Necessary, Yet Dissociable Contributions of the Insular and Ventromedial Prefrontal Cortices to Norm Adaptation: Computational and Lesion Evidence in Humans

Abstract

Social norms and their enforcement are fundamental to human societies. The ability to detect deviations from norms and to adapt to norms in a changing environment is therefore important to individuals' normal social functioning. Previous neuroimaging studies have highlighted the involvement of the insular and ventromedial prefrontal (vmPFC) cortices in representing norms. However, the necessity and dissociability of their involvement remain unclear. Using model-based computational modeling and neuropsychological lesion approaches, we examined the contributions of the insula and vmPFC to norm adaptation in seven human patients with focal insula lesions and six patients with focal vmPFC lesions, in comparison with forty neurologically intact controls and six brain-damaged controls. There were three computational signals of interest as participants played a fairness game (ultimatum game): sensitivity to the fairness of offers, sensitivity to deviations from expected norms, and the speed at which people adapt to norms. Significant group differences were assessed using bootstrapping methods. Patients with insula lesions displayed abnormally low adaptation speed to norms, yet detected norm violations with greater sensitivity than controls. Patients with vmPFC lesions did not have such abnormalities, but displayed reduced sensitivity to fairness and were more likely to accept the most unfair offers. These findings provide compelling computational and lesion evidence supporting the necessary, yet dissociable roles of the insula and vmPFC in norm adaptation in humans: the insula is critical for learning to adapt when reality deviates from norm expectations, and that the vmPFC is important for valuation of fairness during social exchange.

Informational and Normative Influences in Conformity from a Neurocomputational Perspective

“…In the critical phase, when both groups received medium offers for several trials, they demonstrated increased insula activation when offers differed from a previously established norm. The idea that the anterior insula has a key role in processing norms is further supported in a study of patients with insula lesions who adapted slower to new norms compared with healthy controls [76]. These findings underline an involvement of the insula in normative decision-making, possibly by signalling unexpected outcomes regardless of whether they are positive or negative [47].…”

Diffusion of responsibility attenuates altruistic punishment: A functional magnetic resonance imaging effective connectivity study

“…With direct connectivity between dmPFC and target regions (i.e., AI, vmPFC, and precuneus), mentalizing processes implemented by dmPFC modulated neural responses of AI, vmPFC and precuneus, all of which have been previously implicated in punishment behaviors [Baumgartner et al, ; Feng et al, ; Gu et al, ; Xiang et al, ]. The AI is a key region that mediates altruistic punishments [Grecucci et al, ; Harlé et al, ] by encoding deviations from social norms [Civai et al, ].…”

“…The neural and behavioral responses to norm violations do not represent simple heuristics, but are sensitive to social contexts [Güroğlu et al, ; Hu et al, ; Wu et al, ; Yu et al, ], supporting the idea that human motivations to enforce social norms are flexible [Chang and Sanfey, ]. As core regions underlying altruistic punishment, activations of AI and vmPFC predict amounts of punishment to transgressions by respectively signaling norm deviations [Harlé et al, ; Wright et al, ] and valuation of social norms [Gu et al, ; Xiang et al, ] in a context‐dependent manner. The effects of social contexts on altruistic punishment often reflect the modulations of other neural networks, such as the mentalizing network consisting of dorsomedial PFC (dmPFC) and temporo‐parietal junction [Baumgartner et al, ; Güroğlu et al, ; Halko et al, ] and reappraisal network consisting of ventrolateral PFC (vlPFC) [Grecucci et al, ; Tabibnia et al, ].…”

Not on my team: Medial prefrontal cortex responses to ingroup fusion and unfair monetary divisions

“…The response in these regions has been shown to predict helping of outgroup members and differential punishment of ingroup versus outgroup behaviors. Moreover, lesions to these regions are associated with changes in social cognition abilities and social behaviors (Barrash, Tranel, & Anderson, 2000; Bechara, Tranel, & Damasio, 2000; Blair & Cipolotti, 2000; Gu et al., 2015; Hadland et al., 2003; Saver & Damasio, 1991; Tranel et al., 2002). Here, we show that three key regions of the mPFC (putatively areas 8, 9 and 32) show differential responses to (un)fairness depending on whether the individual performing the behavior is an ingroup, outgroup, or neutral individual.…”

“…Lesions to these regions impair and reduce the execution of social behaviors and can lead to the inability to adhere to group or social norms (Anderson, Bechara, Damasio, Tranel, & Damasio, 1999; Gu et al., 2015; Hadland, Rushworth, Gaffan, & Passingham, 2003; Rudebeck, Buckley, Walton, & Rushworth, 2006; Tranel, Bechara, & Denburg, 2002). Notably, accounts have highlighted that these regions play important roles in processing information about group membership and categorization, and information regarding whether the actions of others violate group norms (Cikara, Jenkins, Dufour, & Saxe, 2014; Cikara & Van Bavel, 2014; Hein, Silani, Preuschoff, Batson, & Singer, 2010; Molenberghs, Gapp, Wang, Louis, & Decety, 2016; Molenberghs & Morrison, 2014).…”