Marmoset Anterior Cingulate Area 32 Neurons Exhibit Responses to Presented and Produced Calls During Naturalistic Vocal Communication

Abstract

Vocal communication is a complex social behavior that entails the integration of auditory perception and vocal production. Both anatomical and functional evidence have implicated the anterior cingulate cortex (ACC), including area 32, in these processes, but the dynamics of neural responses in area 32 during naturalistic vocal interactions remain poorly understood. Here, we addressed this by recording the activity of single area 32 neurons using chronically implanted ultra high density Neuropixels probes in freely moving common marmosets (Callithrix jacchus) engaged in an antiphonal calling paradigm in which they exchanged long-distance "phee" calls with a virtual conspecific. We found that many neurons exhibited complex modulations in discharge rates in response to presented calls, prior to and following self-generated calls, and during the interval between presented and produced vocalizations. These findings are consistent with the conceptualization of area 32 as an audiovocal interface integrating auditory information, cognitive processes, and motor outputs in the service of vocal communication. Significance StatementVocal communication is indispensable in the daily lives of social animals including primates. This sophisticated ability requires processing and production of vocalizations across fluid social contexts. Vocal behavior is controlled by a large network of brain areas. Area 32 within the anterior cingulate cortex may be a linchpin of this network, as it is interconnected with both auditory cortical areas and subcortical structures engaging vocal control. This position is ideal for integrating auditory, motor, and cognitive signals serving vocal behaviour. We show for the first time that neural correlates of these three signal types are present in area 32 neurons recorded in freely moving marmosets during naturalistic vocal exchanges. We conclude that area 32 exhibits the properties of an audiovocal interface.