Literature DB >> 25535356

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

Catherine Perrodin1, Christoph Kayser2, Nikos K Logothetis3, Christopher I Petkov4.   

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.

Entities:  

Keywords:  communication; multisensory; neurons; oscillations; voice

Mesh:

Year:  2014        PMID: 25535356      PMCID: PMC4291635          DOI: 10.1073/pnas.1412817112

Source DB:  PubMed          Journal:  Proc Natl Acad Sci U S A        ISSN: 0027-8424            Impact factor:   11.205


  54 in total

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Review 3.  Multisensory integration: flexible use of general operations.

Authors:  Nienke van Atteveldt; Micah M Murray; Gregor Thut; Charles E Schroeder
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4.  Intermodal timing relations and audio-visual speech recognition by normal-hearing adults.

Authors:  M McGrath; Q Summerfield
Journal:  J Acoust Soc Am       Date:  1985-02       Impact factor: 1.840

5.  Cross-modal phase reset predicts auditory task performance in humans.

Authors:  Jeremy D Thorne; Maarten De Vos; Filipa Campos Viola; Stefan Debener
Journal:  J Neurosci       Date:  2011-03-09       Impact factor: 6.167

6.  The natural statistics of audiovisual speech.

Authors:  Chandramouli Chandrasekaran; Andrea Trubanova; Sébastien Stillittano; Alice Caplier; Asif A Ghazanfar
Journal:  PLoS Comput Biol       Date:  2009-07-17       Impact factor: 4.475

7.  Early auditory sensory processing of voices is facilitated by visual mechanisms.

Authors:  Sonja Schall; Stefan J Kiebel; Burkhard Maess; Katharina von Kriegstein
Journal:  Neuroimage       Date:  2013-04-04       Impact factor: 6.556

8.  Visual neurones responsive to faces in the monkey temporal cortex.

Authors:  D I Perrett; E T Rolls; W Caan
Journal:  Exp Brain Res       Date:  1982       Impact factor: 1.972

9.  A normalization model of multisensory integration.

Authors:  Tomokazu Ohshiro; Dora E Angelaki; Gregory C DeAngelis
Journal:  Nat Neurosci       Date:  2011-05-08       Impact factor: 24.884

10.  Eccentricity dependent auditory enhancement of visual stimulus detection but not discrimination.

Authors:  Stephanie Gleiss; Christoph Kayser
Journal:  Front Integr Neurosci       Date:  2013-07-19
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  19 in total

1.  Oscillatory phase shapes syllable perception.

Authors:  Sanne ten Oever; Alexander T Sack
Journal:  Proc Natl Acad Sci U S A       Date:  2015-12-14       Impact factor: 11.205

2.  The evolution of human communication.

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Journal:  J Cell Commun Signal       Date:  2015-02-25       Impact factor: 5.782

Review 3.  Prediction and constraint in audiovisual speech perception.

Authors:  Jonathan E Peelle; Mitchell S Sommers
Journal:  Cortex       Date:  2015-03-20       Impact factor: 4.027

4.  Are We Ready for Real-world Neuroscience?

Authors:  Pawel J Matusz; Suzanne Dikker; Alexander G Huth; Catherine Perrodin
Journal:  J Cogn Neurosci       Date:  2018-06-19       Impact factor: 3.225

5.  Investigating the Anterior Temporal Lobe With Direct Intracranial Recordings.

Authors:  Taylor J Abel; Ariane E Rhone; Kirill V Nourski; Matthew A Howard; Daniel Tranel
Journal:  Neurosurgery       Date:  2015-08       Impact factor: 4.654

6.  Socially meaningful visual context either enhances or inhibits vocalisation processing in the macaque brain.

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Journal:  Nat Commun       Date:  2022-08-19       Impact factor: 17.694

7.  Crossmodal Phase Reset and Evoked Responses Provide Complementary Mechanisms for the Influence of Visual Speech in Auditory Cortex.

Authors:  Pierre Mégevand; Manuel R Mercier; David M Groppe; Elana Zion Golumbic; Nima Mesgarani; Michael S Beauchamp; Charles E Schroeder; Ashesh D Mehta
Journal:  J Neurosci       Date:  2020-10-06       Impact factor: 6.167

8.  Beta modulation reflects name retrieval in the human anterior temporal lobe: an intracranial recording study.

Authors:  Taylor J Abel; Ariane E Rhone; Kirill V Nourski; Timothy K Ando; Hiroyuki Oya; Christopher K Kovach; Hiroto Kawasaki; Matthew A Howard; Daniel Tranel
Journal:  J Neurophysiol       Date:  2016-04-13       Impact factor: 2.714

9.  Gradient theories of brain activation: A novel application to studying the parental brain.

Authors:  Helena J V Rutherford; Jiansong Xu; Patrick D Worhunsky; Rubin Zhang; Sarah W Yip; Kristen P Morie; Vince D Calhoun; Sohye Kim; Lane Strathearn; Linda C Mayes; Marc N Potenza
Journal:  Curr Behav Neurosci Rep       Date:  2019-07-05

10.  Subcortical circuits mediate communication between primary sensory cortical areas in mice.

Authors:  Michael Lohse; Johannes C Dahmen; Victoria M Bajo; Andrew J King
Journal:  Nat Commun       Date:  2021-06-24       Impact factor: 14.919

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