The neural system that bridges reward and cognition in humans: an fMRI study

Abstract

We test the hypothesis that motivational and cognitive processes are linked by a specific neural system to reach maximal efficiency. We studied six normal subjects performing a working memory paradigm (n-back tasks) associated with different levels of monetary reward during an fMRI session. The study showed specific brain activation in relation with changes in both the cognitive loading and the reward associated with task performance. First, the working memory tasks activated a network including the dorsolateral prefrontal cortex [Brodmann area (BA) 9/46] and, in addition, in the lateral frontopolar areas (BA 10), but only in the more demanding condition (3-back task). This result suggests that lateral prefrontal areas are organized in a caudo-rostral continuum in relation with the increase in executive requirement. Second, reward induces an increased activation in the areas already activated by working memory processing and in a supplementary region, the medial frontal pole (BA 10), regardless of the level of cognitive processing. It is postulated that the latter region plays a specific role in monitoring the reward value of ongoing cognitive processes. Third, we detected areas where the signal decreases (ventral-BA 11/47 and subgenual prefrontal cortices) in relation with both the increase of cognitive demand and the reward. The deactivation may represent an emotional gating aimed at inhibiting adverse emotional signals to maximize the level of performance. Taken together, these results suggest a balance between increasing activity in cortical cognitive areas and decreasing activity in the limbic and paralimbic structures during ongoing higher cognitive processing.

Figure 1

(a) An example of a trial illustrating the schematic representation of the 3 WM (n-back) and the control (0-back) tasks. (b) Schematic representation of one run; in each run, there were two trials of each condition (0-, 1-, 2-, and 3-back). Rewarded conditions were pseudorandomly distributed across trials.

Figure 2

Averaged fMRI signal time-course curves for selected voxels in (a) the right DLPFC (signal increased with task difficulty), (b) the SGPFC (signal decreased with task difficulty; ♦, 0-back; ■, 1-back; ▴, 2-back; ▵, 3-back); (c) the left lateral frontal pole and (d) the left rostral DLPFC (where signal increased with the increase of rewarding value); (e) the ventral striatum; and (f) the MPFC (where the signal decreased with the increase of rewarding valued; ♦, high reward; ●, low reward; ▵, no reward). Gray area corresponds to the n-back period per se. The time-scale unit is expressed as TR (repetition time; 2 s per TR).

Figure 3

Cerebral deactivation associated with the increase of difficulty, as observed when the control task is compared with all of the working memory tasks (P < 0.001 uncorrected), superimposed on two coronal slices (y = 12 and y = 39) and one sagittal slice (x = 0). Deactivation can be observed in the ventral striatum (Left), in the SGPFC (Center), in the VPFC, and in the ACC (Right).

Figure 4

Cerebral activation and deactivation (P < 0.001 uncorrected) superimposed on sagittal views related to (a) activation associated with reward (slices are centered on the Talairach's coordinates: x = 0, y = 57, z = 0), (b) activation common to reward and WM (slices are centered on the Talairach's coordinates: x = 39, y = 54, z = 12), (c) deactivation associated with reward (slices are centered on the Talairach's coordinates: x = 0, y = 9, z = −12), and (d) deactivation common to the reward and WM (slices are centered on the Talairach's coordinates: x = −12, y = 42, z = −6).