Abstract

The neural mechanisms underlying processing of auditory feedback during self-vocalization are poorly understood. One technique used to study the role of auditory feedback involves shifting the pitch of the feedback that a speaker receives, known as pitch-shifted feedback. We utilized a pitch shift self-vocalization and playback paradigm to investigate the underlying neural mechanisms of audio-vocal interaction. High-resolution electrocorticography (ECoG) signals were recorded directly from auditory cortex of 10 human subjects while they vocalized and received brief downward (−100 cents) pitch perturbations in their voice auditory feedback (speaking task). ECoG was also recorded when subjects passively listened to playback of their own pitch-shifted vocalizations. Feedback pitch perturbations elicited average evoked potential (AEP) and event-related band power (ERBP) responses, primarily in the high gamma (70–150 Hz) range, in focal areas of non-primary auditory cortex on superior temporal gyrus (STG). The AEPs and high gamma responses were both modulated by speaking compared with playback in a subset of STG contacts. From these contacts, a majority showed significant enhancement of high gamma power and AEP responses during speaking while the remaining contacts showed attenuated response amplitudes. The speaking-induced enhancement effect suggests that engaging the vocal motor system can modulate auditory cortical processing of self-produced sounds in such a way as to increase neural sensitivity for feedback pitch error detection. It is likely that mechanisms such as efference copies may be involved in this process, and modulation of AEP and high gamma responses imply that such modulatory effects may affect different cortical generators within distinctive functional networks that drive voice production and control.

Highlights

  • In order to maintain effective vocal communication, the brain needs to finely control the acoustical parameters of self-generated vocal sounds

  • Further analysis showed that the significant increases in power were most prominent in the high gamma (70–150 Hz) range, and from the anatomical standpoint, these responses were closely co-localized with areas of significant average evoked potential (AEP) responses during both speaking and playback

  • We found that the pitch-shift stimuli elicit AEP responses within non-primary areas of human auditory cortex that are enhanced during active vocal production of a vowel sound as compared to passive listening to playback of the same self-produced vocalizations

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Summary

Introduction

In order to maintain effective vocal communication, the brain needs to finely control the acoustical parameters of self-generated vocal sounds. Electrophysiological recordings in animals [10,11,12] and humans [13,14,15,16,17,18,19] have shown that the auditory cortical responses to normal (unaltered) voice feedback are attenuated during active vocal production compared with passive listening to the playback of selfproduced voice This effect is suggested to be associated with motor-driven mechanisms (e.g. efference copies) that suppress neural responses to predictable sensory feedback input. When a pitch perturbation was applied to voice auditory feedback, some auditory cortical responses were found to be enhanced during active vocalization compared with passive listening to playback [21,22] These findings suggest that efference projections originating from motor-related areas may change tuning properties of auditory cortical neurons in such a way as to increase their sensitivity for accurate detection and correction of unexpected feedback changes (errors) during vocal production

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