How pain empathy depends on ingroup/outgroup decisions: A functional magnet resonance imaging study

https://doi.org/10.1016/j.pscychresns.2015.08.006Get rights and content

Highlights

  • The aim of the current work was to examine influences of experimentally generated groups on pain empathy.

  • Therefore, we used a fMRI picture paradigm and manipulated group membership.

  • There was no ingroup bias in the activity of the anterior cingulate cortex or the anterior insula as predicted, although there were interaction effect in several structures.

  • These activation patterns might indicate inhibition of pain experience.

Abstract

Showing empathy is crucial for social functioning and empathy is related to group membership. The aim of the current study was to investigate the influence of experimentally generated groups on empathy for pain in a functional magnetic resonance imaging (fMRI) paradigm. Thirty healthy participants underwent a minimal group paradigm to create two groups. While BOLD contrast was measured using fMRI, subjects were instructed to empathize with ingroup and outgroup members, who were depicted in a picture paradigm of painful and neutral situations. Behavioral measure of state empathy was measured using a visual analog scale. Furthermore, self-reported trait empathy measures were obtained. Repeated-measures ANOVAs were conducted for fMRI and behavioral data. In addition to a main effect of pain in pain-related areas, a main effect of group in areas belonging to the visual cortex was found. Although there was no ingroup bias for empathy ratings, subjects showed altered neural activation in regions of the right fusiform gyrus, the cerebellum, the hippocampal and amygdala region during the pain×group interaction. Activation in the preceding structures, revealed by the interaction of pain by group, suggests that activation in the pallidum might reflect specific empathy for pain-related regulation processes.

Introduction

During daily life situations, we need to classify people all the time. A special type of social classification is to decide, whether a person belongs to one′s own group (“ingroup”) or to another group (“outgroup”). Decisions concerning ingroup membership are a result of social categorization and stereotyping (Tajfel et al., 1971, Jost and Hamilton, 2005). Another explanation is that decisions concerning ingroup membership depend on social projection (the tendency to expect similarity between oneself and others) (Bianchi et al., 2009, DiDonato et al., 2011), as well as shared group norms and congruence with these values (Amiot et al., 2012). The fit between one′s emotional reaction towards a certain situation and the emotional reaction of ingroup members influences the self-categorization as a member of that group (Livingstone et al., 2011). That is called intergroup emotion. The phenomenon to prefer one′s ingroup members is called ingroup favourism, resulting in attribution of more positive characteristics to one′s ingroup (Hewstone et al., 2002). People also tend to show more altruistic behavior towards ingroup members and to show more mistrust towards outgroup members (Baumgartner et al., 2012). An ingroup bias also occurs when groups are generated artificially, so-called minimal groups (Tajfel et al., 1971). There is not only an ingroup bias concerning altruistic behavior, but also concerning empathy – which is assumed to influence altruism and interpersonal behavior. This has been well examined for real groups (Dickter and Bartholow, 2007, Avenanti et al., 2010, Campbell and de Waal, 2011, Cheon et al., 2011, Bruneau et al., 2012). However, whether empathy is also affected by minimal group membership has rarely been explored (Montalan et al., 2012).

Based on empirical neuro-scientific research, some theorists differentiate between two forms of empathy. Distinguished by their underlying neural processes, these are cognitive and affective empathy (Preston and de Waal, 2002, Decety and Jackson, 2004, Shamay-Tsoory et al., 2004, Blair, 2005, Shamay-Tsoory et al., 2009, Shamay-Tsoory, 2011). There is meta-analytic evidence for a core network of empathy, consisting of the anterior insula, the posterior part of the anterior cingulate cortex (pACC) and the anterior part of the medial cingulate cortex (aMCC) (Fan et al., 2011, Lamm et al., 2011, Engen and Singer, 2013). Fan et al. (2011) postulates an association of affective-perceptional empathy with activation in the right anterior insula as well as an association between activation of dorsal aMCC and cognitive-evaluative empathy, which leads to the conclusion that both forms of empathy can be distinguished by specific regional activation differences. Empirically based theories also postulate a limitation to related constructs like emotional contagion or perspective taking (Hein and Singer, 2008, Engen and Singer, 2013).

Affective and cognitive neural mechanisms might work together while people experience empathy (Bernhardt and Singer, 2012). Therefore, focusing just on behavior does not enable understanding of the underlying mechanism. Possibly, both affective mechanisms complement one another and compensate for deficits in the other mechanism, albeit behavioral results are not observably altered.

Recent theories assume a relationship between emotional regulation and empathic abilities (Decety and Lamm, 2006). It has also been shown that there is a positive association between empathic reactions, morally desirable actions, and regulation skills(Eisenberg et al., 1994). On the one hand, executive functions play a role in emotion regulation in the context of empathy, e.g., activation control, attention shifting, attention focusing and inhibition control (Decety and Lamm, 2006, Eisenberg et al., 1994); on the other hand, cognitive strategies such as cognitive reappraisal modulate affective responses (Decety and Lamm, 2006, Cheng et al., 2007) are proposed to regulate the experience of empathy.

There is evidence for gender differences in empathy. It is said that women rate themselves as more empathetic than men (Baron-Cohen and Wheelwright, 2004, Derntl et al., 2010, Borracci et al., 2015), but on closer inspection, empathy in women depends on emotion-associated neural processes whereas men use areas associated with cognitive processing during empathy tasks (Derntl et al., 2010). Reviews of sex differences and gender influences on empathy and related features lead to the conclusion that women show higher affective empathy compared with men; concerning cognitive empathy, it may be the other way round (Christov-Moore et al., 2014).

Empathy for pain is often used as a model for empathy in general, because pain experience results in clearly localizable activation of brain networks, is easy to operationalize, and controllable with regard to the induced state According to the shared network hypothesis of empathy, empathy for pain and self-related pain rely on mutual networks as well as distinct activation patterns (Lamm et al., 2011). Most studies on empathy of pain have found activation in a network including the anterior insula (aI) and the anterior cingulate cortex (ACC) (Morrison et al., 2004, Jackson et al., 2005, Jackson et al., 2006a, Jackson et al., 2006b, Cheng et al., 2007, Gu and Han, 2007, Lamm et al., 2007a, Lamm et al., 2007b, Moriguchi et al., 2007, Saarela et al., 2007, Singer et al., 2004). Other studies have found activation in somato-sensoric areas as well (Morrison et al., 2004, Botvinick et al., 2005, Jackson et al., 2005, Jackson et al., 2006a). Empathy for pain is modulated by pain intensity (Hein and Singer, 2008); contextual factors (Hein and Singer, 2008) such as imitation (De Coster et al., 2013); observer characteristics (Hein and Singer, 2008) such as attention processing and perspective taking ability; alexithymia (Bernhardt and Singer, 2012); prior pain experience (Preis and Kroener-Herwig, 2012, Preis et al., 2013); age (Chen et al., 2014); sex (Coll et al., 2012, Preis and Kroener-Herwig, 2012, Preis et al., 2013); and variables of the observed person (Hein and Singer, 2008) such as affection, similarity to the observer (Preis and Kroener-Herwig, 2012) or group membership (Hein and Singer, 2008, Xu et al., 2009, Hein et al., 2010, Cheon et al., 2011, Bernhardt and Singer, 2012, Montalan et al., 2012).

Recent scientific work has assumed an influence of group membership on empathy for pain. Depending on the used paradigm, racial ingroup membership resulted in a higher activation of the ACC and AI (Xu et al., 2009) or the temporo-parietal junction (TPJ) (Cheon et al., 2011), respectively. The AI and ACC seemed more activated while ingroup members of a soccer fan club were presented (Hein et al., 2010). Perceived ingroup membership has also been associated with AI activity (Bernhardt and Singer, 2012). Results for groups generated by a minimal group paradigm have been rare. A recent study has referred to an ingroup bias for behavioral data: Empathy ratings for ingroup members have shown higher amplitude compared with ratings for outgroup members (Montalan et al., 2012). Therefore, the influence of experimentally induced groups on empathy for pain has still been unexplored.

The current study examined the impact of experimental groups on empathy for pain and its neural correlates. Therefore, empathy for pain was induced by a photo paradigm. After providing self-report data and passing through a minimal group paradigm, subjects underwent functional magnetic resonance imaging (fMRI). It was hypothesized that experimentally induced group membership has an impact on empathy for pain on a behavioral level as well as on a neural level. Subjects experiencing empathy for pain show a higher activation in the AI and ACC (Jackson et al., 2005, Jackson et al., 2006a, Jackson et al., 2006b). Those two areas are hypothesized to show activation differences during empathy for pain for ingroup members as an interactional effect between pain and group membership, as has previously been demonstrated for ethnic groups (Xu et al., 2009). Furthermore, subjects were expected to show differences in empathy for pain rating when they were watching their ingroup members compared with watching outgroup members.

Section snippets

Subjects

Thirty healthy, right-handed volunteers (see Table 1) participated in the experiment. To be included, subjects had to be 18–35 years of age and without either a history of or current neurological or psychiatric disease. They also had to have normal or corrected-to-normal vision. After the fMRI session, all of the volunteers were paid 20 €. The study was approved by the local ethics committee of the medical faculty, Philipps-University Marburg.

Procedure

The study consisted of two parts, an online

Behavioral measures

As shown in Table 1, identification and competence ratings, done as a manipulation check, showed significant differences for ingroup and outgroup members (identification: T(29)=4.631, p<0.001; competence: T(29)=4.546, p<0.001) whereas sympathy ratings between groups did not become significant (sympathy: T(29)=1.474, p=0.151). It can be concluded that the experimental group manipulation was successful, although subjects did not report an ingroup favouratism concerning sympathy. There were no

Discussion

The current study explored how pain empathy is modulated by experimentally induced group membership (minimal group paradigm). This differs from former studies which focused on real groups such as ethnic groups (Xu et al., 2009) or groups of the same preference (soccer fans) (Hein et al., 2010). The photographs used for the picture paradigm were well evaluated for operationalizing pain empathy (Jackson et al., 2005, Moriguchi et al., 2007, Gu et al., 2010). Pictures belonging to the pain

Conflict of interest

The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest.

Acknowledgments

This work was supported by the excellence initiative “Landes-Offensive zur Entwicklung Wissenschaftlich-ökonomischer Exzellenz” (LOEWE) of the Hessian Ministry for Science and Arts, Germany.

We thank the reviewers for their substantial and helpful comments on an earlier version of this manuscript. Further, we are very grateful to Mechthild Wallnig and Rita Werner for their contribution in the fMRI data collection as well as Steffi Tank for providing language help.

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