Our first hypothesis was confirmed; when appraising one's own or others social actions, conceptual generalization was associated with higher emotional intensity. This association was consistent across MDD and control groups as well as conditions (POS_S-AG, NEG_S-AG, POS_O-AG, NEG_O-AG). The second hypothesis was also confirmed; redundant integration of conceptually differentiated information regarding one's own relative to others’ negative actions was associated with self-hate on the IGQ-67 and MDD. This was demonstrated by showing higher interdependence of conceptual overgeneralization and negative emotional biases in the MDD group. This was reproducible in the MDD subgroup not taking medication, thereby ruling out abnormal performance due to effects of antidepressants. Individuals with higher interdependence of conceptual overgeneralization and negative emotional biases also showed stronger self-hate, even when correcting for effects of group.
Confirming our third hypothesis, we found that individuals displaying nonredundant integration of conceptual information when appraising negative actions showed increased coupling of the right superior ATL with frontal-subcortical circuits, for guilt relative to indignation, irrespective of group. Interestingly, this included an anterior right dorsolateral PFC area, previously associated with cognitive reappraisal of emotions (Ochsner & Gross, 2005
; Wiech et al., 2006
). As predicted, this analysis yielded ATL-septal area coupling. However, this did not include the expected subgenual cingulate region across groups, which only emerged when focusing the analysis on between-subject differences in the control group. In addition to the subgenual cingulate/septal area, this analysis revealed frontopolar and hypothalamic areas of ATL coupling previously shown to be strong in people at low risk of MDD (Green, Lambon Ralph, et al., 2012
). This result demonstrated that control individuals with high ATL coupling in these areas when feeling guilty display nonredundant conceptual–emotional integration.
We were able to show that perceived emotional intensity and conceptual generalization are interdependent on a trial-by-trial basis. We further validated the number of concepts chosen as a measure of conceptual generalization by showing its high association with a more complex measure that takes normative data on the associative strength (i.e., dominance, (Ashcraft, 1978
)) between a given concept and a given social behavior into account (Supplementary Results). This dominance-weighted measure showed that participants choosing a high number of concepts to describe social behavior did so, because they selected concepts that were not highly associated with the given behavior in a normative sample (e.g., choosing the concept “possessive” among others to describe one's act of gossiping about one's best friend, ) as a sign of conceptual overgeneralization. This demonstrated that the concepts provided in the task were unrelated enough to one another to prevent participants from describing multiple distinct aspects equally related to a given social behavior by using multiple concepts. Providing a selection of distinct but equally applicable concepts would have rendered the number of concepts chosen unusable as an index of conceptual generalization.
This confirms the hypothesis that conceptual differentiation plays a role in the experience of emotions. However, the task did not allow us to determine whether conceptual generalization caused increased perception of emotional intensity or whether access to conceptual information was reduced when participants faced more emotionally intense stimuli. The degree of interdependence between conceptual overgeneralization and emotional appraisal was found to be stronger in MDD and in individuals with overgeneralized self-blaming emotions as measured on the IGQ-67 self-hate scale. Since we controlled for the overall degree of conceptual generalization/differentiation and emotional intensity, which did not differ between groups and were not associated with self-hate, this result points to other complementary cognitive components of appraisal that must influence the relationship between conceptual generalization and perceived emotional intensity of social behavior. Although, the CSKD task did not identify those other cognitive components directly, we were able to identify their neural correlates by correlating between-subject differences on conceptual generalization-dependence of emotional intensity with fMRI measures of functional integration with the right superior ATL.
Individuals showing noninterdependence between conceptual overgeneralization and intensity of negative emotions (i.e., nonredundant integration of conceptual information) exhibited stronger functional coupling of the right ATL and the ipsilateral anterior dorsolateral PFC, as well as the septal part of the nucleus accumbens for guilt (self-blaming emotion) relative to indignation (other-blaming emotion). By inclusively masking with guilt versus fixation, we ensured that these effects arose as relative increases in coupling for guilt compared with both control conditions. This sheds new light on the evidence that dysfunction of the dorsolateral PFC contributes to symptoms of major depression (Price & Drevets, 2010
; Siegle, Thompson, Carter, Steinhauer, & Thase, 2007
) and that its lesion was associated with higher rates of depression in patients with penetrating head injuries (Koenigs et al., 2008
). While the lack of dorsolateral PFC function in MDD is usually seen as due to a lack of regulating negative emotions (Price & Drevets, 2010
; Siegle et al., 2007
), our findings point to a more specific role in protecting against self-blaming biases.
Similar right anterior dorsolateral PFC areas have been shown to be activated for reappraisal (i.e., changing the meaning (Ochsner & Gross, 2005
)) of emotional stimuli and thereby decreasing their perceived intensity (Ochsner & Gross, 2005
; Wiech et al., 2006
). While there is general agreement on the importance of the right anterior dorsolateral PFC for reappraisal of emotions, for moral judgments (Greene, Nystrom, Engell, Darley, & Cohen, 2004
), and for social-executive functions including empathic perspective taking (Eslinger, Moore, Anderson, & Grossman, 2011
), there are different views on the exact contribution of the dorsolateral PFC to socio-moral functioning (Moll & de Oliveira-Souza, 2007
). The cognitive control model predicts that the dorsolateral PFC modulates information stored elsewhere in the brain (Miller & Cohen, 2001
), whereas representational models of dorsolateral PFC function predict sequential event and action context information to be stored in this area (Moll, Zahn, de Oliveira-Souza, Krueger, & Grafman, 2005
; Wood & Grafman, 2003
). Our results would be compatible with both theoretical perspectives.
Our finding of increased ATL coupling with the septal part of the nucleus accumbens when feeling guilty relative to indignation in individuals showing adaptive integration of conceptual information was predicted from our previous work on guilt-selective functional disconnections of these regions in the remitted MDD group (Green, Lambon Ralph, et al., 2012
) and strong coupling in people at low risk of MDD (Green et al., 2010
). The current results confirm the hypothesis that the degree of coupling when experiencing guilt is associated with the degree of nonredundancy with which conceptual information is integrated into the experience of emotions. Previous studies have shown that the septal region is selectively activated when donating to charity relative to receiving monetary reward (Moll et al., 2006
) and when cooperating in trust games (Krueger et al., 2007
). The septal region was also more active in guilt-prone people (Green, Lambon Ralph, et al., 2012
; Zahn, Moll, Paiva, et al., 2009
) when feeling guilt compared with indignation. Moreover, neurodegeneration in this region was shown to lead to a loss of experimentally probed guilt and pity while controlling for other negative emotions such as embarrassment, disgust, and anger (Moll et al., 2011
). This evidence is in keeping with the prediction that the septal region hosts representations of key ingredients for affiliative emotions such as guilt and pity (Moll et al., 2008
). The current study shows that individuals differ with respect to how they integrate conceptual knowledge within the ATL with emotional information in the septal region and that this affects their resilience toward MDD.
Unexpectedly, however, ATL coupling with the adjacent subgenual cingulate region, reproducibly shown to be activated selectively for guilt (Basile et al., 2011
; Green, Lambon Ralph, et al., 2012
; Morey et al., 2012
; Zahn, de Oliveira-Souza, et al., 2009
, Zahn, Moll, Paiva, 2009
), did not differ between participants with redundant and nonredundant integration of conceptual information when appraising negative emotions across both groups. The subgenual cingulate region emerged, however, together with a network of hypothalamic and frontopolar regions previously shown to display guilt-selective functional disconnection in MDD (Green, Lambon Ralph, et al., 2012
), when repeating the analysis in the control group only. A further analysis showed that there were relatively few individuals in the MDD group who exhibited higher subgenual cingulate coupling in the guilt relative to the indignation condition at all. This “floor” effect in the MDD group may explain why analyses of between-subject differences across groups in this area did not yield significant results. This is in keeping with the evidence that the subgenual cingulate plays a key role in the pathophysiology of MDD (Drevets, Ongur, & Price, 1998
; Ressler & Mayberg, 2007
) and that its stimulation leads to remission of depressive symptoms (Mayberg et al., 2005
Although our main analysis focused on the interdependence of conceptual information and emotions, we also explored neural correlates of individual differences in conceptual differentiation of social actions irrespective of its influence on emotions. Interestingly, individuals who conceptually differentiated to a higher degree in the NEG_S-AG than in the NEG_O-AG condition exhibited stronger inter-hemispheric ATL coupling for guilt relative to indignation. Higher inter-hemispheric ATL coupling, however, was also displayed by individuals who showed redundant integration of conceptual information when making emotional appraisals. Thus, inter-hemispheric ATL coupling appears to be employed by individuals who are well able to differentiate conceptually when appraising their negative actions, but who may over-rely on their conceptual system when making emotional appraisals and may, therefore, be more vulnerable to self-negative biases when their conceptual system fails to protect against overgeneralization. Integration of conceptual information across hemispheres is compatible with the view that conceptual knowledge is represented bilaterally (Ralph, Pobric, & Jefferies, 2009
), thereby allowing for compensation of unilateral ATL lesions through contralateral take-over of function (Ralph, Ehsan, Baker, & Rogers, 2012
) (Warren, Crinion, Ralph, & Wise, 2009
). Bilateral organization of social conceptual information would also explain why some studies found selective activations for social stimuli in the left (Ross & Olson, 2010
), some in the right (Skipper et al., 2011
; Zahn et al., 2007
), and others in bilateral ATLs (Simmons, Reddish, Bellgowan, & Martin, 2010
). Further studies are needed to confirm a role of inter-hemispheric ATL coupling in enhancing conceptual differentiation capacity and to determine the unique contributions of each hemisphere.
Previous studies assessing the redundancy of associations between social concepts across different aspects of the self (e.g., work, relationship) used card sorting tasks in remitted MDD and found either reduced redundancy for positive (Dalgleish et al., 2011
) or increased redundancy for negative information (Dozois & Dobson, 2001
). This is concordant with our finding of changes in the cognitive architecture of social knowledge in MDD persisting into the remitted stage. Redundancy was previously defined as the repeated use of a given social concept or phrase to describe several aspects of one's self (Dozois & Dobson, 2001
) or periods of one's past self (Dalgleish et al., 2011
). Thus, redundancy referred to the architecture of associations between social concepts and autobiographical or situational context. The finding of increased redundancy of associations for negative social information (Dozois & Dobson, 2001
), despite not specifically assessing the contribution of conceptual differentiation (i.e., whether people accessed knowledge of differentiated aspects of the meaning of their behavior), concurs with our result of higher redundancy between conceptual and other aspects of information relevant to emotional appraisal in remitted MDD.
On a more cautionary note, this study did not determine to what degree redundant social conceptual integration is a scar effect (Lewisohn, Steinmetz, Larson, & Franklin, 1981
; Wichers, Geschwind, van Os, & Peeters, 2010
) of a previous depressive episode versus the correlate of a primary vulnerability to MDD. Regarding confounding factors that may have affected task performance, one needs to consider executive demands of the task, ability, and motivation to follow the instructions, as well as the general level of conceptual differentiation, which may be influenced by educational factors. All these factors were carefully controlled by focusing the analysis on the comparison of carefully matched task conditions of self- and other-agency. Thus, all these confounding factors were equal for the compared conditions and can therefore not explain individual differences in conceptual differentiation depending on agency.