Low-serotonin levels increase delayed reward discounting in humans

Abstract

Previous animal experiments have shown that serotonin is involved in the control of impulsive choice, as characterized by high preference for small immediate rewards over larger delayed rewards. Previous human studies under serotonin manipulation, however, have been either inconclusive on the effect on impulsivity or have shown an effect in the speed of action-reward learning or the optimality of action choice. Here, we manipulated central serotonergic levels of healthy volunteers by dietary tryptophan depletion and loading. Subjects performed a "dynamic" delayed reward choice task that required a continuous update of the reward value estimates to maximize total gain. By using a computational model of delayed reward choice learning, we estimated the parameters governing the subjects' reward choices in low-, normal, and high-serotonin conditions. We found an increase of proportion in small reward choices, together with an increase in the rate of discounting of delayed rewards in the low-serotonin condition compared with the control and high-serotonin conditions. There were no significant differences between conditions in the speed of learning of the estimated delayed reward values or in the variability of reward choice. Therefore, in line with previous animal experiments, our results show that low-serotonin levels steepen delayed reward discounting in humans. The combined results of our previous and current studies suggest that serotonin may adjust the rate of delayed reward discounting via the modulation of specific loops in parallel corticobasal ganglia circuits.

Figure 1.

A trial of the delayed reward choice task. At the onset of the trial, the subject must select either a white or yellow mosaic after the fixation cross turns red (“Go” signal). Each button press (green disk) adds a number of colored patches to the selected mosaic. In the example shown here, if the white mosaic is selected, the subject receives 5 yen in two steps of 1.5 s each. If the yellow mosaic is selected, the subject receives 20 yen in four steps. The position of the squares (left or right) changed randomly at each step. At each trial, the initial numbers of black patches for both mosaics were randomly drawn from uniform distributions and indicated different delays. The intertrial interval, which corresponds to the reward display, was fixed and equal to one time step [adapted from the study by Schweighofer et al. (2006)].

Figure 2.

Effect of tryptophan conditions on the percentage of small reward choices (a), the discount parameter γ (b), the learning rate α (c), and the variability of action choice β (d). Note that the smaller discount parameters lead to steeper discounting. Asterisks indicate significant differences: *p < 0.05, **p < 0.01.