Selective functional integration between anterior temporal and distinct fronto-mesolimbic regions during guilt and indignation

Abstract

It has been hypothesized that the experience of different moral sentiments such as guilt and indignation is underpinned by activation in temporal and fronto-mesolimbic regions and that functional integration between these regions is necessary for the differentiated experience of these moral sentiments. A recent fMRI study revealed that the right superior anterior temporal lobe (ATL) was activated irrespective of the context of moral feelings (guilt or indignation). This region has been associated with context-independent conceptual social knowledge which allows us to make finegrained differentiations between qualities of social behaviours (e.g. "critical" and "faultfinding"). This knowledge is required to make emotional evaluations of social behaviour. In contrast to the context-independent activation of the ATL, there were context-dependent activations within different fronto-mesolimbic regions for guilt and indignation. However, it is unknown whether functional integration occurs between these regions and whether regional patterns of integration are distinctive for the experience of different moral sentiments. Here, we used fMRI and psychophysiological interaction analysis, an established measure of functional integration to investigate this issue. We found selective functional integration between the right superior ATL and a subgenual cingulate region during the experience of guilt and between the right superior ATL and the lateral orbitofrontal cortex for indignation. Our data provide the first evidence for functional integration of conceptual social knowledge representations in the right superior ATL with representations of different feeling contexts in fronto-mesolimbic regions. We speculate that this functional architecture allows for the conceptually differentiated experience of moral sentiments in healthy individuals.

Neural systems for guilt from actions affecting self versus others

“…These regions were largely consistent with the regions about which we hypothesized based on prior work, particularly with respect to inferior frontal gyrus (Shin et al, 2000; Takahashi et al, 2004), frontopolar cortex (Basile et al, 2010; Moll et al, 2007; Moll et al, 2011), dorsomedial PFC (Kedia et al, 2008; Takahashi et al, 2004), supramarginal gyrus (Kedia et al, 2008; Moll et al, 2007), and at a reduced significance threshold also septal/subgenual cingulate areas (Basile et al, 2010; Green et al, 2010; Moll et al, 2011; Zahn et al, 2009a; Zahn et al, 2009c). However, other hypothesized areas including the posterior STS (Takahashi et al, 2004), posterior cingulate/precuneus (Basile et al, 2010; Kedia et al, 2008) and the anterior temporal poles (Shin et al, 2000) were not observed in our results.…”

“…For instance, Shin and colleagues (2000) also examined a similar range of emotions and compared the magnitude of these emotions elicited by guilt scripts as compared to neutral scripts. However, Shin et al and most prior studies did not actually compare the magnitude of these emotions to the magnitude of guilt elicited specifically by the guilt scripts (Basile et al, 2010; Kedia et al, 2008; Ruby and Decety, 2004; Shin et al, 2000; Takahashi et al, 2004; Zahn et al, 2009c), while some assessed this relationship in a few select emotions (Green et al, 2010; Kedia et al, 2008; Zahn et al, 2009c) or none at all (Basile et al, 2010; Takahashi et al, 2004). One notable exception by Moll et al (2007) found that the emotional scripts elicited the following emotions in order of intensity: indignation-other, guilt, compassion, embarrassment, indignation-self, and disgust.…”

“…Within this broader area, a small number of studies have focused on guilt (Basile et al, 2010; Green et al, 2010; Kedia et al, 2008; Moll et al, 2011; Shin et al, 2000; Takahashi et al, 2004; Zahn et al, 2009C). Personal scripts eliciting guilt that were read during PET scanning recruited bilateral anterior temporal cortex, anterior cingulate gyrus, left anterior insula, and left inferior frontal gyrus (Shin et al, 2000).…”

“…We hypothesized that the intensity of guilt associated with harm to others would be greater than for harm to self. Specifically, we predicted that guilt would be associated with regions implicated in prior research including the inferior frontal gyrus (Shin et al, 2000; Takahashi et al, 2004), posterior STS (Takahashi et al, 2004), frontopolar cortex (Basile et al, 2010; Moll et al, 2007; Moll et al, 2011; Kedia et al, 2008; Takahashi et al, 2004), septal and the nearby subgenual cingulate areas (Basile et al, 2010; Green et al, 2010; Moll et al, 2011; Zahn et al, 2009a; Zahn et al, 2009c), posterior cingulate/precuneus (Basile et al, 2010; Kedia et al, 2008), temporoparietal junction (Kedia et al, 2008; Moll et al, 2007), and the anterior temporal poles (Shin et al, 2000). Furthermore, we predicted that guilt feelings for negative events that affect others would activate guilt regions that are differentially responsive by social and interpersonal consequences.…”

Proneness to Decreased Negative Emotions in Major Depressive Disorder when Blaming Others rather than Oneself

“…This was based on the assumption that people are not able to distinguish emotions such as shame, guilt, or self-contempt/disgust well [16]. Recent work on the neural basis of moral emotions [38], however, has shown that participants exhibit distinctive neural signatures to be associated with stimuli subjectively reported as evocative of a particular moral emotion [39,40]. This is in keeping with anthropological evidence of transcultural ubiquity of distinct moral emotions [41] that must rely on transculturally stable conceptual underpinnings [42].…”