An Actor-Critic Circuit in the Songbird Enables Vocal Learning

The ability to learn and to modify complex vocal sequences requires extensive practice coupled with performance evaluation through auditory feedback. An efficient solution to the challenge of vocal learning, stemming from reinforcement learning theory, proposes that an “actor” learns correct vocal behavior through the instructive guidance of an auditory “critic.” However, the neural circuit mechanisms supporting performance evaluation and even how “actor” and “critic” circuits are instantiated in biological brains are fundamental mysteries. Here, I use a songbird model to dissociate “actor” and “critic” circuits and uncover biological mechanisms for vocal learning.

First, I employ closed-loop optogenetic methods in singing birds to identify two inputs to midbrain dopamine neurons that operate in an opponent fashion to guide vocal learning. Next, I employ electrophysiological methods to establish a microcircuit architecture underlying this opponent mechanism. Notably, I show that disrupting activity in these midbrain dopamine inputs precisely when auditory feedback is processed impairs learning, showing that they function as “critics.” Conversely, I show that disrupting activity in a downstream premotor region prior to vocal production prevents learning, consistent with an “actor” role. Taken together, these experiments dissociate discrete “actor” and “critic” circuits in the songbird’s brain and elucidate neural circuit and microcircuit mechanisms by which “actors” and “critics” working cooperatively enable vocal learning.