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

Catherine Perrodin; Christoph Kayser; Nikos K Logothetis; Christopher I Petkov

doi:10.1073/pnas.1412817112

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

Journal article

Open access

Peer reviewed

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

Catherine Perrodin, Christoph Kayser, Nikos K Logothetis and Christopher I Petkov

Proceedings of the National Academy of Sciences - PNAS, Vol.112(1), pp.273-278

01/06/2015

DOI: 10.1073/pnas.1412817112

PMCID: PMC4291635

PMID: 25535356

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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.

Animal Communication

Animals

Auditory Perception - physiology

Brain - physiology

Evoked Potentials, Visual

Humans

Macaca mulatta - physiology

Male

Neurons - physiology

Sensation

Visual Perception - physiology

Voice

Details

Title: Subtitle: Natural asynchronies in audiovisual communication signals regulate neuronal multisensory interactions in voice-sensitive cortex
Creators: Catherine Perrodin - Max Planck Institute for Biological Cybernetics
Christoph Kayser - University of Glasgow
Nikos K Logothetis - Max Planck Institute for Biological Cybernetics
Christopher I Petkov - Newcastle University
Resource Type: Journal article
Publication Details: Proceedings of the National Academy of Sciences - PNAS, Vol.112(1), pp.273-278
DOI: 10.1073/pnas.1412817112
PMID: 25535356
PMCID: PMC4291635
NLM abbreviation: Proc Natl Acad Sci U S A
ISSN: 0027-8424
eISSN: 1091-6490
Grant note: WT102961MA / Wellcome Trust NC/K000608/1 / National Centre for the Replacement, Refinement and Reduction of Animals in Research WT092606/Z/10/Z / Wellcome Trust 102961/Z/13/Z / Wellcome Trust BB/L027534/1 / Biotechnology and Biological Sciences Research Council 102961 / Wellcome Trust
Language: English
Date published: 01/06/2015
Academic Unit: Iowa Neuroscience Institute; Neurosurgery; Otolaryngology
Record Identifier: 9984360132902771

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