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Visual speech differentially modulates beta, theta, and high gamma bands in auditory cortex

Karthik Ganesan, John Plass, Adriene M. Beltz, Zhongming Liu, Marcia Grabowecky, Satoru Suzuki, William C. Stacey, Vibhangini S. Wasade, Vernon L. Towle, James X Tao, Shasha Wu, Naoum P Issa, David Brang
doi: https://doi.org/10.1101/2020.09.07.284455
Karthik Ganesan
1University of Michigan, Ann Arbor, MI 48109
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John Plass
1University of Michigan, Ann Arbor, MI 48109
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Adriene M. Beltz
1University of Michigan, Ann Arbor, MI 48109
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Zhongming Liu
1University of Michigan, Ann Arbor, MI 48109
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Marcia Grabowecky
2Northwestern University, Evanston, IL 60208
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Satoru Suzuki
2Northwestern University, Evanston, IL 60208
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William C. Stacey
1University of Michigan, Ann Arbor, MI 48109
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Vibhangini S. Wasade
3Henry Ford Hospital, Detroit, MI 48202
4Department of Neurology, Wayne State University School of Medicine, MI 48201
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Vernon L. Towle
5Department of Neurology, The University of Chicago, Chicago, IL 60637
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James X Tao
5Department of Neurology, The University of Chicago, Chicago, IL 60637
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Shasha Wu
5Department of Neurology, The University of Chicago, Chicago, IL 60637
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Naoum P Issa
5Department of Neurology, The University of Chicago, Chicago, IL 60637
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David Brang
1University of Michigan, Ann Arbor, MI 48109
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  • For correspondence: djbrang@umich.edu
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Abstract

Speech perception is a central component of social communication. While speech perception is primarily driven by sounds, accurate perception in everyday settings is also supported by meaningful information extracted from visual cues (e.g., speech content, timing, and speaker identity). Previous research has shown that visual speech modulates activity in cortical areas subserving auditory speech perception, including the superior temporal gyrus (STG), likely through feedback connections from the multisensory posterior superior temporal sulcus (pSTS). However, it is unknown whether visual modulation of auditory processing in the STG is a unitary phenomenon or, rather, consists of multiple temporally, spatially, or functionally discrete processes. To explore these questions, we examined neural responses to audiovisual speech in electrodes implanted intracranially in the temporal cortex of 21 patients undergoing clinical monitoring for epilepsy. We found that visual speech modulates auditory processes in the STG in multiple ways, eliciting temporally and spatially distinct patterns of activity that differ across theta, beta, and high-gamma frequency bands. Before speech onset, visual information increased high-gamma power in the posterior STG and suppressed beta power in mid-STG regions, suggesting crossmodal prediction of speech signals in these areas. After sound onset, visual speech decreased theta power in the middle and posterior STG, potentially reflecting a decrease in sustained feedforward auditory activity. These results are consistent with models that posit multiple distinct mechanisms supporting audiovisual speech perception.

Significance Statement Visual speech cues are often needed to disambiguate distorted speech sounds in the natural environment. However, understanding how the brain encodes and transmits visual information for usage by the auditory system remains a challenge. One persistent question is whether visual signals have a unitary effect on auditory processing or elicit multiple distinct effects throughout auditory cortex. To better understand how vision modulates speech processing, we measured neural activity produced by audiovisual speech from electrodes surgically implanted in auditory areas of 21 patients with epilepsy. Group-level statistics using linear mixed-effects models demonstrated distinct patterns of activity across different locations, timepoints, and frequency bands, suggesting the presence of multiple audiovisual mechanisms supporting speech perception processes in auditory cortex.

Competing Interest Statement

The authors have declared no competing interest.

Footnotes

  • Conflict of Interest Statement The authors declare no competing financial interests.

Copyright 
The copyright holder for this preprint is the author/funder, who has granted bioRxiv a license to display the preprint in perpetuity. It is made available under a CC-BY-NC-ND 4.0 International license.
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Posted September 07, 2020.
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Visual speech differentially modulates beta, theta, and high gamma bands in auditory cortex
Karthik Ganesan, John Plass, Adriene M. Beltz, Zhongming Liu, Marcia Grabowecky, Satoru Suzuki, William C. Stacey, Vibhangini S. Wasade, Vernon L. Towle, James X Tao, Shasha Wu, Naoum P Issa, David Brang
bioRxiv 2020.09.07.284455; doi: https://doi.org/10.1101/2020.09.07.284455
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Visual speech differentially modulates beta, theta, and high gamma bands in auditory cortex
Karthik Ganesan, John Plass, Adriene M. Beltz, Zhongming Liu, Marcia Grabowecky, Satoru Suzuki, William C. Stacey, Vibhangini S. Wasade, Vernon L. Towle, James X Tao, Shasha Wu, Naoum P Issa, David Brang
bioRxiv 2020.09.07.284455; doi: https://doi.org/10.1101/2020.09.07.284455

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