Neuronal circuit mechanisms for learning during social interactions

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 DESCRIPTION (provided by applicant): Even brief social interactions can lead to long lasting memories that profoundly shape future behavior. For example, speech, language, and other culturally transmitted behaviors are learned from social experiences. Resolving how the brain forms and retains long-lasting memories of social experiences is an important goal in neuroscience because it can provide fundamental insights into how we learn from one another and how we communicate. Aside from human speech and language learning, song learning in birds provides one of the clearest examples of this. Following only brief tutoring from an adult bird, a juvenile songbird will establish an accurate, long-lasting memory of the adult model's song, as evidenced by the precise vocal imitation of this song many weeks, and in some species, months and years, later. A major challenge to identifying the neuronal circuits that encode and retain these lasting representations has been our inability to remotely monitor and manipulate neuronal activity on time scales congruent with social interactions and learning. Using optogenetic manipulation of conditionally targeted neurons, voice recognition software and optical imaging of neuronal activity, we have overcome these methodological road blocks. This research will identify the specific neurons that encode and store the memory of the tutor's song needed for vocal imitation using tutoring contingent optogenetic inhibition and two-photon imaging of neuronal activity in juvenile birds. Several lines of evidence have implicated the song premotor nucleus HVC in tutor song memory. However, it is not clear whether a single class of neurons in HVC or downstream of HVC, including those in the auditory forebrain, function to encode this memory. The objective of this proposal is to resolve this issue by identifying the specific class or classes of neurons that encode the tutor song memory, revealing how it is functionally represented in the juvenile brain, and examining how the song memory interacts with circuits important for evaluating singing performance. In the first aim of this proposal we wil use the conditional expression of an inhibitory light sensitive channel to transiently silence different classes of neurons in these brain regions to test their necessity in tutor song learning. In the second aim we will use in vivo imaging of neuronal activity to examine how sensory experience of the tutor's song is functionally and spatially represented in the brain. In the third aim we will use optogenetic inhibition during vocal rehearsal to identify how neurons encoding the tutor song memory interact with auditory feedback circuits. Through these aims we will provide fundamental insights into how the brain encodes and retains memories of vocal models and how these memories shape future behaviors.