Reward Learning over Weeks Versus Minutes Increases the Neural Representation of Value in the Human Brain

Over the past few decades, neuroscience research has illuminated the neural mechanisms supporting learning from reward feedback. Learning paradigms are increasingly being extended to study mood and psychiatric disorders as well as addiction. However, one potentially critical characteristic that this research ignores is the effect of time on learning: human feedback learning paradigms are usually conducted in a single rapidly paced session, whereas learning experiences in ecologically relevant circumstances and in animal research are almost always separated by longer periods of time. In our experiments, we examined reward learning in short condensed sessions distributed across weeks versus learning completed in a single "massed" session in male and female participants. As expected, we found that after equal amounts of training, accuracy was matched between the spaced and massed conditions. However, in a 3-week follow-up, we found that participants exhibited significantly greater memory for the value of spaced-trained stimuli. Supporting a role for short-term memory in massed learning, we found a significant positive correlation between initial learning and working memory capacity. Neurally, we found that patterns of activity in the medial temporal lobe and prefrontal cortex showed stronger discrimination of spaced- versus massed-trained reward values. Further, patterns in the striatum discriminated between spaced- and massed-trained stimuli overall. Our results indicate that single-session learning tasks engage partially distinct learning mechanisms from distributed training. Our studies begin to address a large gap in our knowledge of human learning from reinforcement, with potential implications for our understanding of mood disorders and addiction.

SIGNIFICANCE STATEMENT Humans and animals learn to associate predictive value with stimuli and actions, and these values then guide future behavior. Such reinforcement-based learning often happens over long time periods, in contrast to most studies of reward-based learning in humans. In experiments that tested the effect of spacing on learning, we found that associations learned in a single massed session were correlated with short-term memory and significantly decayed over time, whereas associations learned in short massed sessions over weeks were well maintained. Additionally, patterns of activity in the medial temporal lobe and prefrontal cortex discriminated the values of stimuli learned over weeks but not minutes. These results highlight the importance of studying learning over time, with potential applications to drug addiction and psychiatry.