To engage in productive social interactions, the brain must coordinate processing of complex social sensory cues with production of appropriate social responses. Deficits in appropriate responses to social sensory cues are a feature of several prevalent neurological disorders, including frontotemporal dementia and autism spectrum disorders. While complex social signals (i.e., visual, auditory) are processed in cortex, nuclei controlling social behaviors (conserved across vertebrates), called the social behavior network (SBN), lie mainly in the diencephalon. Tremendous progress has been made in studying cortical sensory circuits and the SBN separately but apart from mammalian olfactory systems we are lacking basic knowledge of how information is coordinated between sensory cortex and SBN circuits. These connections are very likely to be critical for productive social interactions. The long-term goal of this training proposal is to characterize components of a circuit connecting auditory cortical regions with SBN nuclei. This research will be carried out in songbirds (specifically, Zebra finches; Taeniopygia guttata), which are ideal for realizing the proposal's long- term goal. Zebra finches learn and employ complex vocalizations in a rich variety of social contexts. In songbirds, complex social vocalizations induce immediate early gene labeling in both secondary auditory cortical regions and SBN nuclei. Lesions of secondary auditory cortex impair vocal recognition and mate preference, suggesting that cortical inputs to social nuclei play key roles in social decision-making. I have gathered preliminary data showing that secondary auditory cortical regions send projections to a region of the avian cortex, the medial arcopallium, and previous data demonstrate the medial arcopallium sends projections to several SBN nuclei. Based on these findings, this proposal hypothesizes that cortical auditory regions provide SBN nuclei with social-auditory input in part through this arcopallial region of the songbird cortex to influence behavioral decisions.
The specific aims of my proposal will characterize this circuit through 1) testing how inactivation of auditory cortical regions during playback of social vocalizations alters immediate early gene measurements across SBN nuclei, 2) optogenetically identifying and stimulating synaptic connections between auditory cortex and the medial arcopallium, and 3) testing selectivity of medial arcopallial neurons for auditory- social stimuli in freely moving animals. This proposal will be the first to characterize an auditory cortical -> SBN circuit in vertebrates by bridging progress made in auditory systems neuroscience and research in the neural basis of social behavior. Deficits in social sensory cue processing and the ability to engage in social behavior are features of several neurological disorders. The findings generated by this proposal will open up new avenues for research on this vital function by expanding basic knowledge of coordination between cortical sensory circuits and social behavior nuclei.
The ability to engage in appropriate social interactions depends on sensory processing circuitry as well as social behavior circuitry, but intersections of higher-order sensory and social behavior circuits in vertebrates are rarely considered. Currently our knowledge of circuits connecting sensory processing of social signals in the cortex to social behavior nuclei is limited to the olfactory system in mammals. This training proposal will be the first to characterize an auditory cortical -> social behavior nuclei circuit, opening new avenues for study of symptoms of neurological disorders and diseases that impact social functions.