Vocal learning by songbirds provides a model for studying general mechanisms of sensorimotor learning with particular relevance to human speech learning. For both songbirds and humans, hearing the sounds of others, and auditory feedback of oneself, plays a central role in vocal learning. Our previous work suggests that a basal ganglia-forebrain pathway participates in processing auditory feedback and in driving experience-dependent changes to vocalizations. Moreover, these experiments suggest that variability introduced from basal ganglia circuitry to song motor structures and behavior may play a crucial role in enabling song plasticity. Here, we propose to further test this idea by combining behavioral and neural approaches to study contributions of variability to song production and plasticity. We will use chronic recordings from basal ganglia circuitry and song motor structures in singing birds to characterize normal levels of behavioral and neural variation as well as to examine neuron-neuron and neuron-behavior co-variation (Aim 1). We will then use feedback manipulations in adult birds to drive adaptive changes in song and study the relationship between behavioral variability and the capacity for plasticity (Aim 2). Finally, we will monitor and manipulate activity (via chronic recordings and lesions) during conditions of adaptive plasticity to investigate mechanisms underlying the generation of neural variability and their requirement for behavioral change (Aim 3). Songbirds provide a system where the influence of performance-based feedback on a well-defined and quantifiable behavior potentially can be understood at a mechanistic level. Such an understanding will provide basic insight into normal learning processes and contribute to our ability to prevent and correct disabilities that arise from dysfunction of these processes.
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