Reduced striatal responses to reward prediction errors in older compared with younger adults

Abstract

We examined whether older adults differ from younger adults in how they learn from rewarding and aversive outcomes. Human participants were asked to either learn to choose actions that lead to monetary reward or learn to avoid actions that lead to monetary losses. To examine age differences in the neurophysiological mechanisms of learning, we applied a combination of computational modeling and fMRI. Behavioral results showed age-related impairments in learning from reward but not in learning from monetary losses. Consistent with these results, we observed age-related reductions in BOLD activity during learning from reward in the ventromedial PFC. Furthermore, the model-based fMRI analysis revealed a reduced responsivity of the ventral striatum to reward prediction errors during learning in older than younger adults. This age-related reduction in striatal sensitivity to reward prediction errors may result from a decline in phasic dopaminergic learning signals in the elderly.

Figure 1.

Schematic of the task. The design involved five learning blocks with 48 trials each (24 per learning condition, randomly intermixed). Each block involved a new set of four stimuli (two per learning condition). Feedback was deterministic.

Figure 2.

A, Accuracy in proportion correct (y-axis) averaged into six equally large trial bins (x-axis) displayed separately for the positive learning condition (left) and the negative learning condition (right). Younger adults are shown in black, older adults are shown in gray. Error bars reflect the SEM. B, RTs in milliseconds (y-axis) averaged into six equally large trial bins (x-axis) displayed separately for the negative learning condition (left) and the positive learning condition (right). Younger adults are shown in black, older adults are shown in gray. Error bars reflect the SEM.

Figure 3.

A, Significant activations (t statistics) for the positive learning condition across age groups. BOLD activity is time locked to feedback onset. Activations are significant at p < 0.05, corrected for multiple comparisons. B, Significant activations (t statistics) for the negative learning condition across age groups. BOLD activity is time-locked to feedback onset. Activations are significant at p < 0.05, corrected for multiple comparisons. C, Significant main effect of age group in the positive learning condition in the ventromedial PFC (Talairach coordinates: −6, 39, 0, t statistics, significant at p < 0.001, cluster size >20 voxels).

Figure 4.

A, Time courses for activity in the vmPFC and vStr (Fig. 3A) for the positive learning condition (+50 and −00 outcomes, left) and the negative learning condition (−50 and +00 outcomes, middle) separately for younger adults (black) and older adults (gray). Right: Difference in percentage signal change between positive and neutral outcomes (positive learning) and negative and neutral outcomes (negative learning) separately for younger adults (black) and older adults (gray). B, Time courses for activity in the SMA/ACC and dlPFC (Fig. 3B) for the positive learning condition (+50 and *00 outcomes, left) and the negative learning condition (−50 and *00 outcomes, middle) separately for younger adults (black) and older adults (gray). Right: Difference in percentage signal change between positive and neutral outcomes (positive learning) and negative and neutral outcomes (negative learning) separately for younger adults (black) and older adults (gray).

Figure 5.

A, Significant within-subject correlations (t statistics) between BOLD activity and prediction error estimates for the positive learning condition across age groups. Activations are significant at p < 0.05, corrected for multiple comparisons. B, Significant within-subject correlations (t statistics) between BOLD activity and prediction error estimates for the negative learning condition across age groups. Activations are significant at p < 0.05, corrected for multiple comparisons. C, Significant age differences in the correlations between BOLD activity and prediction error estimates for the positive learning condition in the ventromedial PFC (Talairach coordinates: −7, 42, −1) and vStr (Talairach coordinates: 12, 5, −1; t statistics, significant at p < 0.001, cluster size >20 voxels).

Figure 6.

A, Conjunction analysis for learning conditions. Green: Areas activated in the positive learning condition (contrast: +50 > −00). Orange: Areas activated in the negative learning condition (contrast: −50 > +00). Red: areas activated in both learning conditions (conjunction). All activations significant at p < 0.005, cluster size >20 voxels. B, Conjunction analysis for prediction-error related activity. Green: Areas activated in the positive learning condition (contrast: +50 > −00). Orange: Areas activated in the negative learning condition (contrast: −50 > +00). Red: Areas activated in both learning conditions (conjunction). All activations significant at p < 0.005, cluster size >20 voxels.