Mechanisms for internally and externally guided sensorimotor learning

PROJECT SUMMARY Expressive social behaviors, including speech and music, are culturally transmitted from a tutor to a pupil. Such learning depends on a pupil’s ability to integrate social and sensory cues provided by a tutor performing the relevant behavior. Once learned, the underlying motor program must be coordinated with a range of innate motor programs to generate holistic behaviors necessary to effective social signaling. The central hypothesis that this proposal seeks to test is that the same brain circuitry that enables the pupil to integrate social and sensory cues from an adult tutor also function in the adult to enable integration of the learned and innate programs necessary to effective social signaling. In the past cycle, we discovered where neural signals encoding social and sensory cues provided by a tutor are integrated in the pupil’s brain. Specifically, we showed that neurons in a midbrain dopamine cell group (A11) in a juvenile songbird are selectively excited during interactions with a singing adult male tutor, and that pairing song playback with the optogenetically- triggered release of dopamine from A11 terminals in a sensorimotor cortical analogue (HVC) is sufficient to drive song copying. Despite these important insights, exactly when and how tutor experience transforms auditory and motor coding in HVC to facilitate vocal learning remains unknown. Therefore, in Aim 1 we will use multiphoton (2p) longitudinal imaging, fiber photometry to test the hypothesis that tutor experience rapidly strengthens the auditory and motor network in the pupil’s HVC. We will also use novel machine learning tools for vocal analysis and optogenetic methods to test the idea that these sensorimotor changes enable HVC to enhance the acoustic complexity of the pupil’s song, a first step in vocal copying. Our prior studies support the idea that social and auditory cues provided by the tutor drive coincident DA release and auditory synaptic activity in the pupil’s HVC, rapidly potentiating sensorimotor synapses in this region. Therefore, in Aim 2, we will use ex vivo channelrhodopsin circuit-mapping to test the hypothesis that coincident DA release and auditory synaptic actvity rapidly potentiates auditory synapses onto HVC interneurons, and that these effects are strongest during juvenile sensitive periods for learning. Notably, the courtship display of the adult songbird includes a learned song that is seamlessly coordinated with a variety of innate behaviors, including female- directed calling, orientation, and pursuit. In Preliminary Studies, we found that lesions of A11’s axon terminals in HVC of the adult male finch abolish female-directed singing without affecting his innate courtship behaviors. In contrast, selectively ablating A11 cell bodies abolished all of the male’s courtship behaviors. In Aim 3, we will map, monitor and manipulate A11’s projections to HVC and other motor centers to test the idea that A11 acts as a central hub to enable the seamless and rapid coordination of learned and innate motor programs in response to social cues provided by a nearby female.