Functional Specialization of the Primate Frontal Lobe during Cognitive Control of Vocalizations

Abstract

Cognitive vocal control is indispensable for human language. Frontal lobe areas are involved in initiating purposeful vocalizations, but their functions remain elusive. We explored the respective roles of frontal lobe areas in initiating volitional vocalizations. Macaques were trained to vocalize in response to visual cues. Recordings from the ventrolateral prefrontal cortex (vlPFC), the anterior cingulate cortex (ACC), and the pre-supplementary motor area (preSMA) revealed single-neuron and population activity differences. Pre-vocal activity appeared first after the go cue in vlPFC, showing onset activity that was tightly linked to vocal reaction times. However, pre-vocal ACC onset activity was not indicative of call timing; instead, ramping activity reaching threshold values betrayed call onset. Neurons in preSMA showed weakest correlation with volitional call initiation and timing. These results suggest that vlPFC encodes the decision to produce volitional calls, whereas downstream ACC represents a motivational preparatory signal, followed by a general motor priming signal in preSMA.