Dissociation of Unit Activity and Gamma Oscillations during Vocalization in Primate Auditory Cortex.

Abstract

Vocal production is a sensory-motor process in which auditory self-monitoring is used to ensure accurate communication. During vocal production, the auditory cortex of both humans and animals is suppressed, a phenomenon that plays an important role in self-monitoring and vocal motor control. However, the underlying neural mechanisms of this vocalization-induced suppression are unknown. γ-band oscillations (>25 Hz) have been implicated a variety of cortical functions and are thought to arise from activity of local inhibitory interneurons, but have not been studied during vocal production. We therefore examined γ-band activity in the auditory cortex of vocalizing marmoset monkeys, of either sex, and found that γ responses increased during vocal production. This increase in γ contrasts with simultaneously recorded suppression of single-unit and multiunit responses. Recorded vocal γ oscillations exhibited two separable components: a vocalization-specific nonsynchronized ("induced") response correlating with vocal suppression, and a synchronized ("evoked") response that was also present during passive sound playback. These results provide evidence for the role of cortical γ oscillations during inhibitory processing. Furthermore, the two distinct components of the γ response suggest possible mechanisms for vocalization-induced suppression, and may correspond to the sensory-motor integration of top-down and bottom-up inputs to the auditory cortex during vocal production.SIGNIFICANCE STATEMENT Vocal communication is important to both humans and animals. In order to ensure accurate information transmission, we must monitor our own vocal output. Surprisingly, spiking activity in the auditory cortex is suppressed during vocal production yet maintains sensitivity to the sound of our own voice ("feedback"). The mechanisms of this vocalization-induced suppression are unknown. Here we show that auditory cortical γ oscillations, which reflect interneuron activity, are actually increased during vocal production, the opposite response of that seen in spiking units. We discuss these results with proposed functions of γ activity during inhibitory sensory processing and coordination of different brain regions, suggesting a role in sensory-motor integration.