A novel role for higher order auditory circuits: social group dynamics and descending pathways to the Social Behavior Network - Project Summary/Abstract Healthy social group living relies heavily on the ability to process complex sensory environments. In several prevalent neurological and neuropsychiatric disorders, deficits in social interactions are frequently associated with pathology in auditory circuits. Broad lesions of higher auditory circuits result in alterations in social behavior. Despite a strong connection between auditory cognition and social behavior, we lack basic knowledge about how higher auditory circuits influence social group dynamics. The long-term goal of this proposal is to provide enhanced training that will enable the applicant to establish mechanisms by which higher auditory circuits support integration into social groups at behavioral and neural levels. Aims in this proposal will test the extent to which higher auditory pathways are critical for social group living through investigation of their role in complex group dynamics and their neural circuit outputs to social behavior brain areas. In the K99 phase, Aim 1 will test the extent to which specific damage to the pathway between primary and secondary auditory pallium (caudomedial nidoapllium, NCM) modifies approach and avoidance behavior in pair bonds and small groups of animals during social group formation. Preliminary data demonstrate that descending neural pathways from higher auditory areas modify social auditory processing in a social behavior nucleus, the lateral ventromedial nucleus of the hypothalamus (VMHl). Thus, Aim 2 will test the extent to which electrophysiological signatures of auditory memory (which is critical during social interactions) are represented in higher auditory NCM versus social behavior nucleus VMHl. During the mentored phase and in completion of the above Aims, the applicant will receive, in addition to novel conceptual training, comprehensive training implementing viral-mediated genetic ablation of neural pathways, automated behavioral analysis of complex social group dynamics, social network analysis, and multi-site in vivo electrophysiological recordings. In the R00 independent phase, the applicant will leverage this training to advance a research program that expands from study of single brain regions to synaptically-connected networks, and from individual behavior to large social group dynamics. Aims 3 & 4 will move forward to test the roles of descending pathways in the speed of integration into large social groups, and test the hypothesis that VMHl uses higher auditory circuit input to evaluate competing motivations (i.e., make decisions to engage in social versus non-social behaviors). The innovative approach of this proposal comes from the intersection of technical and conceptual advances in systems neuroscience, behavioral neuroendocrinology, and behavioral ecology using a highly gregarious study species, zebra finches, that constantly dissect complex auditory environments in large social groups. Expanding basic knowledge of mechanisms by which higher auditory pathways impact social group living can provide a critical foundation for future design of treatments for social symptoms of neurological and neuropsychiatric disorders.
