Limbic circuits for motor performance
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An animal's behavior is ultimately driven by the need to obtain rewards or satisfy goals, such as forging for food, finding a mate, or territorial defense. Midbrain dopamine (DA) neurons respond to singular events providing rewards, performance errors, and social interactions, through reward prediction error signaling. However, it is common for multiple objectives to be encountered at the same time, leading to the question of how the brain establishes one as the priority. What information is needed to weigh one need over another, and how does the dopaminergic system encode the highest priority? Here, songbirds were used to understand how DA neurons signal different types of rewards during two social contexts, and also to implicate a new brain region involved in performance error signaling. First, I measured DA release in two striatal regions as male songbirds were presented with the choice between rewarding objectives, such as singing a good song, courting a female, or obtaining a water reward. I found that the dopaminergic system deals with competing rewards using two methods: 1) providing different information about objectives to distinct areas of the striatum, and 2) prioritizing the response to one need over the rest by decreasing the DA response to all other objectives. Second, I used neural tracing, functional mapping, and lesion studies to show that the lateral habenula receives inputs from areas known to encode song-related error signals, is functionally connected to midbrain dopamine neurons involved in performance error signaling, and when bilaterally lesioned in juvenile males, causes species atypical vocalizations in adulthood.
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Fetcho, Joseph