Elsevier

NeuroImage

Volume 30, Issue 1, March 2006, Pages 313-324
NeuroImage

Neural correlates of regulating negative emotions related to moral violations

https://doi.org/10.1016/j.neuroimage.2005.09.034Get rights and content

Abstract

Previous neuroimaging studies have identified several brain regions associated with regulating emotional responses. Different kinds of emotional stimuli, however, may recruit different regulatory processes and, in turn, recruit different regions. We compared emotion regulation for two types of negative emotional stimuli: those involving moral violations (moral stimuli), and those not involving moral violations (non-moral stimuli). In addition, we investigated whether activation in medial prefrontal cortex (MPFC), a region implicated previously in specifically moral processing, may instead reflect greater social and emotional content. Ten female subjects were scanned using fMRI while they passively viewed or were instructed to decrease emotional reactions to moral and non-moral pictures closely matched on social and emotional content. Passive viewing of both picture types elicited similar activations in areas related to the processing of social and emotional content, including MPFC and amygdala. During regulation, different patterns of activation in these regions were observed for moral vs. non-moral pictures. These results suggest that the neural correlates of regulating emotional reactions are modulated by the emotional content of stimuli, such as moral violations. In addition, the current findings suggest that some brain regions previously implicated in moral processing reflect the processing of greater social and emotional content in moral stimuli.

Introduction

The ability to distinguish between actions that are considered appropriate or inappropriate, based on a system of moral values, is of considerable importance to both the individual and society. How individuals develop moral values and exercise moral behavior has been examined in many fields of study. This topic has received attention within the domain of cognitive neuroscience only recently, and its neural correlates are only beginning to be understood.

The important role that emotion plays in moral thought and behavior has been increasingly recognized (Damasio, 1994, Haidt, 2001, Haidt, 2003). Situations in which moral issues are involved are typically emotionally charged, and emotions often serve to guide moral appraisals. In certain situations, however, emotions that are associated with moral situations can be undesirable, and may require cognitive reappraisal to diminish the unwanted emotional response. For example, a criminal defense attorney may find it necessary to publicly justify a crime that they privately consider morally reprehensible, an experience that creates an unpleasant emotional state. However, to perform his or her job effectively, the same individual must be able to set aside such feelings, or reappraise the situation in a way that renders it less emotionally distressing. In fact, the regulation of these emotions may be considered a skill that must be refined for optimal job performance. Whether regulation of emotions related to moral violations is similar to emotion regulation involving other emotional experiences, such as fear of visiting a dentist, is yet unknown. Moral emotion regulation may recruit additional cognitive processes not recruited during emotional regulation for other types of situations. In the current study, our focus was on investigating the neural correlates of processing moral emotional stimuli (i.e., those involving moral violations) and non-moral emotional stimuli (i.e., those not involving moral violations), as well as the neural correlates associated with voluntary regulation of these emotions, using functional magnetic resonance imaging (fMRI).

Recent neuroimaging studies (using fMRI) have identified a network of brain regions involved in moral processing, including medial prefrontal cortex (MPFC), superior temporal sulcus (STS), and less consistently, posterior cingulate. These studies used a variety of paradigms ranging from picture viewing (Moll et al., 2002a) to decision making (Greene et al., 2001, Greene et al., 2004, Moll et al., 2002b, Heekeren et al., 2003, Heekeren et al., 2005), but all typically compared pictures or statements/scenarios depicting moral violations to similar stimuli without moral content. For example, Moll et al. (2002a) contrasted moral statements (‘The elderly are useless’) with similar non-moral statements (‘The elderly sleep more at night’), and reported activity in MFG and STS in response to moral statements only. Greene et al. (2001) compared judgments regarding moral dilemmas containing a high degree of emotional content (where harm is directly caused to another person) to those with less emotional content (where harm is indirectly caused to another person) as well as to non-moral dilemmas, and found that the highly emotional moral dilemmas activated MFG, STS, and posterior cingulate.

Although most neuroimaging studies involving moral tasks include comparable non-moral tasks designed to differ only in moral content, moral stimuli are inherently more emotionally arousing and include more social content (i.e., faces, interaction between individuals) compared to non-moral stimuli. For example, Moll et al. (2002b) used unpleasant pictures with or without moral violations. While the moral pictures often showed personal interactions, such as one individual causing harm to another, the unpleasant pictures primarily consisted of objects, such as snakes or cigarettes. Although MFG and STS were activated specifically by moral pictures, this could represent a more general involvement of these regions in processing social and emotional stimuli, rather than processing related to morality per se. The first goal of the current study was to address this question by assessing brain activity while subjects viewed moral and non-moral pictures that were closely equated on emotional arousal and social content. Pictures were selected on the basis of unpleasant emotional content and were divided into those that did or did not contain moral violations, while ensuring that social content (e.g., faces, interpersonal interactions), did not differ across moral and non-moral pictures. We used subject and pilot ratings to confirm that moral pictures contained a significantly higher degree of moral content than non-moral pictures, but did not significantly differ from non-moral pictures on measures of emotional arousal or social complexity. We hypothesized that brain regions previously implicated in moral processing would be activated to a similar extent when viewing both moral and non-moral pictures. Specifically, we predicted MPFC activation in both moral and non-moral conditions, given the demonstrated involvement of this region in several types of social and emotional paradigms (see Ochsner et al., 2004b, Phan et al., 2002 for reviews). Whether other regions previously activated by moral tasks such as STS and posterior cingulate would also be activated in the non-moral condition was an open question.

The second goal of the study was to compare patterns of brain activation while individuals attempted to decrease their emotional responses to moral and non-moral pictures. Previous studies of emotion regulation have often used a strategy known as reappraisal, in which individuals attempt to decrease their emotional response to stimuli by reinterpreting an emotional stimulus in a manner that renders it less emotionally arousing (Gross, 2002, Jackson et al., 2000, Ochsner et al., 2002, Ochsner et al., 2004a). Three neuroimaging studies have assessed reappraisal-related brain activation (Beauregard et al., 2001, Ochsner et al., 2002, Ochsner et al., 2004a). All studies reported increased activation in prefrontal regions including the superior frontal gyrus (BA6/8) and anterior cingulate, and decreased activation in limbic regions that were active during the passive viewing of emotional stimuli, such as the amygdala. In the current study, we compared the neural correlates of two types of negative emotional stimuli, moral and non-moral pictures. Our prediction that regulating different types of emotion would engage differential patterns of brain activation was based on two main considerations. First, moral emotions engage patterns of brain activation that are not engaged by basic emotional processing (Greene et al., 2001, Greene et al., 2004, Moll et al., 2002a, Moll et al., 2002b, Heekeren et al., 2003, Heekeren et al., 2005), suggesting that the regulation of moral emotions also recruits different brain regions than those involved in basic emotion regulation. Second, although the regulation of different types of emotional responses has not been previously compared in a single study, evidence suggests that the regulation of different emotions recruits distinct brain regions. For example, Kalisch et al. (2005) found that decreasing anxiety related to the anticipation of a painful stimulus primarily activated a region of anterolateral cortex. In contrast, studies in which individuals decrease emotions associated with viewing unpleasant pictures have reported activation in other prefrontal regions, such as the superior frontal gyrus (Ochsner et al., 2002, Ochsner et al., 2004a). In addition, a recent study in our laboratory identified distinct neural correlates associated with the regulation of emotional responses to negative and positive pictures (Kim, 2004). Therefore, we expected that the regulation of moral and non-moral emotions would also engage different patterns of brain activation. However, given that emotion regulation for different types of negative emotions has not been previously compared in the same study, our hypotheses regarding the neural correlates of moral vs. non-moral emotion regulation were primarily exploratory in nature.

The primary experimental task used in the current study required subjects to view a series of pictures depicting negative emotional scenes that did or did not contain a moral violation. This aspect of the study emulated a previous study by Moll et al. (2002a), in which subjects also viewed negative moral and non-moral pictures. Similar to their design, we equated our moral and non-moral pictures on ratings of emotional arousal. In addition, we matched pictures on amount of social content as well as general complexity, to ensure that moral content was the only aspect that differed between moral and non-moral pictures. Based on this additional matching, we predicted that both types of stimuli would elicit similar activations in brain regions specifically associated with moral processing in Moll et al., such as the MPFC. For the regulation task, we used a task similar to the one used by Ochsner et al. (2002). While viewing moral and non-moral pictures, subjects were instructed either to view the pictures and allow themselves to experience whatever thoughts or feelings each picture evoked, or to attempt to reinterpret the picture in a manner such that they felt less of an emotional response. We predicted that the act of attempting to decrease emotional responses for moral and non-moral stimuli would elicit activity in reappraisal-related regions reported in previous studies (Ochsner et al., 2002, Ochsner et al., 2004a, Beauregard et al., 2001), and that morally relevant stimuli would engage additional processing in regions associated with resolving moral emotions. We also predicted diminished limbic activation during regulation, reflecting the success of regulation processes in diminishing emotional responses. Subjects were not informed during scanning that stimuli were grouped according to the presence or absence of moral violations, in an effort to avoid biasing their responses (a post-scan interview confirmed that subjects did not notice the moral/non-moral picture dichotomy).

Section snippets

Subjects

Ten healthy right-handed female adults free from any history of neurological or psychiatric impairment, and of similar education level, were recruited (age range 18–29 years). Only females were recruited because males and females have been suggested to differ substantially in how they process stimuli with moral salience (Jaffee and Hyde, 2000). Subjects provided written informed consent prior to the study, which was approved by the Emory University Institutional Review Board.

Picture stimuli

Two sets of color

Emotion regulation

All subjects met the criterion for successful regulation performance during the practice session. The post-scan questionnaire that asked subjects to indicate strategies they used during the regulation tasks while in the scanner found that all subjects except one used a strategy in accordance with the instruction to reinterpret the scenes to render the picture less emotionally arousing. More specifically, subjects reported accomplishing this by pretending that the scenes were unreal (e.g.,

Discussion

The present study contrasted the neural correlates of passively viewing vs. actively decreasing emotional reactions to unpleasant pictures that either contained or did not contain moral violations. There were three primary results. First, as predicted, passively viewing moral and non-moral pictures resulted in common activations in several regions involved in social and emotional processing, including the amygdala and MPFC. Second, two regions of activation specific to viewing moral pictures

Conclusions

To our knowledge, this study is the first to compare the neural correlates of emotion regulation for different types of negative emotional stimuli and to examine the neural correlates of responses to morally salient stimuli while systematically controlling for potential stimulus confounds such as the degree of social and emotional content. We observed similar patterns of activation when individuals passively viewed moral and non-moral emotional pictures in brain regions including the amygdala

Acknowledgments

This research was supported in parts by a research grant from the Natural Sciences and Engineering Research Council of Canada (#253461) to C.L.H., and a pilot grant from the Biomedical Imaging Technology Center (Emory University School of Medicine/Georgia Tech College of Engineering).

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