Affective traits link to reliable neural markers of incentive anticipation

Abstract

While theorists have speculated that different affective traits are linked to reliable brain activity during anticipation of gains and losses, few have directly tested this prediction. We examined these associations in a community sample of healthy human adults (n=52) as they played a Monetary Incentive Delay task while undergoing functional magnetic resonance imaging (FMRI). Factor analysis of personality measures revealed that subjects independently varied in trait Positive Arousal and trait Negative Arousal. In a subsample (n=14) retested over 2.5years later, left nucleus accumbens (NAcc) activity during anticipation of large gains (+$5.00) and right anterior insula activity during anticipation of large losses (-$5.00) showed significant test-retest reliability (intraclass correlations>0.50, p's<0.01). In the full sample (n=52), trait Positive Arousal correlated with individual differences in left NAcc activity during anticipation of large gains, while trait Negative Arousal correlated with individual differences in right anterior insula activity during anticipation of large losses. Associations of affective traits with neural activity were not attributable to the influence of other potential confounds (including sex, age, wealth, and motion). Together, these results demonstrate selective links between distinct affective traits and reliably-elicited activity in neural circuits associated with anticipation of gain versus loss. The findings thus reveal neural markers for affective dimensions of healthy personality, and potentially for related psychiatric symptoms.

Keywords: Accumbens; Affect; FMRI; Insula; Punishment; Reward.

Figure 1. Representative Monetary Incentive Delay task trials

During each trial, subjects first saw a cue indicating potential gain or loss of different amounts (2 sec), next watched a fixation cross as they waited a variable delay (2–2.5 sec), next responded with a button press to a rapidly presented target of variable duration (160–260 msec), and finally saw the outcome of their action, depending on the cue presented and their success at responding before the target's disappearance (1.5–2.0 sec). Trials were separated by a variable intertrial interval (2–6 sec).

Figure 2. MID Task, group activation contrasts, volumes of interest, and peak activation profiles

Group contrast maps for gain versus nongain anticipation in the NAcc (top left panel) and loss versus nonloss anticipation in the anterior insula (bottom left panel). Mean (±SEM) peak percent signal change during anticipation was extracted from NAcc and anterior insula volumes of interest, averaged by condition (over 15 trials per condition), and plotted (right panels). Anticipation of large gains (+$5.00; p <.001), as well as small gains (+$0.50; p <.01) and large losses (−$5.00; p <.01), increased activity relative to anticipation of no outcome in the NAcc. Anticipation of large losses (−$5.00; p <.001) and gains (+$5.00; p <.001) increased activity relative to anticipation of no outcome in the anterior insula.

Figure 3. Representative subjects and temporal stability of left NAcc activity during anticipation of large gains

Individual contrast maps for gain versus nongain anticipation at Test 1 and Test 2 (top two rows; slice anterior coordinate =11, threshold p<.001 uncorrected, cluster =16 contiguous 2 mm³ voxels). Plot depicts peak percent signal change in left NAcc during anticipation of large gains (+$5.00) at Test 1 versus Test 2 (bottom).

Figure 4. Representative subjects and temporal stability of right anterior insula activity during anticipation of large losses

Individual contrast maps for loss versus nonloss anticipation at Test 1 and Test 2 (top two rows; slice anterior coordinate =11, threshold p<.001 uncorrected, cluster = 16 contiguous 2 mm³ voxels). Plot depicts peak percent signal change in right anterior insula during anticipation of large losses (−$5.00) at Test 1 versus Test 2 (bottom).

Figure 5. Associations of affective traits with neural activity during anticipation of large gains and losses

Left NAcc activity during anticipation of large gains (+$5.00) was significantly associated with trait Positive Arousal (r=.30, R² = .09, Fisher's Z=.32, p<.05; upper left) but not trait Negative Arousal (r=.05, p=ns; upper right), whereas right anterior insula activity during anticipation of large losses (−$5.00) was significantly associated with trait Negative Arousal (r=.32, R² = . 10, Fisher's Z=.33, p<.05; lower left) but not trait Positive Arousal (r=.00, p=ns; lower right).

Figure 6. Structural equation model supporting a double dissociation interpretation of links from affective traits to brain activity

This full model fits the data ((χ²(4) = 2.29; p = 0.68; Goodness of Fit Index (GFI) = 1, Root Mean Squared Error of Approximation (RMSEA) = 0), but path coefficients from trait Positive Arousal to L NAcc activity to the +$5.00 cue (Z = 2.36, p < 0.05) and from trait Negative Arousal to R Anterior Insula activity to the −$5.00 cue (Z = 2.46, p < 0.05) are significant, while crossover paths are not.