Experience-dependent tuning of socially selective neural circuits

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PROJECT SUMMARY Appropriately recognizing and responding to social partners is a fundamental principle guiding every social interaction from single cells to humans. Social environment is known to interact with development to give rise to typical behavioral responses, however the mechanisms by which social experience shapes the development and tuning features of the nervous system to give rise to these behaviors remains poorly understood. How does the social environment throughout development interact to shape how the brain encodes and discriminates social information? The proposed research addresses these questions in a novel experimentally tractable system for investigating social development of a neural circuit, the northern paper wasp, Polistes fuscatus. P. fuscatus females have highly diverse color markings on their face which they use to discriminate social partners via vision alone. Like humans, P. fuscatus wasps treat faces as special visual objects and the development of this specialized recognition ability is dependent on social experience. The social lives of these wasps are rich and complex, allowing for highly refined social memory and even transitive inference of social relationships. Conveniently, wasps do not possess image forming eyes prior to adult emergence. This key feature allows for the ability to precisely control both the timing and diversity of social experience, while maintaining normal larval development. Further, we have recently discovered a common population of socially responsive neurons in the central brain of P. fuscatus, which show selective tuning to visual stimuli of forward- facing wasps above other visual objects, analogous to the ‘face cells’ in the primate brain. These cells encode both social detection and identity discrimination, providing a clear neural target to study how social experience shapes the tuning features of a socially selective circuits. The proposed experiments take advantage of the unique strengths of this system to address this question at three levels. First, we will assess how these circuits are impacted by long-term social isolation. Second, we will track the developmental tuning trajectory of these circuits to identify how these circuits develop and are refined through maturity to give rise to the highly selective features found in mature adult wasps. Third, we will investigate how both individual neural and population-level tuning features are affected by the diversity of social experiences wasps have, via manipulation of facial diversity among groups. These experiments will aid in discovering fundamental features of how social circuits are tuned via social experience and guide future experiments to identify shared principles guiding social cognition. Further this award will also support the awardee’s transition to an independent research career at a research-intensive university and support the establishment of their laboratory studying how social experience shapes the development of circuits underlying social cognition.