Top–Down Inhibitory Mechanisms Underlying Auditory–Motor Integration for Voice Control: Evidence by TMS

Abstract

The dorsolateral prefrontal cortex (DLPFC) has been implicated in auditory–motor integration for accurate control of vocal production, but its precise role in this feedback-based process remains largely unknown. To this end, the present event-related potential study applied a transcranial magnetic stimulation (TMS) protocol, continuous theta-burst stimulation (c-TBS), to disrupt cortical activity in the left DLPFC as young adults vocalized vowel sounds while hearing their voice unexpectedly shifted upwards in pitch. The results showed that, as compared to the sham condition, c-TBS over left DLPFC led to significantly larger vocal compensations for pitch perturbations that were accompanied by significantly smaller cortical P2 responses. Source localization analyses revealed that this brain activity pattern was the result of reduced activation in the left superior frontal gyrus and right inferior parietal lobule (supramarginal gyrus). These findings demonstrate c-TBS-induced modulatory effects of DLPFC on the neurobehavioral processing of vocal pitch regulation, suggesting that disrupting prefrontal function may impair top–down inhibitory control mechanisms that prevent speech production from being excessively influenced by auditory feedback, resulting in enhanced vocal compensations for feedback perturbations. This is the first study that provides direct evidence for a causal role of the left DLPFC in auditory feedback control of vocal production.

Assessing the Effects of Continuous Theta Burst Stimulation Over the Dorsolateral Prefrontal Cortex on Human Cognition: A Systematic Review

“…On the language domain, one study reports that neither cTBS nor iTBS over the left DLPFC influenced language switching (LS) control (Pestalozzi et al, 2020 ). However, in one study, cTBS over the left DLPFC led to increased vocal compensation for pitch perturbations, which was electro-physiologically accompanied by a reduction in P2 cortical responses (Liu et al, 2020 ). These results on the effects of TBS over DLPFC on language regulation attract diverse arguments, where on the one hand, DLPFC does not regulate language switching, and on the other, it exerts a top-down control over voice production.…”

“…Moreover, it is evident that the left DLPFC modulates speech. The cTBS over the left DLPFC not only led to increased vocal compensation for pitch perturbation, but was also responsible for the reduction in cortical responses (Liu et al, 2020 ). This implies that the left DLPFC exerts a top-down inhibitory control on vocal production in response to auditory feedback, which was diminished after cTBS stimulation.…”

Neurobehavioral Effects of LSVT® LOUD on Auditory-Vocal Integration in Parkinson’s Disease: A Preliminary Study

“…Previous research has shown an association between reduced vocal compensations for pitch perturbations and increased P2 amplitudes in healthy populations following working memory training (Guo et al, 2017) and in individuals with PD following external auditory cueing (Huang et al, 2019). Moreover, one recent TMS study reported that disrupting activity in the left DLPFC by continuous theta-burst stimulation (c-TBS) led to enhanced vocal compensations for pitch perturbations that were accompanied by reduced P2 responses (Liu et al, 2020). Consistently, reduced high-gamma activity in the DLPFC was predictive of abnormally enhanced vocal compensations for pitch perturbations in patients with AD (Ranasinghe et al, 2019).…”

“…In addition, recent source localization work has shown the contribution of the prefrontal cortex to the generation of P2 responses to pitch perturbations (Huang et al, 2016;Guo et al, 2017). It is thus suggested that a top-down inhibitory mechanism mediated by the prefrontal cortex may underlie auditory-motor control of vocal production, preventing vocal motor behaviors from being excessively influenced by auditory feedback (Liu et al, 2020). In light of this idea, individuals with PD may be impaired in this top-down mechanism such that auditory feedback errors cannot be correctly perceived and appropriately corrected, resulting in their abnormally enhanced vocal compensations.…”

“…Particularly, improved vocal SPL was predicted by increased activity in the right middle temporal gyrus (MTG), premotor cortex (PMC), and dorsolateral prefrontal cortex (DLPFC), suggesting that LSVT LOUD can improve self-monitoring of speech production by recalibrating auditory-motor integration in a top-down manner (Narayana et al, 2010). In the context of speech motor control, the MTG and PMC are involved in the detection and correction of voice auditory feedback errors (Chang et al, 2013;Kort et al, 2016;Guo et al, 2017), while the DLPFC can exert top-down inhibitory influences on vocal pitch regulation (Liu et al, 2020). Therefore, LSVT LOUD may augment auditory feedback control of vocal pitch production through the top-down modulations of the speech motor systems.…”