Choice-Selective Neurons in the Auditory Cortex and in Its Striatal Target Encode Reward Expectation

Abstract

Learned behavioral responses to sounds depend largely on the expected outcomes associated with each potential choice. Where and how the nervous system integrates expectations about reward with auditory sensory information to drive appropriate decisions is not fully understood. Using a two-alternative choice task in which the expected reward associated with each sound varied over time, we investigated potential sites along the corticostriatal pathway for the integration of sound signals, behavioral choice, and reward information in male mice. We found that auditory cortical neurons encode not only sound identity, but also the animal's choice and the expected size of reward. This influence of reward expectation on sound- and choice-related activity was further enhanced in the major striatal target of the auditory cortex: the posterior tail of the dorsal striatum. These results indicate that choice-specific information is integrated with reward signals throughout the corticostriatal pathway, potentially contributing to adaptation in sound-driven behavior.

SIGNIFICANCE STATEMENT Learning and maintenance of sensory-motor associations require that neural circuits keep track of sensory stimuli, choices, and outcomes. It is not clear at what stages along the auditory sensorimotor pathway these signals are integrated to influence future behavior in response to sounds. Our results show that the activity of auditory cortical neurons and of their striatal targets encodes the animals' choices and expectation of reward, in addition to stimulus identity. These results challenge previous views of the influence of motor signals on auditory circuits and identifies potential loci for integration of task-related information necessary for updating auditory decisions in changing environments.