Dopamine and the interdependency of time perception and reward

Abstract

Time is a fundamental dimension of our perception of the world and is therefore of critical importance to the organization of human behavior. A corpus of work - including recent optogenetic evidence - implicates striatal dopamine as a crucial factor influencing the perception of time. Another stream of literature implicates dopamine in reward and motivation processes. However, these two domains of research have remained largely separated, despite neurobiological overlap and the apothegmatic notion that "time flies when you're having fun". This article constitutes a review of the literature linking time perception and reward, including neurobiological and behavioral studies. Together, these provide compelling support for the idea that time perception and reward processing interact via a common dopaminergic mechanism.

Keywords: Dopamine; Motivation; Reward; Time perception; Timing.

Fig. 1.

The psychological modules in scalar expectancy theory. Multiplicative factors such as the pacemaker rate (Λ) and memory constant (K *) can affect the pacemaker pulse count and result in scalar timing. Adapted from Church (1984).

Fig. 2.

The direct (green) and indirect (red) pathways of the basal ganglia, with dopamine projections in blue. NAc, nucleus accumbens; GPe, globus pallidus external segment; GPi, globus pallidus internal segment; VP, ventral pallidum; STN, subthalamic nucleus; SNc, substantia nigra pars compacta; SNr, substantia nigra pars reticulata; VTA, ventral tegmental area. Off-plane nuclei depicted in their approximate ML DV position. The Allen Human Brain Atlas was used as an anatomical reference in creating this figure (Allen Institute for Brain Science, 2010; Ding et al., 2016).

Fig. 3.

Schematic references for common timing tasks. Across panels red is used to indicate short durations while blue is used to indicate long durations. Interval discrimination tasks: (A) The temporal bisection paradigm trains subjects to give different responses to short and long reference intervals, then presents intervals of intermediate durations to find the point of subjective equality between the short and long intervals. This generates a response curve that can shift left or right to reflect changes in the subject’s report of time. (B) The oddball paradigm presents a series of cues, all of the same duration. One of the later cues is randomly replaced with an oddball cue of a different duration, that the subject must classify as longer or shorter than the rest. (C) Sequence paradigms present two cues in a row, asking subjects to either determine if the second was longer or shorter than the first. Sometimes the duration of the first is held constant while the second varies, while in other tasks the order of the long and short cues is randomly assigned. Interval production tasks: (D) The peak interval procedure provides a reward for the first response a fixed duration after a cue. On a small number of probe trials, no reward is available and the peak rate of responding is taken as the subject’s estimate of the duration. (E) The serial fixed interval task is similar, except that the previous reward is used as the cue to begin the interval. In some versions of this task, the most recent response resets the interval, requiring animals to withhold responding for the entire duration.

Fig. 4.

Hypothetical Roles for Dopamine. (A) The dopamine clock hypothesis. Under the dopamine clock hypothesis, high levels of dopamine cause the internal clock to speed up, which in turn causes the behavioral output to exhibit underestimation or overproduction depending on the task. (B) Dopamine signals reflect reward prediction errors, which are used to rescale the speed of the clock depending on whether the reward arrived earlier or later than expected. This would change the speed of the clock on subsequent trials with the goal of increasing temporal accuracy when predicting reward. (C) Dopamine signals reflect temporal prediction errors when external cues of time disagree with the internal clock. In this case, dopamine signals could adjust the position of the internal clock to agree with the external cues. (D) External timing cues compared with the output of the internal clock produce dopaminergic prediction errors that are then used to inform the behavioral output. (E) Dopamine signals inform the behavioral output by ramping to a threshold for action initiation. The level of dopamine activity encodes the temporal proximity to reward, which is informed by the internal clock.