Forgetting in Reinforcement Learning Links Sustained Dopamine Signals to Motivation

It has been suggested that dopamine (DA) represents reward-prediction-error (RPE) defined in reinforcement learning and therefore DA responds to unpredicted but not predicted reward. However, recent studies have found DA response sustained towards predictable reward in tasks involving self-paced behavior, and suggested that this response represents a motivational signal. We have previously shown that RPE can sustain if there is decay/forgetting of learned-values, which can be implemented as decay of synaptic strengths storing learned-values. This account, however, did not explain the suggested link between tonic/sustained DA and motivation. In the present work, we explored the motivational effects of the value-decay in self-paced approach behavior, modeled as a series of ‘Go’ or ‘No-Go’ selections towards a goal. Through simulations, we found that the value-decay can enhance motivation, specifically, facilitate fast goal-reaching, albeit counterintuitively. Mathematical analyses revealed that underlying potential mechanisms are twofold: (1) decay-induced sustained RPE creates a gradient of ‘Go’ values towards a goal, and (2) value-contrasts between ‘Go’ and ‘No-Go’ are generated because while chosen values are continually updated, unchosen values simply decay. Our model provides potential explanations for the key experimental findings that suggest DA's roles in motivation: (i) slowdown of behavior by post-training blockade of DA signaling, (ii) observations that DA blockade severely impairs effortful actions to obtain rewards while largely sparing seeking of easily obtainable rewards, and (iii) relationships between the reward amount, the level of motivation reflected in the speed of behavior, and the average level of DA. These results indicate that reinforcement learning with value-decay, or forgetting, provides a parsimonious mechanistic account for the DA's roles in value-learning and motivation. Our results also suggest that when biological systems for value-learning are active even though learning has apparently converged, the systems might be in a state of dynamic equilibrium, where learning and forgetting are balanced.Author Summary: Dopamine (DA) has been suggested to have two reward-related roles: (1) representing reward-prediction-error (RPE), and (2) providing motivational drive. Role(1) is based on the physiological results that DA responds to unpredicted but not predicted reward, whereas role(2) is supported by the pharmacological results that blockade of DA signaling causes motivational impairments such as slowdown of self-paced behavior. So far, these two roles are considered to be played by two different temporal patterns of DA signals: role(1) by phasic signals and role(2) by tonic/sustained signals. However, recent studies have found sustained DA signals with features indicative of both roles (1) and (2), complicating this picture. Meanwhile, whereas synaptic/circuit mechanisms for role(1), i.e., how RPE is calculated in the upstream of DA neurons and how RPE-dependent update of learned-values occurs through DA-dependent synaptic plasticity, have now become clarified, mechanisms for role(2) remain unclear. In this work, we modeled self-paced behavior by a series of ‘Go’ or ‘No-Go’ selections in the framework of reinforcement-learning assuming DA's role(1), and demonstrated that incorporation of decay/forgetting of learned-values, which is presumably implemented as decay of synaptic strengths storing learned-values, provides a potential unified mechanistic account for the DA's two roles, together with its various temporal patterns.