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Reward probability and timing uncertainty alter the effect of dorsal raphe serotonin neurons on patience

Abstract


Recent experiments have shown that optogenetic activation of serotonin neurons in the dorsal raphe nucleus (DRN) in mice enhances patience in waiting for future rewards. Here, we show that serotonin effect in promoting waiting is maximized by both high probability and high timing uncertainty of reward. Optogenetic activation of serotonergic neurons prolongs waiting time in no-reward trials in a task with 75% food reward probability, but not with 50 or 25% reward probabilities. Serotonin effect in promoting waiting increases when the timing of reward presentation becomes unpredictable. To coherently explain the experimental data, we propose a Bayesian decision model of waiting that assumes that serotonin neuron activation increases the prior probability or subjective confidence of reward delivery. The present data and modeling point to the possibility of a generalized role of serotonin in resolving trade-offs, not only between immediate and delayed rewards, but also between sensory evidence and subjective confidence.


Introduction


The neuromodulator, serotonin, is extensively involved in behavioral, affective, and cognitive functions of the brain. Chemical and electrode recordings from the dorsal raphe nucleus (DRN) have shown that the activity of serotonin neurons increases when animals perform tasks requiring them to wait for delayed rewards1,2,3. Local pharmacological inhibition of DRN serotonin neural activity in rats impairs their patience in waiting for delayed rewards4. We recently used transgenic mice that express the channelrhodopsin-2 (ChR2) variant C128S in serotonin neurons5,6 and showed that their selective activation in the DRN enhances the patience of mice waiting for both a conditioned reinforcer tone and a food reward7. A recent study also confirmed that optogenetic activation of DRN serotonin neurons enhances patience in waiting8. These results established a causal relationship between serotonin neural activation and patience in waiting for future rewards.


We therefore questioned whether activation of serotonin neurons always promotes waiting for delayed reward or whether its effect depends on the subject’s reward prediction. In our previous optogenetic study, serotonergic activation prolonged waiting time by ~30% before the mice eventually gave up waiting7. Serotonin neuron activation was most effective at the time when mice decided whether to continue waiting7. These results suggest that cognitive status, such as the anticipation of future rewards, modulates the promotion of patience by serotonin.


In the current study, we tested whether the probability, amount, and timing uncertainty of future rewards affects promotion of patience by serotonin neuron activation. We find that serotonin effect in promoting waiting is maximized by both high-reward probability (RP) and high-reward timing uncertainty. We further propose a Bayesian decision model of waiting, which assumes serotonin neuron activation increases the prior RP to reproduce the major features of the experimental results. The model reproduces the more prominent effect of serotonin with reward timing uncertainty because the likelihood function for reward delivery has a longer tail in time. The present data and modeling suggest that serotonin neuron activation enhance patience in waiting for future rewards by increasing subjective confidence of future goals.


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