Abstract
Dopamine is thought to regulate learning from appetitive and aversive events. Here we examined how optogenetically-identified dopamine neurons in the lateral ventral tegmental area of mice respond to aversive events in different conditions. In low reward contexts, most dopamine neurons were exclusively inhibited by aversive events, and expectation reduced dopamine neurons' responses to reward and punishment. When a single odor predicted both reward and punishment, dopamine neurons' responses to that odor reflected the integrated value of both outcomes. Thus, in low reward contexts, dopamine neurons signal value prediction errors (VPEs) integrating information about both reward and aversion in a common currency. In contrast, in high reward contexts, dopamine neurons acquired a short-latency excitation to aversive events that masked their VPE signaling. Our results demonstrate the importance of considering the contexts to examine the representation in dopamine neurons and uncover different modes of dopamine signaling, each of which may be adaptive for different environments.
Highlights
Dopamine is thought to be a key regulator of learning from appetitive as well as aversive events (Schultz et al, 1997; Wenzel et al, 2015)
We used a series of behavioral paradigms with probabilistic outcomes that are designed to test specific hypotheses regarding the integration of different outcomes and the effect of reward contexts
We monitored aversion-related behaviors to examine the trial-by-trial relationship to dopamine responses. By harnessing these controlled experimental conditions, our results indicate that dopamine neurons have different modes of signaling
Summary
Dopamine is thought to be a key regulator of learning from appetitive as well as aversive events (Schultz et al, 1997; Wenzel et al, 2015). Accumulating evidence supports this idea with respect to rewarding and reward-predicting events (Bayer and Glimcher, 2005; Cohen et al, 2012; Eshel et al, 2015; Hart et al, 2014; Roesch et al, 2007; Schultz, 2010; Schultz et al, 1997), how dopamine neurons integrate information about aversive events remains highly controversial. The idea of RPE coding by dopamine neurons has been substantiated by further experiments in a variety of species including monkeys (Bayer and Glimcher, 2005; Hollerman and Schultz, 1998; Waelti et al, 2001), rats (Flagel et al, 2011; Pan et al, 2005; Roesch et al, 2007), Matsumoto et al eLife 2016;5:e17328.
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