Cognitive regulation during decision making shifts behavioral control between ventromedial and dorsolateral prefrontal value systems

Abstract

Cognitive regulation is often used to influence behavioral outcomes. However, the computational and neurobiological mechanisms by which it affects behavior remain unknown. We studied this issue using an fMRI task in which human participants used cognitive regulation to upregulate and downregulate their cravings for foods at the time of choice. We found that activity in both ventromedial prefrontal cortex (vmPFC) and dorsolateral prefrontal cortex (dlPFC) correlated with value. We also found evidence that two distinct regulatory mechanisms were at work: value modulation, which operates by changing the values assigned to foods in vmPFC and dlPFC at the time of choice, and behavioral control modulation, which operates by changing the relative influence of the vmPFC and dlPFC value signals on the action selection process used to make choices. In particular, during downregulation, activation decreased in the value-sensitive region of dlPFC (indicating value modulation) but not in vmPFC, and the relative contribution of the two value signals to behavior shifted toward the dlPFC (indicating behavioral control modulation). The opposite pattern was observed during upregulation: activation increased in vmPFC but not dlPFC, and the relative contribution to behavior shifted toward the vmPFC. Finally, ventrolateral PFC and posterior parietal cortex were more active during both upregulation and downregulation, and were functionally connected with vmPFC and dlPFC during cognitive regulation, which suggests that they help to implement the changes to the decision-making circuitry generated by cognitive regulation.

Figure 1.

Experimental procedure and behavioral results. A, Structure and timing of an experimental trial. ITI, Intertrial interval. B, Average bids for each condition. DIST, DISTANCE; NAT, NATURAL; IND, INDULGE. Error bars show SEM. **p < 0.001.

Figure 2.

Evidence for value modulation during the full evaluation period. A, B, vmPFC (A) and right dlPFC (B) regions that correlated with bids during NATURAL trials, and (from left to right) changes in activation in these regions in DISTANCE − NATURAL trials, INDULGE − NATURAL trials, and INDULGE − DISTANCE trials.

Figure 3.

Evidence for behavioral control modulation that varies as a function of time during cognitive regulation. A–C, vmPFC (A), left dlPFC (B), and right dlPFC (C) regions in which a linear contrast of correlation with behavior in each condition (DISTANCE = −1; NATURAL = 0; INDULGE = +1) showed a significant interaction with time (early evaluation vs late response initiation). The hot colors indicate greater correlation with behavior in INDULGE compared with DISTANCE. The cool colors indicate the opposite. D–F, Time course of activation in each condition (blue, DISTANCE; green, NATURAL; yellow, INDULGE). Parameter estimates indicate the average strength of association with bid at each time point, and encompass a 20 s window beginning at onset of instruction (see Materials and Methods for details). The dashed vertical lines demarcate trial events and are shifted forward 5 s to account for hemodynamic lag. The horizontal double lines at the top of the plots indicate time points at which two conditions differ (p < 0.05). The line colors indicate the conditions being compared. Transparent areas indicate SEM.

Figure 4.

Correlation between individual differences in regulatory success and differences in correlation with bid at the end of the choice period for vmPFC in DISTANCE − NATURAL trials (A), vmPFC in INDULGE − NATURAL trials (B), left dlPFC in DISTANCE − NATURAL trials (C), and left dlPFC in INDULGE − NATURAL trials (D).

Figure 5.

Regions implementing cognitive regulation. Regions more activated during DISTANCE − NATURAL trials (A), and INDULGE − NATURAL trials (B). C, Overlap between DISTANCE (blue) and INDULGE (red) in left vlPFC and PPC. Time courses of BOLD activation are displayed for left PPC (right) and left vlPFC (left). See Materials and Methods for details.