Sensory-Motor Interactions for Vocal Pitch Monitoring in Non-Primary Human Auditory Cortex

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.

Sensory–motor networks involved in speech production and motor control: An fMRI study

“…Such recordings further refine our understanding of the spatial distribution of neural networks involved in auditory feedback processing during speaking (Chang et al, 2013; Greenlee et al, 2013). Results of those studies have shown that spatially segregated sub-regions within higher order auditory cortex on posterolateral STG exhibited neural responses to pitch shifts that are modulated during speaking compared with playback.…”

“…By recording electrocorticograms (ECoG) in those subjects, we have described auditory cortical responses after perturbed and unperturbed feedback states and reported neural response changes and the correlation of those changes with vocal behavior (i.e. compensation) in response to pitch shifts (Greenlee et al, 2013). Because ECoG provides limited anatomic sampling of only portions of an individual brain, we have begun using fMRI to provide greater anatomic sampling to supplement the insights gained from ECoG Recordings.…”

“…EEG, MEG, ECoG) of speech production and motor control in an auditory feedback perturbation paradigm (Behroozmand and Larson, 2011; Behroozmand et al, 2011, 2009; Chang et al, 2013; Flinker et al, 2010; Greenlee et al, 2013, 2011; Heinks-Maldonado et al, 2006, 2005; Houde et al, 2002; Sitek et al, 2013). Results of these studies showed that the motor act of speaking modulates speech sound processing in auditory cortical areas.…”

“…no or small feedback error) (Behroozmand and Larson, 2011). However, when feedback was briefly perturbed in the middle of speech, neural responses within auditory cortex were increased during speaking (Behroozmand et al, 2009; Chang et al, 2013; Greenlee et al, 2013; Liu et al, 2010). It is hypothesized that such response modulation underlies detection of feedback changes and correction of unintended speech errors during speaking.…”

Understanding the mechanisms underlying voluntary responses to pitch-shifted auditory feedback

“…Intentional behaviors including the voice are generally thought to involve prefrontal mechanisms (Koval et al, 2011;Schafer and Moore, 2011). Reports using functional magnetic resonance imaging (fMRI) or electrocorticography (ECoG) methods suggest the superior temporal gyrus and premotor cortex are involved in the pitch-shift reflex (Parkinson et al, 2012;Greenlee et al, 2013). Thus far, there is no evidence that prefrontal cortex is involved in responses to pitch-shift stimuli.…”