Impact of aging on frontostriatal reward processing

Abstract

Healthy aging is associated with a progressive decline across a range of cognitive functions. An important factor underlying this decline may be the age-related impairment in stimulus-reward processing. Several studies have investigated age-related effects, but compared young versus old subjects. This is the first study to investigate the effect of aging on brain activation during reward processing within a continuous segment of the adult life span. We scanned 49 healthy adults aged 40-70 years, using functional MRI. We adopted a simple reward task, which allowed separate evaluation of neural responses to reward anticipation and receipt. The effect of reward on performance accuracy and speed was not related to age, indicating that all subjects could perform the task correctly. We identified a whole-brain significant age-related decline of ventral striatum activation during reward anticipation as compared to neutral anticipation. Importantly, the specificity of this finding was underscored by the observation that there was no general decline in activation during anticipation. Activation in the ventral striatum increased with age during reward receipt as compared to receiving neutral outcome. Finally, activation in the ventromedial prefrontal cortex during outcome was not affected by age. Our data demonstrate that the typical shift in striatal activation from reward receipt to reward anticipation in young adults disappears with healthy aging. These changes are consistent the well-ocumented age-related decline of striatal dopamine availability, and may provide a stepping stone for further research of age-related neurodegenerative diseases.

Keywords: aging; fMRI; reward; ventral striatum; ventromedial prefrontal cortex.

Figure 1

Schematic representation of the reward task. There were two types of trials: neutral trials (A) and potentially rewarding trials (B) as indicated by the cue (neutral face for a neutral trial and a smiling face for a potentially rewarding trial). Subjects had to press a button as fast as possible when the target stimulus appeared. The fixation time between cue and target was varied. Feedback was given after the response and indicated via color if the response was given within the time limit (green) or not (red). Also the amount of money won in that trial was presented (either +1 or +0). Finally, the cumulative amount of money won was presented. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 2

Behavioral data. Scatter plot of the reward effect (reward anticipation vs. neutral anticipation) on accuracy (indicated by the difference in number of correct trials) and reaction time as a function of age (with linear trend line and 95% confidence interval), and line plots for the three age groups (±standard error of the mean) for neutral trials and potentially rewarding trials.

Figure 3

Whole‐brain effect of age on brain activation during reward anticipation versus neutral anticipation. Activation was tested for significance at a familywise error (FWE) corrected cluster level of P = 0.05 (cluster‐defining threshold of P = 0.001, cluster size of 36 voxels). L = left, R = right. [Color figure can be viewed in the online issue, which is available at http://wileyonlinelibrary.com.]

Figure 4

Reward anticipation. Scatter plot of the reward effect (reward anticipation vs. neutral anticipation) on brain activation in the left and right ventral striatum as a function of age (with linear trend line and 95% confidence interval), and line plots for the three age groups (±standard error of the mean) for neutral anticipation and reward anticipation.

Figure 5

Reward receipt. Scatter plot of the reward effect (reward receipt vs. correct neutral outcome) on brain activation in the left and right ventral striatum as a function of age (with linear trend line and 95% confidence interval), and line plots for the three age groups (±standard error of the mean) for correct neutral outcome and reward receipt.

Figure 6

Activation shift from receipt to anticipation. Scatter plot of the shift in activation from reward receipt to reward anticipation on brain activation in the left and right ventral striatum as a function of age (with linear trend line and 95% confidence interval), and line plots for the three age groups (±standard error of the mean) for reward anticipation and reward receipt.