Effects of Cortical Stimulation on Feedback‐Dependent Vocal Control in Non‐Human Primates

Abstract

Objectives Hearing plays an important role in our ability to control voice, and perturbations in auditory feedback result in compensatory changes in vocal production. The auditory cortex (AC) has been proposed as an important mediator of this behavior, but causal evidence is lacking. We tested this in an animal model, hypothesizing that AC is necessary for vocal self‐monitoring and feedback‐dependent control, and that altering activity in AC during vocalization will interfere with vocal control. Methods We implanted two marmoset monkeys (Callithrix jacchus) with bilateral AC electrode arrays. Acoustic signals were recorded from vocalizing marmosets while altering vocal feedback or electrically stimulating AC during random subsets of vocalizations. Feedback was altered by real‐time frequency shifts and presented through headphones and electrical stimulation delivered to individual electrodes. We analyzed recordings to measure changes in vocal acoustics during shifted feedback and stimulation, and to determine their interaction. Results were correlated with the location and frequency tuning of stimulation sites. Results Consistent with previous results, we found electrical stimulation alone evoked changes in vocal production. Results were stronger in the right hemisphere, but decreased with lower currents or repeated stimulation. Simultaneous stimulation and shifted feedback significantly altered vocal control for a subset of sites, decreasing feedback compensation at some and increasing it at others. Inhibited compensation was more likely at sites closer to vocal frequencies. Conclusions Results provide causal evidence that the AC is involved in feedback‐dependent vocal control, and that it is sufficient and may also be necessary to drive changes in vocal production. Level of Evidence N/A Laryngoscope, 133:1–10, 2023

Vocal error monitoring in the primate auditory cortex

“…Results of these studies have potentially important implications for understanding feedback error coding and vocal control. The ability to encode vocal feedback errors is important for feedback-dependent vocal control 33,51 , which may be an evolutionarily ancient precursor to sensorimotor learning of human speech. Corollary discharge predictions have also been linked to our ability to discriminate between self-generated and external sounds 52 , as well as to detect unexpected acoustics form non-vocal self-generated sounds [53][54][55][56] .…”

Frontal-Auditory Cortical Interactions and Sensory Prediction During Vocal Production in Marmoset Monkeys

“…Importantly, there is also a correlation between feedback-sensitive activity in the auditory cortex and behavioral compensation to altered vocal feedback that implies a role in feedback-dependent vocal control. 11,24 Because error calculation requires information not only about vocal sensory feedback but also about intended vocal outputs 3,4 , the auditory cortex has been hypothesized to receive top-down sensory predictions from brain structures that initiate and control vocal production. These predictions, termed efference copies or corollary discharges, are common to many sensory-motor systems.…”