Dopamine Dynamics Drive Birdsong Learning

Abstract

While learning in response to extrinsic reinforcement is theorized to be driven by dopamine signals that encode the difference between expected and experienced rewards, skills that enable verbal or musical expression can be learned without extrinsic reinforcement. Instead, spontaneous execution of these skills is thought to be intrinsically reinforcing. Whether dopamine signals similarly guide learning of these intrinsically reinforced behaviors is unknown. Juvenile zebra finches are distinguished by their ability to copy the song of an adult tutor, a spontaneous, intrinsically reinforced process. Here, I use the zebra finch as a model system to study the neural mechanisms that operate within a song-specialized region of the basal ganglia (sBG) to enable this remarkable form of motor learning. Using in vivo microdialysis and computational methods to quantify juvenile song development, I first determined that dopamine (DA) signaling in the sBG is necessary for song learning. Using genetically encoded DA sensors and fiber photometry, I showed that DA dynamics in the sBG faithfully track the learned quality of juvenile song performance on a rendition-by-rendition basis. Consequently, my experiments provide compelling evidence that DA functions in the sBG as a reward prediction error-like signal to drive song learning, a process that evolves spontaneously and does not depend on extrinsic reward or punishment. Furthermore, I found that DA release in the sBG is driven not only by inputs from midbrain DA neurons classically associated with reinforcement learning but also by song premotor “cortical” inputs, which act via local cholinergic signaling in the sBG to elevate DA during singing. While I was able to show that both cholinergic and dopaminergic signaling in the sBG are necessary for song learning, I further found that only DA tracks the learned quality of song performance. Therefore, dopamine dynamics in the basal ganglia encode performance quality to drive self-directed and long-term learning of natural behaviors.