Communication is an inherently interactive process involving the exchange of information between individuals. For communication to occur, individuals must both recognize the sound as a social signal (e.g. vocalizations), rather than another sound in the environment, as well as the relevant information encoded within the structure of the signal, such as the caller's identity. Despite the relative ease with which the primate auditory system is able to perform these computations, and evidence of vocal signal processing in primate cortex, relatively is known about the neural mechanisms underlying recognition of these communication signals. The primary aim of this proposal is to investigate the complementary roles of auditory and frontal cortex for vocal signal recognition during natural communication. To investigate this process, we employ a multi-technique approach aimed at elucidating the mechanisms underlying vocal signal recognition throughout the ventral auditory cortical system during marmoset antiphonal conversations.
Aim 1 utilizes neuroimaging (fMRI) to identify vocalization responsive populations in the auditory and frontal cortex in awake subjects. The primary aim here is to test whether particular areas of these substrates in the cortical auditory system and will serve as a foundation for subsequent experiments in the proposal.
Aim 2 builds on these findings to record the neurophysiological characteristics of neurons in auditory and frontal cortex while freely-moving marmosets engage in their naturally occurring antiphonal conversations. We employ a novel interactive playback paradigm in which subjects directly engage in these vocal interactions with a software-generated `Virtual Marmoset' (VM). Because the vocal behavior and signals of the VM can be experimentally manipulated, we will use this paradigm to test the responses of neurons throughout these substrates for call recognition and social recognition.
Aim 3 utilizes optogenetic techniques to explicitly test the functional contributions of auditory cortex for vocal signal recognition. We employ a novel, chronic optogenetic preparation developed in my laboratory for marmosets to selectively photostimulate primary auditory cortex and the rostral belt region during antiphonal conversations. Subjects will engage in the same VM paradigms used in Aim 2 during these experiments to test the respective functional contributions of these substrates on call and social recognition during natural communication.
Auditory recognition disorders in speech and language are typically thought to result from neurological abnormalities in neocortex rather than the auditory periphery. Yet little is known about the neural mechanisms that underlie audition in primate models. This innovative proposal aims to address this issue by examining the neural circuitry underlying vocal recognition during natural communication.
| 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 |
| 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 |
| Izpisua Belmonte, Juan Carlos; Callaway, Edward M; Caddick, Sarah J et al. (2015) Brains, genes, and primates. Neuron 86:617-31 |
| 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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