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

Abstract

The control of speech and vocal production involves the calculation of error between the intended vocal output and the resulting auditory feedback. Consistent with this model, recent evidence has demonstrated that the auditory cortex is suppressed immediately before and during vocal production, yet is still sensitive to differences between vocal output and altered auditory feedback. This suppression has been suggested to be the result of top-down signals containing information about the intended vocal output, potentially originating from motor or other frontal cortical areas. However, whether such frontal areas are the source of suppressive and predictive signaling to the auditory cortex during vocalization is unknown. Here, we simultaneously recorded neural activity from both the auditory and frontal cortices of marmoset monkeys while they produced self-initiated vocalizations. We found increases in neural activity in both brain areas preceding the onset of vocal production, notably changes in both multi-unit activity and local field potential theta-band power. Connectivity analysis using Granger causality demonstrated that frontal cortex sends directed signaling to the auditory cortex during this pre-vocal period. Importantly, this pre-vocal activity predicted both vocalization-induced suppression of the auditory cortex as well as the acoustics of subsequent vocalizations. These results suggest that frontal cortical areas communicate with the auditory cortex preceding vocal production, with frontal-auditory signals that may reflect the transmission of sensory prediction information. This interaction between frontal and auditory cortices may contribute to mechanisms that calculate errors between intended and actual vocal outputs during vocal communication.