Cooperation and deception recruit different subsets of the theory-of-mind network

Abstract

The term "theory of mind" (ToM) describes an evolved psychological mechanism that is necessary to represent intentions and expectations in social interaction. It is thus involved in determining the proclivity of others to cooperate or defect. While in cooperative settings between two parties the intentions and expectations of the protagonists match, they diverge in deceptive scenarios, in which one protagonist is intentionally manipulated to hold a false belief about the intention of the other. In a functional magnetic resonance imaging paradigm using cartoons showing social interactions (including the outcome of the interaction) between two or three story characters, respectively, we sought to determine those brain areas of the ToM network involved in reasoning about cooperative versus deceptive interactions. Healthy volunteers were asked to reflect upon the protagonists' intentions and expectations in cartoons depicting cooperation, deception or a combination of both, where two characters cooperated to deceive a third. Reasoning about the mental states of the story characters yielded substantial differences in activation patterns: both deception and cooperation activated bilateral temporoparietal junction, parietal and cingulate regions, while deception alone additionally recruited orbitofrontal and medial prefrontal regions. These results indicate an important role for prefrontal cortex in processing a mismatch between a character's intention and another's expectations as required in complex social interactions.

Figure 1. Brain activation in frontal, temporoparietal and temporal regions.

Activation patterns are rendered on the brain surface in the contrasts of stories describing deception (DEC), cooperation (COOP) and both (COOPDEC). n = 13, extent threshold k = 15; height threshold p<0.02.

Figure 2. Brain activation in medial frontal, cingulate and parietal regions.

Brain activation patterns are shown for the contrasts of stories describing deception (DEC), cooperation (COOP) and both (COOPDEC). n = 13, extent threshold k = 15; height threshold p<0.02.

Figure 3. Activation in frontal and temporal regions during the different ToM conditions.

The graph shows the mean signal intensity (+/− s.e.m.) (in arbitrary units) in these regions in the conditions DEC (black), COOP (white) and COOPDEC (grey), respectively. The ANOVA with the factors condition and region showed main effects of condition (F(2) = 7.917 p<0.001, region (F(2) = 4.830 p<0.01 and a significant condition*region interaction (F(4) = 9.910 p<0.001 with significantly higher activation in medial prefrontal cortex during DEC compared to COOP and COOPDEC (t(12) = 2.537 p<0.01 and t(12) = 2.290 p<0.01, respectively); in inferior frontal cortex during DEC and COOPDEC compared to COOP (t(12) = 3.041 p<0.01 and t(12) = 4.005 p<0.001), and in temporoparietal junction in COOPDEC compared to DEC (t(12) = 2.079 p<0.01) and COOP (t(12) = 4.173 p<0.001). Activation during DEC was significantly higher in medial PFC than in TPJ (t(12) = 3.179 p<0.01), and during COOP and COOPDEC significantly higher in TPJ than in inferior frontal gyrus (t(12) =  3.726 p<0.01 and t(12) = 2.757 p<0.01).

Figure 4. Examples of the ToM cartoon stories presented to the subjects.

Panels show (A) cooperation, (B) deception, and (C) cooperation/deception. (D) shows an example of a jumbled cartoon story presented in the non-ToM condition.