Feedback-Based Learning in Aging: Contributions and Trajectories of Change in Striatal and Hippocampal Systems

Abstract

The striatum supports learning from immediate feedback by coding prediction errors (PEs), whereas the hippocampus (HC) plays a parallel role in learning from delayed feedback. Both regions show evidence of decline in human aging, but behavioral research suggests greater decline in HC versus striatal functions. The present study included male and female humans and used fMRI to examine younger and older adults' brain activation patterns during a learning task with choice feedback presented immediately or after a brief delay. Participants then completed a surprise memory task that tested their recognition of trial-unique feedback stimuli, followed by assessments of postlearning cue preference, outcome probability awareness, and willingness to pay. The study yielded three main findings. First, behavioral measures indicated similar rates of learning in younger and older adults across conditions, but postlearning measures indicated impairment in older adults' ability to subsequently apply learning to discriminate between cues. Second, PE signals in the striatum were greater for immediate versus delayed feedback in both age groups, but PE signals in the HC were greater for delayed versus immediate feedback only in younger adults. Third, unlike younger adults, older adults failed to exhibit enhanced episodic memory for outcome stimuli in the delayed-feedback condition. Together, these findings indicate that HC circuits supporting learning and memory decline more than striatal circuits in healthy aging, which suggests that declines in HC learning signals may be an important predictor of deficits in learning-dependent economic decisions among older adults.SIGNIFICANCE STATEMENT The hippocampus (HC) and striatum play distinct and critical roles in learning. Substantial research suggests that age-related decline in learning supported by the HC outpaces decline in learning supported by the striatum; however, such inferences have been drawn by comparing performance in tasks with fundamentally different structures. The present study overcomes this obstacle by implementing a single fMRI-learning paradigm with a subtle variation in feedback timing to examine differential age effects on memory supported by the HC and striatum. Our results provide converging behavioral and brain-imaging evidence showing that HC circuits supporting learning and memory decline more than striatal circuits in healthy aging and that declines in HC learning signals may predict early deficits in learning-dependent decisions among older adults.

Keywords: aging; fMRI; hippocampus; learning; memory; striatum.