Striatal outcome processing in healthy aging

Abstract

Functional MRI of young adults has implicated the striatum in the processing of rewarding and punishing events. To date, only two published experiments (Samanez-Larkin et al., 2007; Schott et al., 2007) have explored similar phenomena in older adults, with both studies emphasizing the anticipation of monetary outcomes. To better understand older participants' striatal responses to delivered outcomes, we engaged 20 older adults and 13 younger adults in a card-guessing task that rewarded correct guesses with monetary gain and punished incorrect guesses with monetary loss. Overall, the older adults retained most of the typical features of the striatal response, so that activity in the caudate head showed reliable differentiation between rewards and punishments during the 6- to 9-sec postoutcome window. Comparison of the older and younger adults also pointed to some potential aging effects on outcome activity, including reductions in the magnitude and extent of striatal activation, and a trend for the older adults to show a decreased early punishment response. In sum, our data suggest that the signaling of outcome valence remains relatively stable into late adulthood, although more research is needed to understand some subtle changes that might occur across the life span.

Figure 1

The modified version of the card-guessing task, with a lengthened intertrial interval to account for the possibility of prolonged hemodynamic responses in older participants. The figure depicts a reward trial. During punishment trials, a red, downward-pointing arrow was displayed.

Figure 2

Overlay of the outcome-sensitive activity found in five young adult studies using the card-guessing task (Delgado et al., 2003, Experiment 2; Delgado et al., 2000; Delgado et al., 2004, high-incentive trials; Tricomi et al., 2004, Experiment 3, choice condition; Tricomi et al., 2006). Each study contributed a statistical map of the valence × time interaction, thresholded at p < .001 with a contiguity requirement ≥3 voxels. Maps were overlaid on the reference brain used for three of the studies (Delgado et al., 2003; Delgado et al., 2000; Delgado et al., 2004); data that were not originally presented in this space (Tricomi et al., 2004; Tricomi et al., 2006) were aligned to the reference with a linear model (Woods, Grafton, Watson, et al., 1998). Colors indicate the number of studies in which a voxel showed a significant effect: Blue = 1, green = 2, yellow = 3, orange = 4, red = 5. Images are shown according to radiological convention (right = left).

Figure 3

Significant valence × time interaction effects in the older adults. Note the use of separate significance criteria within and outside of the striatum (see the Method section). Yellow voxels, p < .001; orange voxels, p < .0001. Clusters also met a contiguity threshold of ≥3 voxels. Images are shown according to radiological convention (right = left). The white boundary outlines the masked region that was included in the voxelwise analyses.

Figure 4

Hemodynamic time courses extracted from the three striatal clusters that showed significant valence × time effects in the older adults. Dashed line indicates onset of the outcome display, and shaded regions highlight a priori timepoints of interest. Asterisks denote significant differences between the reward and punishment means at a specific timepoint; p < .05, corrected. For purposes of presentation, a preoutcome baseline estimate was subtracted from the single-participant time courses prior to plotting the group averages [preoutcome baseline = mean(reward T1, reward T2, punish T1, punish T2)]. Error bars represent standard errors of the means.

Figure 5

Overlay of the older and younger adults' statistical maps for the valence × time interaction. As in Figure 3, separate thresholds were used within (p < .001) and outside (p < .0001) the striatum; clusters also met a contiguity threshold of ≥3 voxels. Blue voxels = active in older adults only, red voxels = active in younger adults only, green voxels = active in both older and younger adults. Images are shown according to radiological convention (right = left). The white boundary outlines the masked region that was included in the voxelwise analyses.

Figure 6

(A) Direct overlay of the older and younger adults' average striatal responses for the reward and punishment trials, respectively. Note that time courses were derived from the left and right striatal voxels that exhibited significant valence × time effects in both age groups (see green voxels, Figure 5). The dashed line indicates onset of the outcome display, and shaded regions highlight a priori timepoints of interest. For purposes of presentation, a preoutcome baseline estimate was subtracted from the plotted time courses (for details, see Figure 4). Error bars represent standard errors of the means. (B) Example of age-related blunting effects in the left caudate. Time-course presentation follows the same conventions as were used in panel A.