Human and nonhuman primates communicate with conspecifics using vocalizations. For communication in this medium to be successful, listeners must be able to recognize vocal signals (e.g. words for humans) and parse them from the plethora of other biotic and abiotic sounds in the acoustic environment. Rather than be the culmination of vocal signal recognition, identifying species-specific acoustic signals is only one part of a more complex process. Like other objects, vocal signals comprise a number of categories that reflect social dimensions of the caller, such as individual identity, sex, dialect, etc. These social categories are encoded in the acoustic structure of the vocalization due to idiosyncrasies in the caller's voice and are known to be perceptually meaningful in both human and nonhuman primate vocal interactions. While the neural basis of speech recognition has been extensively studied using various neuroimaging techniques and patients, much less is known about its underlying cellular mechanisms. Given similarities in vocal perception and homologies in the auditory system neuroanatomy, nonhuman primates represent an excellent model for explicating the neural mechanisms underlying vocal signal recognition in primate neocortex. Nearly all earlier neural studies of vocalization processing in nonhuman primate cortex involve experiments in which vocalization exemplars are presented to restrained animals. Communication, however, is an inherently interactive process involving the exchange of signals between conspecifics.
The aim of this proposal is to examine vocal signal recognition in naturally behaving common marmosets while they engage in antiphonal calling, a vocal behavior characterized by the reciprocal exchange of vocalizations. Since marmosets will only produce an antiphonal call in response to a particular call type, this behavior represents a natural (i.e. untrained) recognition system and is uniquely suited to explore the neural basis of social categorization during natural communication for the following three reasons. First, previous work shows that social categories of callers affect the dynamics of antiphonal calling. Second, we developed novel, interactive playback software that allows us to elicit this vocal response under experimental conditions. And third, we can record the activity of single neurons in marmoset prefrontal cortex while subjects are freely-moving. These three components represent a potentially powerful approach to addressing the three aims of this proposal.
Specific Aim 1 is to combine single-unit neurophysiology and histology to characterize the functional neuroanatomy of marmoset frontal cortex for vocal communication.
This aim will establish a foundation for all subsequent physiology, both in this proposal and further in the future.
Specific Aim 2 seeks to extensively test the perceptual basis of social categorization by presenting subjects with synthetically manipulated vocalizations.
Specific Aim 3 builds on the preceding aims of this proposal by testing the neural basis of social categorization during antiphonal calling using the neuroanatomical locations of Aim 1 and the perceptual findings of Aim 2.

Public Health Relevance

Speech and language recognition disorders are typically thought to result from neurological abnormalities in neocortex rather than the auditory periphery, but little is known about the neural mechanisms that underlie this process. To bridge this gap, we will investigate the neural basis of vocal signal recognition and categorization in primate prefrontal cortex during natural vocal communication. This innovative proposal seeks to elucidate the neural basis of communication signal recognition in neocortex and contribute to developing subsequent clinical treatments.

National Institute of Health (NIH)
National Institute on Deafness and Other Communication Disorders (NIDCD)
Research Project (R01)
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Auditory System Study Section (AUD)
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Shekim, Lana O
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University of California San Diego
Schools of Arts and Sciences
La Jolla
United States
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Toarmino, Camille R; Yen, Cecil C C; Papoti, Daniel et al. (2017) Functional magnetic resonance imaging of auditory cortical fields in awake marmosets. Neuroimage 162:86-92
Toarmino, Camille R; Wong, Lauren; Miller, Cory T (2017) Audience affects decision-making in a marmoset communication network. Biol Lett 13:
Nummela, Samuel U; Jovanovic, Vladimir; de la Mothe, Lisa et al. (2017) Social Context-Dependent Activity in Marmoset Frontal Cortex Populations during Natural Conversations. J Neurosci 37:7036-7047
Miller, Cory T; Freiwald, Winrich A; Leopold, David A et al. (2016) Marmosets: A Neuroscientific Model of Human Social Behavior. Neuron 90:219-33
MacDougall, Matthew; Nummela, Samuel U; Coop, Shanna et al. (2016) Optogenetic manipulation of neural circuits in awake marmosets. J Neurophysiol 116:1286-94
Izpisua Belmonte, Juan Carlos; Callaway, Edward M; Caddick, Sarah J et al. (2015) Brains, genes, and primates. Neuron 86:617-31
Chow, Cecilia P; Mitchell, Jude F; Miller, Cory T (2015) Vocal turn-taking in a non-human primate is learned during ontogeny. Proc Biol Sci 282:20150069
Mitchell, Jude F; Priebe, Nicholas J; Miller, Cory T (2015) Motion dependence of smooth pursuit eye movements in the marmoset. J Neurophysiol 113:3954-60
Miller, Cory T; Thomas, A Wren; Nummela, Samuel U et al. (2015) Responses of primate frontal cortex neurons during natural vocal communication. J Neurophysiol 114:1158-71
Mitchell, Jude F; Reynolds, John H; Miller, Cory T (2014) Active vision in marmosets: a model system for visual neuroscience. J Neurosci 34:1183-94

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