Adult age differences in frontostriatal representation of prediction error but not reward outcome.

Gregory R Samanez-Larkin,Darrell A Worthy,Samuel M Mcclure,Rui Mata,Brian Knutson

doi:10.3758/s13415-014-0297-4

Abstract

Emerging evidence from decision neuroscience suggests that although younger and older adults show similar frontostriatal representations of reward magnitude, older adults often show deficits in feedback-driven reinforcement learning. In the present study, healthy adults completed reward-based tasks that did or did not depend on probabilistic learning, while undergoing functional neuroimaging. We observed reductions in the frontostriatal representation of prediction errors during probabilistic learning in older adults. In contrast, we found evidence for stability across adulthood in the representation of reward outcome in a task that did not require learning. Together, the results identify changes across adulthood in the dynamic coding of relational representations of feedback, in spite of preserved reward sensitivity in old age. Overall, the results suggest that the neural representation of prediction error, but not reward outcome, is reduced in old age. These findings reveal a potential dissociation between cognition and motivation with age and identify a potential mechanism for explaining changes in learning-dependent decision making in old adulthood.Electronic supplementary materialThe online version of this article (doi:10.3758/s13415-014-0297-4) contains supplementary material, which is available to authorized users.

Highlights

Emerging evidence from decision neuroscience suggests that younger and older adults show similar frontostriatal representations of reward magnitude, older adults often show deficits in feedback-driven reinforcement learning
A diffusion tensor-imaging study revealed that the structural connectivity of the prefrontal cortex to the striatum could account for age differences in probabilistic reward learning (Samanez-Larkin, Levens, Perry, Dougherty, & Knutson, 2012)
Given prior evidence for age differences in the processing of monetary losses, even in the absence of learning (Samanez-Larkin et al, 2007; Wu et al, 2014), our analyses focused on the gain-learning conditions

Summary

Introduction

Emerging evidence from decision neuroscience suggests that younger and older adults show similar frontostriatal representations of reward magnitude, older adults often show deficits in feedback-driven reinforcement learning. A recent review of behavioral research showed the largest and most reliable adult age differences in decision tasks that depend on learning novel stimulus–reward associations, but few age differences in tasks that did not require recent learning (Mata, Josef, Samanez-Larkin, & Hertwig, 2011) Building on these findings, a diffusion tensor-imaging study revealed that the structural connectivity of the prefrontal cortex to the striatum could account for age differences in probabilistic reward learning (Samanez-Larkin, Levens, Perry, Dougherty, & Knutson, 2012). A diffusion tensor-imaging study revealed that the structural connectivity of the prefrontal cortex to the striatum could account for age differences in probabilistic reward learning (Samanez-Larkin, Levens, Perry, Dougherty, & Knutson, 2012) Together, this prior evidence has suggested that older adults show intact sensitivity to reward magnitude (Samanez-Larkin et al, 2007), decision-making deficits in older age may result from decreased frontostriatal connectivity. This reduction in connectivity may compromise the dynamic updating of reward predictions (Eppinger et al, 2011)

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