Hedonic Hotspots Regulate Cingulate-driven Adaptation to Cognitive Demands

Abstract

Positive hedonic states are known to attenuate the impact of demanding events on our body and brain, supporting adaptive behavior in response to changes in the environment. We used functional magnetic resonance imaging to examine the neural mechanism of this hedonic regulation. The effect of hedonic state (as induced by funny vs. neutral cartoons) on flexible behavioral and neural adaptation to cognitive demands was assessed in a flanker task in female volunteers. Behavioral results showed that humor reduced the compensatory adjustments to cognitive demands, as observed in sequential adaptations. This modulation was also reflected in midcingulate cortex (MCC; also known as the dorsal anterior cingulate cortex, ACC) activation. Furthermore, hedonic context increased activation in ventral striatum (VS) and ventral pallidum (VP). These hedonic hotspots attenuated the medial prefrontal cortex response to the cognitive demands in the ACC (also known as the rostral ACC). Activity in the ACC proved predictive of subsequent behavioral adaptation. Moreover, psychophysiological interaction analyses revealed that the MCC and the ACC were functionally connected with VS and VP, respectively. These observations reveal how MCC-VS and VP-ACC interactions are involved in the detection and hedonic modulation of behavioral adaptations to cognitive demands, which supports behavioral flexibility.