Neural Correlates of Vocal Production and Motor Control in Human Heschl's Gyrus

Abstract

The present study investigated how pitch frequency, a perceptually relevant aspect of periodicity in natural human vocalizations, is encoded in Heschl's gyrus (HG), and how this information may be used to influence vocal pitch motor control. We recorded local field potentials from multicontact depth electrodes implanted in HG of 14 neurosurgical epilepsy patients as they vocalized vowel sounds and received brief (200 ms) pitch perturbations at 100 Cents in their auditory feedback. Event-related band power responses to vocalizations showed sustained frequency following responses that tracked voice fundamental frequency (F0) and were significantly enhanced in posteromedial HG during speaking compared with when subjects listened to the playback of their own voice. In addition to frequency following responses, a transient response component within the high gamma frequency band (75-150 Hz) was identified. When this response followed the onset of vocalization, the magnitude of the response was the same for the speaking and playback conditions. In contrast, when this response followed a pitch shift, its magnitude was significantly enhanced during speaking compared with playback. We also observed that, in anterolateral HG, the power of high gamma responses to pitch shifts correlated with the magnitude of compensatory vocal responses. These findings demonstrate a functional parcellation of HG with neural activity that encodes pitch in natural human voice, distinguishes between self-generated and passively heard vocalizations, detects discrepancies between the intended and heard vocalization, and contains information about the resulting behavioral vocal compensations in response to auditory feedback pitch perturbations.

Contributions of sensory tuning to auditory-vocal interactions in marmoset auditory cortex

“…These studies demonstrated that auditory cortex is activated during both speech production and perception, with reduced responses during speaking, termed speech-induced suppression. Human studies have also demonstrated vocal feedback sensitivity similar to that observed in marmosets (Behroozmand et al 2011, 2016; Chang et al 2013). However, a lack of spatial resolution has prevented a more accurate characterizations of the auditory component of speech production-related activity in human auditory cortex.…”

Altered resting‐state functional connectivity of the putamen and internal globus pallidus is related to speech impairment in Parkinson's disease

“…STG serves as functional integration area with partial overlap between speech perception and production mechanisms (Price, 2012). This functional overlap makes STG uniquely suited to detect and integrate auditory feedback during speech production (Behroozmand et al., 2015, 2016; Hickok & Poeppel, 2007; Parkinson et al., 2012; Paus, Perry, Zatorre, Worsley, & Evans, 1996; Tourville & Guenther, 2011; Tourville, Reilly, & Guenther, 2008). The STG cluster identified in the present study corresponds closely to an anterolateral region of Heschl's gyrus that electrocorticography data has linked to online voice error correction following rapid perturbations in auditory feedback (Behroozmand et al., 2016).…”

“…This functional overlap makes STG uniquely suited to detect and integrate auditory feedback during speech production (Behroozmand et al., 2015, 2016; Hickok & Poeppel, 2007; Parkinson et al., 2012; Paus, Perry, Zatorre, Worsley, & Evans, 1996; Tourville & Guenther, 2011; Tourville, Reilly, & Guenther, 2008). The STG cluster identified in the present study corresponds closely to an anterolateral region of Heschl's gyrus that electrocorticography data has linked to online voice error correction following rapid perturbations in auditory feedback (Behroozmand et al., 2016). Compared to healthy individuals, those with PD respond to rapid perturbations in auditory feedback with an exaggerated compensation in vocal output compared to healthy controls (Chen et al., 2013; Huang et al., 2016; Liu, Wang, Metman, & Larson, 2012).…”

Beta Rebound in Visuomotor Adaptation: Still the Status Quo?

“…The brain can detect a mismatch between sensory predictions based on the forward model and actual sensory reafference, and this enables an efficient change of the motor plan (Schafer and Marcus, 1973;Behroozmand et al, 2016). At the same time, the outdated forward model needs to be updated (Synofzik et al, 2008).…”