Contextual Cues Facilitate Dynamic Value Encoding in the Mesolimbic Dopamine System

Adaptive behavior in a dynamic environmental context often requires rapid revaluation of stimuli that deviates from well-learned associations. The divergence between stable value-encoding and appropriate behavioral output remains a critical component of theories of dopamine's function in learning, motivation, and motor control. Yet, how dopamine neurons are involved in the revaluation of cues when the world changes, to alter our behavior, remains unclear. Here, we make use of a complementary set of in vivo approaches to clarify the contributions of the mesolimbic dopamine system to the dynamic reorganization of reward- seeking behavior. Male and female rats were trained to discriminate when a conditioned stimulus would be followed by a sucrose reward by exploiting the prior, non-overlapping presentation of a another discrete cue-an occasion setter. Only when the occasion setter's presentation preceded the conditioned stimulus did the conditioned stimulus predict sucrose delivery, dissociating the average value of the conditioned stimulus from its immediate value, on a trial-to-trial basis. Activity of ventral tegmental area dopamine neurons was essential for rats to successfully update behavioral response to the occasion setter. Moreover, dopamine release in the nucleus accumbens following the conditioned stimulus only occurred when the occasion setter indicated it would predict reward and did not reflect its average expected value. Downstream of dopamine release, we found that neurons in the nucleus accumbens dynamically tracked the value of the conditioned stimulus. Together, these results help refine notions of dopamine function, revealing a prominent contribution of the mesolimbic dopamine system to the rapid revaluation of motivation.