Neural bases of sensorimotor adaptation in the vocal motor system

Abstract

The present study used event-related potential (ERP) recordings to investigate the neural mechanisms of sensorimotor adaptation in response to altered auditory feedback (AAF) during vocal production. 12 healthy speakers were tested under a vocal motor adaptation paradigm in which the fundamental frequency (F0) of their voice auditory feedback was pitch-shifted downward by one semi-tone (- 100 cents) during vowel vocalizations. Behavioral results revealed that subjects adapted to AAF by producing opposing (upward) responses to pitch-shift stimuli, and this adaptive behavior persisted after feedback alteration was removed (washout). We found that adaptation to AAF was accompanied by a significant increase in the amplitude of a parietal ERP activity elicited after the onset of vocalization. However, no such effect was observed for pre-motor ERPs elicited before vocalization onset. Moreover, we found that adaptive vocal responses were negatively correlated with ERPs over the parietal and positively correlated with those over the fronto-central areas after vocalization onset. These findings suggest that vocal motor adaptation is mediated by sensorimotor reprogramming of feedforward motor commands through incorporating auditory feedback, which is indexed by modulation of behavioral and ERP responses to AAF. We suggest that modulation of neural activities in the parietal cortex highlights its significance as a neural interface for sensorimotor integration and indicates its critical role in vocal motor adaptation. Our findings support the notion that the parietal mechanisms are involved in driving adaptive motor behavior to cope with unexpected changes in the sensory environment to accomplish communication goals during vocal production and motor control.

Singing training predicts increased insula connectivity with speech and respiratory sensorimotor areas at rest

“…Functionally, the IPL and the cerebellum interact with the dAI to dynamically adapt for sensory feedback perturbations during singing, allowing greater pitch-matching accuracy through enhanced sensorimotor feedback and feedforward control mechanisms in singers (Jones and Keough, 2008;Kleber et al, 2017;Kleber et al, 2013;Zarate and Zatorre, 2008). Such functions have been supported by studies investigating the neural correlates of sensorimotor control of speech and song production (Behroozmand and Sangtian, 2018;Correia et al, 2015;Finkel et al, 2019;Guenther and Vladusich, 2012;Hickok, 2017;Houde and Chang, 2015;Parkinson et al, 2012;Shum et al, 2011).…”

Cerebellar contribution to auditory feedback control of speech production: Evidence from patients with spinocerebellar ataxia

“…Auditory feedback provides critical information for the learning and maintenance of feedforward motor commands during speech production (Houde & Jordan, 1998;Jones & Munhall, 2005), and plasticity in the auditory system drives changes in speech motor learning (Jones & Keough, 2008;Ostry & Gribble, 2016). Also, activation of the SMG has been linked to both online and adaptive sensorimotor control of speech production (Behroozmand & Sangtian, 2018;Kort et al, 2014;Kort et al, 2016;Shum, Shiller, Baum, & Gracco, 2011). Also, activation of the SMG has been linked to both online and adaptive sensorimotor control of speech production (Behroozmand & Sangtian, 2018;Kort et al, 2014;Kort et al, 2016;Shum, Shiller, Baum, & Gracco, 2011).…”

“…Finally, artifact-free trials were rereferenced to the average of electrodes on each mastoid, averaged across the condition, and baseline corrected by removing the mean amplitude of the pre- (Mulert et al, 2004) and intracerebral recordings (Zumsteg, Lozano, & Wennberg, 2006). This method has also been successfully applied in recent studies on speech motor control (Behroozmand & Sangtian, 2018;Guo et al, 2017;Huang et al, 2016). sLORETA calculates the standardized current density in 6239 cortical gray matter voxels of a reference brain map normalized to the Montreal Neurological Institute (MNI) space at 5 mm spatial resolution.…”

“…The STG and A1 are fundamental to the detection and correction of feedback errors in vocal output (Chang et al, 2013;Parkinson et al, 2012). Also, activation of the SMG has been linked to both online and adaptive sensorimotor control of speech production (Behroozmand & Sangtian, 2018;Kort et al, 2014;Kort et al, 2016;Shum, Shiller, Baum, & Gracco, 2011). Impaired learning of motor skills has been found to be associated with deactivation in the cerebellar-parietal network (Zwicker, Missiuna, Harris, & Boyd, 2011).…”

Intermittent theta burst stimulation over right somatosensory larynx cortex enhances vocal pitch‐regulation in nonsingers

“…Similarly, state feedback control models suggest that rapid online speech control is achieved via internally represented predictions of sensory consequences of intended vocalizations, whereas the actual feedback during overt production is used to train and update the internal forward model in case of error detection (Hickok et al, ; Houde & Nagarajan, ). Neuroimaging studies indicate that the comparison between predicted and actual auditory feedback involves primary as well as higher‐order auditory regions in posterior superior temporal gyrus (STG) and ventral supramarginal gyrus (SMG) that interact with vPMC (including Broca's area) to generate state corrections, whereas the parietal lobe, cerebellum, and basal ganglia contribute to the programming and maintenance of feedforward control (Behroozmand et al, ; Behroozmand et al, ; Behroozmand & Sangtian, ; Guenther & Vladusich, ; Hickok, ; Houde & Chang, ; Parkinson et al, ; Shum, Shiller, Baum, & Gracco, ; Tourville, Reilly, & Guenther, ; Zarate & Zatorre, ).…”