Auditory-vocal interactions in the primate auditory cortex

Studies of the auditory system have largely focused on sensory coding of sounds in the world around us. In a natural environment, however, both humans and animals commonly engage in both listening and speaking (or vocalizing). During speaking, the auditory system must perform two important tasks, maintaining hearing sensitivity to external sounds (environmental monitoring) and processing acoustic feedback of vocal signals (self-monitoring) for feedback-mediated vocal control. Humans and animals alter vocalization when their perception of its feedback is disturbed. Auditory feedback is also essential during human speech learning as well as during vocal learning for some animal species. Little is known, however, about auditory-vocal interaction mechanisms in the brain and their role in supporting vocal communication. This research investigated these issues by studying cortical processing of self-produced vocalizations and feedback-monitoring during vocalization in marmoset monkeys ( Callithrix jacchus). Methods were developed to record from the cortex of unrestrained animals using implanted multi-electrode arrays. Such methods were necessary because animals will often not vocalize under more controlled experimental conditions. Neurons were recorded in the auditory cortex during self-produced vocalizations. These experiments revealed that the majority of neurons in the auditory cortex exhibited vocalization-induced suppression that began prior to the onset of vocal production. A smaller number of neurons showed vocalization-related excitation. Responses to external auditory stimuli were reduced in vocalization-suppressed neurons, but not vocalization-excited neurons, suggesting that the latter likely play a role in maintaining hearing during vocalization. Further experiments, using the implanted multi-electrode arrays and free roaming methods, showed that the two vocalization responses, suppressed and excited, were observed during all types of vocalizations. The role of auditory feedback during vocalization was investigated during additional experiments in which vocal acoustic feedback was manipulated through attenuation, masking, delay, and frequency shifts. Under these conditions, marmosets exhibited feedback-mediated control of their vocalization acoustics. Furthermore, the activities of auditory cortical neurons were found to be modulated by such altered feedback, suggesting that cortical neurons were sensitive to vocal acoustic feedback and that the auditory cortex may play a role in the feedback-mediated vocal control.