Affective Modulation of Cognitive Control is Determined by Performance-Contingency and Mediated by Ventromedial Prefrontal and Cingulate Cortex

Cognitive control requires a fine balance between stability, the protection of an on-going task-set, and flexibility, the ability to update a task-set in line with changing contingencies. It is thought that emotional processing modulates this balance, but results have been equivocal regarding the direction of this modulation. Here, we tested the hypothesis that a crucial determinant of this modulation is whether affective stimuli represent performance-contingent or task-irrelevant signals. Combining functional magnetic resonance imaging with a conflict task-switching paradigm, we contrasted the effects of presenting negative-and positive-valence pictures on the stability/flexibility trade-off in humans, depending on whether picture presentation was contingent on behavioral performance. Both the behavioral and neural expressions of cognitive control were modulated by stimulus valence and performance contingency: in the performance-contingent condition, cognitive flexibility was enhanced following positive pictures, whereas in the nonperformance-contingent condition, positive stimuli promoted cognitive stability. The imaging data showed that, as anticipated, the stability/flexibility trade-off per se was reflected in differential recruitment of dorsolateral frontoparietal and striatal regions. In contrast, the affective modulation of stability/flexibility shifts was mirrored, unexpectedly, by neural responses in ventromedial prefrontal and posterior cingulate cortices, core nodes of the "default mode" network. Our results demonstrate that the affective modulation of cognitive control depends on the performance contingency of the affect-inducing stimuli, and they document medial default mode regions to mediate the flexibility-promoting effects of performance-contingent positive affect, thus extending recent work that recasts these regions as serving a key role in on-task control processes.