Excitatory and Inhibitory Signaling in the Nucleus Accumbens Encode Different Aspects of a Pavlovian Cue in Sign Tracking and Goal Tracking Rats

When a Pavlovian cue is presented separately from its associated reward, some animals will acquire a sign tracking (ST) response – approach and/or interaction with the cue – while others will acquire a goal tracking response – approach to the site of reward. We have previously shown that cue-evoked excitations in the nucleus accumbens (NAc) encode the vigor of both behaviors; in contrast, reward-related responses diverge over the course of training, possibly reflecting neurochemical differences between sign tracker and goal tracker individuals. However, a substantial subset of neurons in the NAc exhibit inhibitory, rather than excitatory, cue-evoked responses, and the evolution of their signaling during Pavlovian conditioning remains unknown. Using single-neuron recordings in behaving rats, we show that NAc neurons with cue-evoked inhibitions have distinct coding properties from neurons with cue-evoked excitations. Cue-evoked inhibitions become more numerous over the course of training and, like excitations, may encode the vigor of sign tracking and goal tracking behavior. However, the responses of cue-inhibited neurons do not evolve differently between sign tracker and goal tracker individuals. Moreover, cue-evoked inhibitions, unlike excitations, are insensitive to extinction of the cue-reward relationship. Finally, we show that cue-evoked excitations are greatly diminished by reward devaluation, while inhibitory cue responses are virtually unaffected. Overall, these findings converge with existing evidence that cue-excited neurons in NAc, but not cue-inhibited neurons, are profoundly sensitive to the same behavior variations that are often associated with changes in dopamine release.