Melatonin Secretion during a Short Nap Fosters Subsequent Feedback Learning

Abstract

Sleep helps to protect and renew hippocampus-dependent declarative learning. Less is known about forms of learning that mainly engage the dopaminergic reward system. Animal studies showed that exogenous melatonin modulates the responses of the dopaminergic reward system and acts as a neuroprotectant promoting memory. In humans, melatonin is mainly secreted in darkness during evening hours supporting sleep. In this study, we investigate the effects of a short period of daytime sleep (nap) and endogenous melatonin on reward learning. Twenty-seven healthy, adult students took part in an experiment, either taking a 90-min afternoon nap or watching videos (within-subject design). Before and after the sleep vs. wake interval, saliva melatonin levels and reward learning were measured, and in the nap condition, a polysomnogram was obtained. Reward learning was assessed using a two-alternative probabilistic reinforcement-learning task. Sleep itself and subjective arousal or valence had no significant effects on reward learning. However, this study showed for the first time that an afternoon nap can elicit a small but significant melatonin response in about 41% of the participants and that the magnitude of the melatonin response predicts subsequent reward learning. Only in melatonin responders did a short nap improve reward learning. The difference between melatonin-responders and non-responders occurred very early during learning indicating that melatonin might have improved working memory rather than reward learning. Future studies should use paradigms differentiating working memory and reward learning to clarify which aspect of human feedback learning might profit from melatonin.

Keywords: dopaminergic system; feedback learning; melatonin; probabilistic learning; reward; sleep; striatum-dependent; working memory.

FIGURE 1

Probabilistic reward-learning task (“pirate game”). The figure depicts one of 33 learning trials in each block. In each trial, two pictures of islands are presented and the participant has to decide which island to explore. If the “correct” island is chosen, the picture of the island is replaced by a picture of a treasure, a sound of children cheering “yeah” is played, and the treasure counter turns green and increases by one (reward). If the “wrong” island is chosen, the island is replaced by a jolly roger, a disappointed voice uttering “ohhh” is played, and the treasure counter turns red and decreases by one (punishment). The participants were instructed to learn by trial and error to approach the island on which a treasure is hidden more often and to avoid the island which is inhabited by pirates more often. The pictures above are merely symbolic. The actual pictures were color photos sampled from the Internet.

FIGURE 2

Melatonin response during nap correlates with subsequent learning. (A) Mean and SEM of saliva melatonin levels before and after an interval either with sleep in darkness (nap condition) or wake in bright light (video condition). The 90 min sleep/wake interval is indicated by the gray bar. (B) Correlation of the melatonin response with the learning performance after the sleep interval in darkness (nap condition) with a regression line. Note that the guessing frequency is 0.5 correct choices.

FIGURE 3

Influence of sleep/darkness on feedback learning. (A) Learning performance (mean ± SEM) improved during the interval irrespective of condition. Note that the guessing frequency is 0.5 correct choices. (B) Only in the melatonin responders (n = 11) did learning performance increase more during sleep in darkness than during wake in bright light.

FIGURE 4

Melatonin but not sleep fosters subsequent feedback learning. (A) The learning performance was almost identical after waking vs. sleep. (B) Participants who showed an increase in saliva melatonin during the nap (responders) subsequently displayed faster feedback learning as compared to non-responders. Differences occur very early in the task (trials 1–5) indicating that working memory might have supported feedback learning. The p-values correspond to two-tailed t-tests.