Natural Behavior And The Neurobiology Of Primate Communication

Our primate Order is known for the expansion of the neocortex relative to other mammals. This distinction is coupled with a characteristic complex society that is facilitated by dynamic social cognitive mechanisms and systems of communication. Because of this intricate relationship, investigating the neural basis of communication within primates affords the opportunity to better understand how different dimensions of sociality are supported by the structures of the brain itself. Much of the research on the neuroscience of communication in primates has hinged on studies of vocalization processing in head-restrained monkeys either passively listening to stimuli or engaged in a conditional behavioral task. But the information communicated by social signals are heavily influenced by the natural contexts they occur in, and auditory processing of vocalizations within the brain may likewise be heavily affected by the context in which conspecific vocalizations are heard; thus, the experiments may not fully capture the neural basis of communication. I hypothesize that the traditional experimental contexts typical of nonhuman primate neuroscience research has divorced the signal from its natural context, and, consequently, limited our understanding of how various neocortical structures support these processes. Here I sought to address this critical gap in our knowledge by implementing novel experimental paradigms designed to explicate the neurobiology and behavior of natural communication in freely-moving marmoset monkeys (Callithrix jacchus). In this dissertation, I detail the results of new insights gained from the innovative experiments that support my hypothesis. Chapter 1 shows how broad 'states' of neural populations in frontal cortex during natural, untrained behavior of antiphonal conversations in the marmoset predicts whether subjects respond to a conspecific call. Chapter 2 shows robust within-neuron differences in how prefrontal cortex neurons respond to vocalizations between traditional head-restrained contexts and natural behavior suggesting that data recorded in the former context is not predictive of the latter. Finally, Chapter 3 shows my novel multi-speaker paradigm that simulates the natural communication networks in marmosets (i.e. "Cocktail Party") to study the vocal processing of marmosets in complex acoustic environments previously inaccessible to researchers for any other animal model. Results demonstrate that marmosets employ similar perceptual mechanisms as humans to communicate in these dynamic acoustic and social landscapes. These findings establish a novel paradigm in which to explore the neurobiology of primate communication in dynamic, multi-speaker communication networks that more closely resemble their natural communication systems.