Humans readily adopt an intentional stance to other people, comprehending their behavior as guided by unobservable mental states such as belief, desire, and intention. We used fMRI in healthy adults to test the hypothesis that this stance is primed by the default mode of human brain function present when the mind is at rest. We report three findings that support this hypothesis. First, brain regions activated by actively adopting an intentional rather than nonintentional stance to a social stimulus were anatomically similar to those demonstrating default responses to fixation baseline in the same task. Second, moment-to-moment variation in default activity during fixation in the dorsomedial PFC was related to the ease with which participants applied an intentional—but not nonintentional—stance to a social stimulus presented moments later. Finally, individuals who showed stronger dorsomedial PFC activity at baseline in a separate task were generally more efficient when adopting the intentional stance and reported having greater social skills. These results identify a biological basis for the human tendency to adopt the intentional stance. More broadly, they suggest that the brain's default mode of function may have evolved, in part, as a response to life in a social world.

A reliable observation in neuroimaging studies of cognitive control is the response of dorsal ACC (dACC) to events that demand increased cognitive control (e.g., response conflicts and performance errors). This observation is apparently at odds with a comparably reliable association of the dACC with the subjective experience of negative affective states such as pain, fear, and anxiety. Whereas “affective” associates of the dACC are based on studies that explicitly manipulate and/or measure the subjective experience of negative affect, the “cognitive” associates of dACC are based on studies using tasks designed to manipulate the demand for cognitive control, such as the Stroop, flanker, and stop-signal tasks. Critically, extant neuroimaging research has not systematically considered the extent to which these cognitive tasks induce negative affective experiences and, if so, to what extent negative affect can account for any variance in the dACC response during task performance. While undergoing fMRI, participants in this study performed a stop-signal task while regularly reporting their experience of performance on several dimensions. We observed that within-subject variability in the dACC response to stop-signal errors tracked changes in subjective frustration throughout task performance. This association remained when controlling for within-subject variability in subjective reports of cognitive engagement and several performance-related variables indexing task difficulty. These results fit with existing models characterizing the dACC as a hub for monitoring ongoing behavior and motivating adjustments when necessary and further emphasize that such a function may be linked to the subjective experience of negative affect.

Humans commonly understand the unobservable mental states of others by observing their actions. Embodied simulation theories suggest that this ability may be based in areas of the fronto-parietal mirror neuron system, yet neuroimaging studies that explicitly investigate the human ability to draw mental state inferences point to the involvement of a “mentalizing” system consisting of regions that do not overlap with the mirror neuron system. For the present study, we developed a novel action identification paradigm that allowed us to explicitly investigate the neural bases of mentalizing observed actions. Across repeated viewings of a set of ecologically valid video clips of ordinary human actions, we manipulated the extent to which participants identified the unobservable mental states of the actor ( mentalizing ) or the observable mechanics of their behavior ( mechanizing ). Although areas of the mirror neuron system did show an enhanced response during action identification, its activity was not significantly modulated by the extent to which the observers identified mental states. Instead, several regions of the mentalizing system, including dorsal and ventral aspects of medial pFC, posterior cingulate cortex, and temporal poles, were associated with mentalizing actions, whereas a single region in left lateral occipito-temporal cortex was associated with mechanizing actions. These data suggest that embodied simulation is insufficient to account for the sophisticated mentalizing that human beings are capable of while observing another and that a different system along the cortical midline and in anterior temporal cortex is involved in mentalizing an observed action.