Occasion setters determine responses of putative DA neurons to discriminative stimuli

Midbrain dopamine (DA) neurons are involved in the processing of rewards and reward-predicting stimuli, possibly analogous to reinforcement learning reward prediction errors. Here we studied the activity of putative DA neurons (n = 37) recorded in the ventral tegmental area of rats (n = 6) performing a behavioural task involving occasion setting. In this task an occasion setter (OS) indicated that the relationship between a discriminative stimulus (DS) and reinforcement is in effect, so that reinforcement of bar pressing occurred only after the OS (tone or houselight) was followed by the DS (houselight or tone). We found that responses of putative DA cells to the DS were enhanced when preceded by the OS, as were behavioural responses to obtain rewards. Surprisingly though, we did not find a homogeneous increase in the mean activity of the population of putative DA neurons to the OS, contrary to predictions of standard temporal-difference models of DA neurons. Instead, putative DA neurons exhibited a heterogeneous response on a single unit level, so that some units increased and others decreased their activity as a response to the OS. Similarly, putative non-DA cells did not show a homogeneous response to the DS on a population level, but also had heterogeneous responses on a single unit level. The heterogeneity in the responses of neurons in the ventral tegmental area may reflect how DA neurons encode context and point to local differences in DA signalling.