Many behaviors are learned through trial and error by matching performance to internal goals, yet neural mechanisms of performance evaluation remain poorly understood. We recorded basal ganglia–projecting dopamine neurons in singing zebra finches as we controlled perceived song quality with distorted auditory feedback. Dopamine activity was suppressed after distorted syllables, consistent with worse-than-predicted performance, and activated when a predicted distortion did not occur, consistent with better-than-predicted performance. Thus, dopaminergic error signals can evaluate behaviors that are learned, not for reward, but by matching performance to internal goals. We then developed new computational methods to show that spontaneous dopamine activity correlated with natural song variations, demonstrating that dopamine can evaluate natural behavior unperturbed by experimental events such as cues, distortions, or rewards. Attending to mistakes during practicing alone provides opportunities for learning, but self-evaluation during audience-directed performance could distract from ongoing execution. It remains unknown how animals switch between, and process errors during, practice and performance modes. When male zebra finches transitioned from singing alone to singing female-directed courtship song, singing-related error signals were reduced or gated off and dopamine neurons were instead activated by female calls. Dopamine neurons can thus dynamically alter their tuning with changes in social context.

Learning Objectives:

1. Discuss three advantages of the songbird as a model system in neuroscience.

2. Describe the nature of the signal provided by dopamine for song learning.

3. Compare the dopamine signal during solo practice to female-directed performance in zebra finches.