Defining the Neural Circuits for Vocal Memory and Imitation

Ut Southwestern Medical Center, Dallas TX

Investigators

Abstract

PROJECT SUMMARY A significant portion of our behavioral repertoire is initially learned by imitating the behaviors of our parents and other people we interact with while we are young. This is particularly evident when we consider the development of social skills and communicative behaviors like speech and language. Understanding how the brain encodes and retains the memories of social/vocal models that are used to guide accurate imitation is a major scientific challenge. The goal of this research is to identify the cell types and synaptic pathways that encode memories used for learning vocalizations and to map synaptic plasticity mechanisms underlying how these memories are formed in the brain. Studying these memories in the laboratory is complicated by the social nature of their acquisition and the difficulties in isolating discrete and quantifiable imitated behaviors in conventional model species. For example, rodents and non-human primates do not appear to imitate skilled communicative behaviors like vocalizations, but rather communicate using largely innate vocal repertoires. Zebra finches, like people, require social experience from vocal models to form memories used to subsequently guide learning of their courtship song. Unlike some other songbirds, zebra finches do not learn well from passive playback of songs or triggered playback of tutor songs. The study of zebra finch song learning has therefore provided the principal laboratory model for understanding how neural circuits encode memories from social-vocal models that are used to guide precise motor imitation. Research over the last several years demonstrates that the premotor song region HVC is essential for encoding song memories. Yet, neither the neuronal subtypes within HVC nor the presynaptic input pathways necessary for memory encoding have been identified. Using methods for cell- type specific memory manipulation, synaptic connectivity and plasticity mapping, and closed-loop optical inhibition we will define the synaptic pathways encoding song memories and how these memories are synaptically used to guide vocal imitation. In the first aim, we will use optogenetic tools for memory erasure to identify cell subtypes encoding tutor song memories. In the second aim, we will describe the synaptic connectivity and plasticity mechanisms underlying memory formation in these same circuits. In the third aim we will use closed loop silencing of these synaptic pathways to examine the necessity of individual nodes of the circuit in forming vocal memories and vocal imitation. Building on a suite of cutting-edge methods we have developed for use in zebra finches and extensive new data mapping the long-range synaptic connectivity in the songbird brain, this research will identify core circuit mechanisms for forming memories necessary for vocal imitation.