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Contributions of the Avian VTA to Behavioral Switching

Abstract

Birdsong is a motivated behavior used for courtship and territorial defense. Juvenile male Bengalese finches learn song from their fathers, and over time produce an increasingly accurate copy of their tutor's song. Since it is thought that the ventral tegmental area (VTA) is important in learning and crucial for the production of motivated behavior, we sought to examine the role of the VTA during singing. To probe the function of the VTA we recorded multi-unit activity in adult male Bengalese finches. We observed that neural activity in VTA consistently increased prior to the initiation and termination of song bouts, suggesting that increased activity in this region might mediate behavioral switching. To further test this idea, we coupled VTA recordings with a behavioral manipulation known to cause abrupt terminations of song. We delivered disruptive auditory stimuli during specific notes of ongoing song, which caused song terminations on a subset of trials (Sakata, 2006). Neural activity in the VTA transiently increased at a short latency (10-20ms) in response to the stimulus both during and outside of song. These data indicate that the VTA in singing birds has rapid access to information about salient perturbations of sensory experience, and extend findings indicating that the VTA responds to salient stimuli (Horvitz, 1997). Moreover, we consistently found that neural responses were significantly greater in magnitude on trials in which feedback elicited song termination versus trials in which the bird continued to sing, and the probability of song termination increased as the level of VTA neural activity increased. Because song termination was associated with neural responses of higher magnitude, we stimulated in VTA during song to test the idea that activity in this region might be causally related to song termination. Song terminations were produced at significantly lower current intensities in VTA than in surrounding regions. One interpretation of these data is that the VTA monitors the environment for salient stimuli and is able to effect a cessation of ongoing motor behavior when environmental conditions favor behavioral switching. This supports the interesting possibility that VTA participates in action selection, and might function in contexts unrelated to reward.

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