN (Online):1091-6490
Copyright Holders:Copyright © 2015 The Authors
First Published:First published in Proceedings of the National Academy of Sciences of the United States of America 112(1):273-278
Publisher Policy:Reproduced under a Creative Commons License
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Project CodeAward NoProject NamePrincipal InvestigatorFunder's NameFunder RefLead Dept
658701Pathways and mechanisms underlying the visual enhancement of hearing in challenging environments.Christoph KayserBiotechnology and Biological Sciences Research Council (BBSRC)BB/L027534/1INP - CENTRE FOR COGNITIVE NEUROIMAGING