Karin Foerde and Daphna Shohamy
J. Neurosci. 2011;31 13157-13167
The ability to learn from the consequences of actions—no matter when those consequences take place—is central to adaptive behavior. Despite major advances in understanding how immediate feedback drives learning, it remains unknown precisely how the brain learns from delayed feedback. Here, we present converging evidence from neuropsychology and neuroimaging for distinct roles for the striatum and the hippocampus in learning, depending on whether feedback is immediate or delayed. We show that individuals with striatal dysfunction due to Parkinson's disease are impaired at learning when feedback is immediate, but not when feedback is delayed by a few seconds. Using functional imaging (fMRI) combined with computational model-derived analyses, we further demonstrate that healthy individuals show activation in the striatum during learning from immediate feedback and activation in the hippocampus during learning from delayed feedback. Additionally, later episodic memory for delayed feedback events was enhanced, suggesting that engaging distinct neural systems during learning had consequences for the representation of what was learned. Together, these findings provide direct evidence from humans that striatal systems are necessary for learning from immediate feedback and that delaying feedback leads to a shift in learning from the striatum to the hippocampus. The results provide a link between learning impairments in Parkinson's disease and evidence from single-unit recordings demonstrating that the timing of reinforcement modulates activity of midbrain dopamine neurons. Collectively, these findings indicate that relatively small changes in the circumstances under which information is learned can shift learning from one brain system to another.