When desire collides with reason: functional interactions between anteroventral prefrontal cortex and nucleus accumbens underlie the human ability to resist impulsive desires

Abstract

Human decisions are guided by "desire" or "reason," which control actions oriented toward either proximal or long-term goals. Here we used functional magnetic resonance imaging to assess how the human brain mediates the balance between proximal reward desiring and long-term goals, when actions promoting a superordinate goal preclude exploitation of an immediately available reward option. Consistent with the view that the reward system interacts with prefrontal circuits during action control, we found that behavior favoring the long-term goal, but counteracting immediate reward desiring, relied on a negative functional interaction of anteroventral prefrontal cortex (avPFC) with nucleus accumbens (Nacc) and ventral tegmental area. The degree of functional interaction between avPFC and Nacc further predicted behavioral success during pursuit of the distal goal, when confronted with a proximal reward option, and scaled with interindividual differences in trait impulsivity. These findings reveal how the human brain accomplishes voluntary action control guided by "reason," suggesting that inhibitory avPFC influences Nacc activity during actions requiring a restraint of immediate "desires."

Figure 1.

Experimental design of sequential forced-choice task. A, Desire context: subjects were free to select the conditioned stimulus (i.e., to follow previously acquired stimulus–response–reward associations) if this particular stimulus was not part of the target set. This allowed participants to acquire immediate reward as a bonus during pursuit of the superordinate long-term task goal. B, Desire–reason dilemma: subjects had to counteract the behavioral bias oriented toward immediate reward during accomplishment of the superordinate task goal. The conditioned stimulus was part of the target set. Participants had to collect it once, after its first appearance within the current block. When it occurred a second time in the same block, they were required to reject it, because it had already been collected (see Materials and Methods, Task procedure). Subjects thus had to abandon one bonus point to achieve the superordinate long-term task goal (i.e., 4 points at the end of a block), which required a successful resolution of the desire–reason dilemma. L, Left; R, right.

Figure 2.

Downregulation of reward-related activation during a desire–reason dilemma. A, Significant downregulation of activation in the Nacc during a desire–reason dilemma [i.e., in the direct comparison of the conditioned stimulus presented as nontarget with a conditioned stimulus presented as repeated target (Table 1, column 3; reported at p < 0.05, corrected for false discovery rate)]. B, Significant downregulation of activation in the VTA during the desire–reason dilemma in the same comparison. To illustrate the absolute maxima in the left and right VTA, the statistical criterion of p < 0.05, corrected for familywise error, was used.

Figure 3.

Negative functional interactions of the Nacc during the desire–reason dilemma. A, Increase in negative connectivity between left Nacc and left avPFC (for display purposes, activation is reported at p = 0.001, uncorrected). B, Increase in negative connectivity between right Nacc and bilateral avPFC (p = 0.001, uncorrected). C, Negative correlation of general behavioral success (i.e., mean percentage of correctly rejected conditioned stimuli) with the degree of functional interaction between right Nacc and left avPFC during the desire–reason dilemma. D, Positive correlation between interindividual differences in trait impulsivity and the degree of functional coupling between right Nacc and left avPFC.