Electrophysiological Evidence of Early Cortical Sensitivity to Human Conspecific Mimic Voice as a Distinct Category of Natural Sound

Author:

Talkington William J.1,Donai Jeremy2,Kadner Alexandra S.1,Layne Molly L.1,Forino Andrew1,Wen Sijin3,Gao Si3,Gray Margeaux M.4,Ashraf Alexandria J.4,Valencia Gabriela N.1,Smith Brandon D.4,Khoo Stephanie K.4,Gray Stephen J.1,Lass Norman2,Brefczynski-Lewis Julie A.1,Engdahl Susannah1,Graham David5,Frum Chris A.1,Lewis James W.1ORCID

Affiliation:

1. Department of Neuroscience, Rockefeller Neuroscience Institute, West Virginia University, Morgantown

2. Department of Communication Sciences and Disorders, College of Education and Human Services, West Virginia University, Morgantown

3. Department of Biostatistics, West Virginia University, Morgantown

4. Department of Biology, Rockefeller Neuroscience Institute, West Virginia University, Morgantown

5. Department of Computer Science and Electrical Engineering, West Virginia University, Morgantown

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. Supplemental Material https://doi.org/10.23641/asha.12903839

Publisher

American Speech Language Hearing Association

Subject

Speech and Hearing,Linguistics and Language,Language and Linguistics

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