Nucleus accumbens dopamine encodes the trace period during appetitive Pavlovian conditioning
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Pavlovian conditioning tasks have been used to identify the neural systems involved with learning cue-outcome relationships. In delay conditioning, the presentation of a conditioned stimulus (CS) overlaps or co-terminates with the delivery of the unconditioned stimulus (US). Prior studies demonstrate that behavioral responding during delay conditioning is regulated by dopamine signaling in the nucleus accumbens (NAc). In particular, the dopamine response to the CS reflects the relative value of the upcoming reward in these tasks. In contrast to delay conditioning, trace conditioning involves a ‘trace’ period that separates the end of the CS and the delivery of the US. While dopamine has been implicated in trace conditioning, no studies to date have examined how NAc dopamine responds to reward-related stimuli in these tasks. To address this, we developed a within-subject trace conditioning task where distinct audio CSs signaled either a short trace period (5s) or a long trace period (55s) prior to the delivery of a food reward. Male rats exhibited higher levels of conditioned responding and a faster latency to respond to the Short Trace CS relative to the Long Trace CS. Voltammetry recordings in the NAc found that dopamine levels to the CS increased on Short Trace trials but decreased on Long Trace trials. Conversely, US-evoked dopamine responses were greater on Long Trace trials relative to Short Trace trials. We found that the CS dopamine response correlated with the latency to respond and not to the level of conditioned responding. Furthermore, the relationship between CS dopamine and latency was best explained by an exponential function. Taken together, our results illustrate how CS-evoked dopamine signals in the NAc relate to behavioral outcomes. Furthermore, we find that trace period is encoded by the bidirectional NAc dopamine response to the CS during Pavlovian conditioning.
Significance statement
Learning how to associate a given cue with an outcome is fundamental process underlying reward seeking behavior. Dopamine in the ventral striatum is important for establishing the link between cues and rewarding outcomes in Pavlovian conditioning tasks. However, it is unclear how striatal dopamine release responds to cues during trace conditioning when there is temporal gap between the cue and the rewarding outcome. To address this, we performed voltammetry recordings of dopamine release in male rats trained on trace conditioning task. We demonstrate that cue-evoked dopamine signals encode the trace period and is related to the latency to respond. While prior reports find that the relative reward value is signaled by increases in dopamine neuron activity to cues, the current study highlights the that dopamine response to reward-predictive cues can signal the relative reward value through bidirectional changes in dopamine transmission.
