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Research Article: New Research, Sensory and Motor Systems

Neural correlates of vocal auditory feedback processing: Unique insights from electrocorticography recordings in a human cochlear implant user

Charles A. Miller, Roozbeh Behroozmand, Christine P. Etler, Kirill V. Nourski, Richard A. Reale, Hiroyuki Oya, Hiroto Kawasaki and Jeremy D. W. Greenlee
eNeuro 8 January 2021, ENEURO.0181-20.2020; DOI: https://doi.org/10.1523/ENEURO.0181-20.2020
Charles A. Miller
1Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, Iowa, USA
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Roozbeh Behroozmand
2Speech Neuroscience Laboratory, Department of Communication Sciences and Disorders, University of South Carolina, Columbia, South Carolina, USA
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Christine P. Etler
3Department of Otolaryngology – Head and Neck Surgery, The University of Iowa, Iowa City, Iowa, USA
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Kirill V. Nourski
1Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, Iowa, USA
4Iowa Neuroscience Institute, The University of Iowa, Iowa City, Iowa, USA
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Richard A. Reale
1Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, Iowa, USA
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Hiroyuki Oya
1Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, Iowa, USA
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Hiroto Kawasaki
1Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, Iowa, USA
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Jeremy D. W. Greenlee
1Human Brain Research Laboratory, Department of Neurosurgery, The University of Iowa, Iowa City, Iowa, USA
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ABSTRACT

There is considerable interest in understanding cortical processing and the function of top-down and bottom-up human neural circuits that control speech production. Research efforts to investigate these circuits are aided by analysis of spectro-temporal response characteristics of neural activity recorded by electrocorticography (ECoG). Further, cortical processing may be altered in the case of hearing impaired cochlear implant (CI) users, as electric excitation of the auditory nerve creates a markedly different neural code for speech compared to that of the functionally intact hearing system. Studies of cortical activity in CI users typically record scalp potentials and are hampered by stimulus artifact contamination and by spatio-temporal filtering imposed by the skull. We present a unique case of a CI user who required direct recordings from the cortical surface using subdural electrodes implanted for epilepsy assessment. Using experimental conditions where the subject vocalized in the presence (CIs ON) or absence (CIs OFF) of auditory feedback, or listened to playback of self-vocalizations without production, we observed ECoG activity primarily in gamma (32-70 Hz) and high gamma (70-150 Hz) bands at focal regions on the lateral surface of the superior temporal gyrus (STG). High gamma band responses differed in their amplitudes across conditions and cortical sites, possibly reflecting different rates of stimulus presentation and differing levels of neural adaptation. STG gamma responses to playback and vocalization with auditory feedback were not different from responses to vocalization without feedback, indicating this activity reflects not only auditory, but also attentional, efference-copy, and sensorimotor processing during speech production.

Significance statement This unique study directly examined cortical activity during speech vowel sound vocalization and listening tasks in a deaf subject with bilateral cochlear implants and medically intractable epilepsy. Because the subject could not experience bone or air-conducted auditory feedback, unique insights into speech production were made possible. Our findings demonstrate that gamma activity in the superior temporal gyrus reflects a combination of auditory and non-auditory related activation of the auditory cortex during speech production.

  • epilepsy surgery
  • hearing loss
  • speech production.

Footnotes

  • Authors report no conflict of interest.

  • NIH/ NIDCD grants DC015260 and DC00429

This is an open-access article distributed under the terms of the Creative Commons Attribution 4.0 International license, which permits unrestricted use, distribution and reproduction in any medium provided that the original work is properly attributed.

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Neural correlates of vocal auditory feedback processing: Unique insights from electrocorticography recordings in a human cochlear implant user
Charles A. Miller, Roozbeh Behroozmand, Christine P. Etler, Kirill V. Nourski, Richard A. Reale, Hiroyuki Oya, Hiroto Kawasaki, Jeremy D. W. Greenlee
eNeuro 8 January 2021, ENEURO.0181-20.2020; DOI: 10.1523/ENEURO.0181-20.2020

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Neural correlates of vocal auditory feedback processing: Unique insights from electrocorticography recordings in a human cochlear implant user
Charles A. Miller, Roozbeh Behroozmand, Christine P. Etler, Kirill V. Nourski, Richard A. Reale, Hiroyuki Oya, Hiroto Kawasaki, Jeremy D. W. Greenlee
eNeuro 8 January 2021, ENEURO.0181-20.2020; DOI: 10.1523/ENEURO.0181-20.2020
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Keywords

  • epilepsy surgery
  • hearing loss
  • speech production.

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