Adapting the flow of time with dopamine

Abstract

The modulation of interval timing by dopamine (DA) has been well established over decades of research. The nature of this modulation, however, has remained controversial: Although the pharmacological evidence has largely suggested that time intervals are overestimated with higher DA levels, more recent optogenetic work has shown the opposite effect. In addition, a large body of work has asserted DA’s role as a “reward prediction error” (RPE), or a teaching signal that allows the basal ganglia to learn to predict future rewards in reinforcement learning tasks. Whether these two seemingly disparate accounts of DA may be related has remained an open question. By taking a reinforcement learning-based approach to interval timing, we show here that the RPE interpretation of DA naturally extends to its role as a modulator of timekeeping and furthermore that this view reconciles the seemingly conflicting observations. We derive a biologically plausible, DA-dependent plasticity rule that can modulate the rate of timekeeping in either direction and whose effect depends on the timing of the DA signal itself. This bidirectional update rule can account for the results from pharmacology and optogenetics as well as the behavioral effects of reward rate on interval timing and the temporal selectivity of striatal neurons. Hence, by adopting a single RPE interpretation of DA, our results take a step toward unifying computational theories of reinforcement learning and interval timing. NEW & NOTEWORTHY How does dopamine (DA) influence interval timing? A large body of pharmacological evidence has suggested that DA accelerates timekeeping mechanisms. However, recent optogenetic work has shown exactly the opposite effect. In this article, we relate DA’s role in timekeeping to its most established role, as a critical component of reinforcement learning. This allows us to derive a neurobiologically plausible framework that reconciles a large body of DA’s temporal effects, including pharmacological, behavioral, electrophysiological, and optogenetic.