Prefrontal cortex mediation of cognitive enhancement in rewarding motivational contexts

Abstract

Increasing the reward value of behavioral goals can facilitate cognitive processes required for goal achievement. This facilitation may be accomplished by the dynamic and flexible engagement of cognitive control mechanisms operating in distributed brain regions. It is still not clear, however, what are the characteristics of individuals, situations, and neural activation dynamics that optimize motivation-linked cognitive enhancement. Here we show that highly reward-sensitive individuals exhibited greater improvement of working memory performance in rewarding contexts, but exclusively on trials that were not rewarded. This effect was mediated by a shift in the temporal dynamics of activation within right lateral prefrontal cortex, from a transient to predominantly tonic mode, with an additional anticipatory transient boost. In contexts with intermittent rewards, a strategy of proactive cognitive control may enable globally optimal performance to facilitate reward attainment. Reward-sensitive individuals appear preferentially motivated to adopt this resource-demanding strategy, resulting in paradoxical benefits selectively for nonrewarded events.

Conflict of interest statement

The authors declare no conflict of interest.

Figures

Fig. 1.

Experimental design, behavioral, and individual difference effects. (A) A mixed blocked/event-related fMRI design enabled dissociation of transient/sustained activity dynamics across motivational contexts. In the reward block (R+; orange), reward trials (R) and nonreward trials (N) were pseudorandomly intermixed, whereas only nonreward trials were presented in the nonreward block (R-; blue). For transient (trial-by-trial) effects, only nonreward trials were analyzed (orange “N” vs. blue “N”) to examine the impact of motivational context on otherwise identically matched trials. The sustained (block-wise) effect (orange rectangle vs. blue rectangle) isolated persistently increased activation during task blocks, independent of trial-related effects. (B) Reaction times were faster in the R+ context than the R- context. ***, P < 0.001. (C) The RT effect was plotted against a personality trait score for reward sensitivity (z score normalized composite index). The vertical axis indicates the RT facilitation in R+ context with the RTs in R- context partialled out, and the horizontal axis indicates the reward sensitivity score. The contextual RT facilitation of incentive was greater in individuals with higher reward sensitivity score.

Fig. 2.

Localization and dynamics of motivational context effects on brain activity. (A) Brain regions showing shifts in activity dynamics between the R+ and R- context were colored in red, projected onto a 3D brain surface representation. The prefrontal and parietal activations each consisted of one large contiguous cluster representing each region, as listed in Table S1. Green, blue, and yellow arrowheads indicate precentral sulcus (PcS), superior frontal sulcus (SFS), and inferior sulcus (IFS), respectively. (B) Time course of sustained activity in the right lPFC region during the R+ and R- blocks. (C) Time course of transient activity in the right lPFC region during the R+ and R- trials. The early transient effect (EARLY) and late transient effect (LATE) were extracted from the time course (Fig. S3A). Note that sustained effects (B) were not present in these time courses. (D) Scatter plot of correlations for sustained and late-transient transient activity during the R+ blocks/trials. Each dot indicates one participant. The negative correlation indicates that higher sustained activity was associated with a reduced late-trial transient response.

Fig. 3.

Statistical correlation maps and plots between behavioral measurements and brain activity components within the right lPFC ROI. Significant regions were colored in yellow on the transverse anatomical section at the labeled coordinate (P < 0.05 corrected for multiple comparison; Left). The area enclosed by red lines indicates the lPFC ROI identified from whole-brain analyses. The activity and the behavioral measurements of individual participants are plotted to demonstrate: (A) the significant negative correlation that was observed between RT contextual facilitation and late transient activity in R+ trial, indicating that faster RTs were associated with reduced activity; (B) individuals with higher reward sensitivity score exhibited greater sustained activity during R+ block; and (C) the higher-score individuals also exhibited greater transient activity during the early period of R+ trial.

Fig. 4.

LPFC activity dynamics mediates the relationship between individual differences and behavioral performance. (A) The path diagram illustrates the direct and indirect relations among the brain activity, reward sensitivity score, and task performance. The indirect effect was mediated by lPFC brain activity dynamics, comprised of the state/early-transient component and the late-transient component. The beta values indicated beside the arrows were simultaneously estimated in a multivariate regression. **, P < 0.01; *, P < 0.05. (B) For each task period (pretrial, and early/late-task periods), activation magnitudes were separately calculated for 10 highest (HIGH) and 10 lowest (LOW) individuals, in terms of reward sensitivity score. The vertical axis indicates the activity level relative to fixation block (i.e., transient and sustained activations are cumulative). In the R- context the two groups are similar (blue solid and dashed lines). However, in the R+ context, the HIGH group dynamically modulates cognitive control processes in the right lPFC (orange solid lines). The enhancement of sustained and early-transient activity results in the decrease in late-transient activity. On the other hand, the LOW group exhibits a qualitatively different profile in activity dynamics, with very little effect of the R+ context (orange dashed lines).