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Proc Natl Acad Sci U S A. 2015 Jan 6;112(1):273-8. doi: 10.1073/pnas.1412817112. Epub 2014 Dec 22.

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

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Department of Physiology of Cognitive Processes, Max Planck Institute for Biological Cybernetics, 72076 Tübingen, Germany;
Institute of Neuroscience and Psychology, University of Glasgow, Glasgow G12 8QB, United Kingdom;
Department of Physiology of Cognitive Processes, Max Planck Institute for Biological Cybernetics, 72076 Tübingen, Germany; Division of Imaging Science and Biomedical Engineering, University of Manchester, Manchester M13 9PT, United Kingdom; and.
Institute of Neuroscience, Newcastle University Medical School, Newcastle upon Tyne NE2 4HH, United Kingdom


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.


communication; multisensory; neurons; oscillations; voice

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