Electrophysiological evidence of early cortical sensitivity to human conspecific mimic voice as a distinct category of natural sound

William J. Talkington, Jeremy Donai, Alexandra S. Kadner, Molly L. Layne, Andrew Forino, Sijin Wen, Si Gao, Margeaux M. Gray, Alexandria J. Ashraf, Gabriela N. Valencia, Brandon D. Smith, Stephanie K. Khoo, Stephen J. Gray, Norman Lass, Julie A. Brefczynski-Lewis, Susannah Engdahl, David Graham, Chris A. Frum, James W. Lewis

Research output: Contribution to journalArticlepeer-review

1 Scopus citations

Abstract

Purpose: From an anthropological perspective of hominin communication, the human auditory system likely evolved to enable special sensitivity to sounds produced by the vocal tracts of human conspecifics whether attended or passively heard. While numerous electrophysiological studies have used stereotypical human-produced verbal (speech voice and singing voice) and nonverbal vocalizations to identify human voice–sensitive responses, controversy remains as to when (and where) processing of acoustic signal attributes characteristic of “human voiceness” per se initiate in the brain. Method: To explore this, we used animal vocalizations and human-mimicked versions of those calls (“mimic voice”) to examine late auditory evoked potential responses in humans. Results: Here, we revealed an N1b component (96–120 ms poststimulus) during a nonattending listening condition showing significantly greater magnitude in response to mimics, beginning as early as primary auditory cortices, preceding the time window reported in previous studies that revealed species-specific vocalization processing initiating in the range of 147–219 ms. During a sound discrimination task, a P600 (500–700 ms poststimulus) component showed specificity for accurate discrimination of human mimic voice. Distinct acoustic signal attributes and features of the stimuli were used in a classifier model, which could distinguish most human from animal voice comparably to behavioral data—though none of these single features could adequately distinguish human voiceness. Conclusions: These results provide novel ideas for algorithms used in neuromimetic hearing aids, as well as direct electrophysiological support for a neurocognitive model of natural sound processing that informs both neurodevelopmental and anthropological models regarding the establishment of auditory communication systems in humans.

Original languageEnglish (US)
Pages (from-to)3539-3559
Number of pages21
JournalJournal of Speech, Language, and Hearing Research
Volume63
Issue number10
DOIs
StatePublished - Oct 2020

All Science Journal Classification (ASJC) codes

  • Language and Linguistics
  • Linguistics and Language
  • Speech and Hearing

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