Neural correlates of regulating negative emotions related to moral violations

“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, 20…”

“MPFC activation has also been associated with theory of mind tasks (Frith, 2001), and tasks involving self-referential judgments (Kelley et al., 2002).”

“…affective responses is increased activation within the PFC and decreased activation in the amygdala (Beauregard, Levesque, & Bourgouin, 2001; Harenski & Hamann, 2006; Schaefer et al., 2002), suggesting that PFC projections to the amygdala exert an inhibitory top-down influence (Banks, Eddy,…”

“…of which isolated quite similar processes (e.g., by comparing reappraising a picture as less negative to both simply viewing a negative picture and to performing a simple cognitive task, e.g., Harenski and Hamann 2006), then including both of these contrasts would oversample highly dependent data.”

“…(Beauregard et al., 2001; Ochsner et al., 2002, 2004; Schaefer et al., 2002; Levesque et al., 2003, 2004; Kalisch et al., 2005; Phan et al., 2005; Harenski and Hamann, 2006; Ohira et al., 2006), a pattern suggesting that PFC projections to the amygdala exert a top-down, inhibitory influence.”

“Unfortunately, most studies that are designed to separate reactivity from regulation have used only women (Eippert et al., 2007; Goldin et al., 2008; Harenski & Hamann, 2006; Kim & Hamann, 2007; Ochsner et al., 2002, 2004) or did not compare men and women (Phan et al., 2005; Urry et al., 2006; van…”

“…in regions of the vmPFC (i.e., the subgenual ACC or immediately adjacent vmPFC region) similar to that observed in the present study (e.g., Harenski and Hamann, 2006; Kalisch et al., 2005b; Kim and Hamann, 2007; Ochsner et al., 2004a; Urry et al., 2006), supporting a general role for this…”

“A recent study reported that the neural correlates of down-regulating negative emotion differed depending on whether the stimuli depicted violations of moral rules, an effect that was observed even after arousal and other relevant stimulus factors had been equated ( Harenski & Hamann, 2006 ).”

“…is engaged in situations of effortful emotion regulation of highly aversive visual stimuli (e.g., mutilated bodies of humans and animals: Ochsner, Bunge, Gross, & Gabrieli, 2002; Ochsner et al., 2004) or socially complex ones (e.g., moral versus non-moral violations: Harenski & Hamann, 2006).”

“…identified a distributed network of brain regions underlying voluntary emotion regulation in response to affective images (Eippert et al., 2007; Harenski and Hamann, 2006; Ochsner et al., 2002, 2004; Ohira et al., 2006; Phan et al., 2005; Schaefer et al., 2002), film clips (Beauregard et al.,…”

“…been linked to the regulation of amygdala and other cortico-limbic activity (Phelps et al., 2004; Quirk et al., 2003) and varies with the direction of regulation (Eippert et al., 2007; Harenski and Hamann, 2006; McRae et al., 2010; Ochsner et al., 2002; Ohira et al., 2006; Schaefer et al., 2002).”

“…load, conflict, intention, consequences, and emotional regulation (Berthoz et al. 2002; Moll, de Oliveira-Souza, Bramati, et al. 2002; Moll, de Oliveira-Souza, Eslinger, et al. 2002; Heekeren et al. 2003; Greene et al. 2004; Heekeren et al. 2005; Harenski & Hamann 2006; Schaich Borg et al. 2006).”

“, amygdala) that encode and represent specific types of emotional information (Beauregard et al., 2001; Harenski and Hamann, 2006; Kalisch et al., 2005; Keightley et al., 2003; LeDoux, 2000; Levesque et al., 2003, 2004; Mathews et al., 2004; Ochsner et al., 2002, 2004b; Ohira et al., 2006; Phan et al., 2005; Schaefer…”

“…pictures were a subset of those used in Harenski and Hamann (2006) and were matched on emotional arousal and social complexity based on the ratings of three separate groups of healthy participants: a pilot study conducted by the first author, Harenski and Hamann (2006), and Harenski et al. (2010).”

“…instructed to passively view the art used in order to observe how individual differences influenced participants' spontaneous evaluations of and responses to the study stimuli (for a similar approach, see Harenski & Hamann, 2006; Hamann & Canli, 2004; Jackson et al., 2003; Ochsner et al., 2002).”

“Prior neuroimaging and neuropsychological evidence has suggested a role for the VMPC in evaluating harmful actions (Schaich Borg et al., 2006; Ciaramelli et al., 2007; Glenn et al., 2009; Greene et al., 2001, 2004; Harenski and Hamann, 2006; Heekeren et al., 2003; Koenigs et al., 2007; Luo et al., 2006; Mendez et al.,…”

“…assaults, war scenes) versus nonmoral scenes (e.g., body lesions, dangerous animals), matched along a number of dimensions including emotional salience (Moll, de Oliveira-Souza, Bramati, & Grafman, 2002) and social content (i.e., number of agents or interactions depicted) (Harenski & Hamaan, 2006).”

“…such as borderline personality disorer (BPD) (Gunderson, 2007; Meyer, Pilkonis, & Beevers, 2004), voidant personality disorder (AvPD) (Leising, Sporberg, & Rehbein, 006) or schizophrenia spectrum disorders (SSD) (Ballon, Kaur, arks, & Cadenhead, 2007; Meyer & Shean, 2006), among others.”

“Mostly using functional magnetic resonance imaging (fMRI), neuroimaging studies have implicated lateral ventral, ventromedial, dorsomedial, and dorsolateral regions of prefrontal cortex (PFC) when using reappraisal to decrease (Banks et al., 2007; 2001; Beauregard et al., 2001; Bechara, 2004; Eippert et al., 2007; Gol…”

“…2001; Roffman et al., 2005; Beauregard et al., 2001; Levesque et al., 2003; Phan et al., 2005; Schaefer et al., 2002; Mathews and MacLeod, 2005; Harenski and Hamann, 2006; Kalisch et al., 2006; Ohira et al., 2006; Urry et al., 2006), we hypothesized an elevated activity in prefrontal cortex…”

“Correspondence should be addressed to Kristin Prehn, Neuroscience Research Center, Berlin NeuroImaging Center & Charité University Medicine Berlin, Campus Mitte, Charitéplatz 1, 10117 Berlin, Germany, E-mail: kristin.prehn@charite.de or Hauke R. Heekeren, Max Planck Institute for Human Development, Lentzeallee 94, 141…”

“This not only applies for pen-and-paper versions but also for fMRI studies investigating the trolley dilemma (e.g., Greene et al., 2001; Harenski and Hamann, 2006).”

“…OFC when suppressing as compared to maintaining negative emotions as varied as anxiety resulting from the anticipation of shocks, sadness , and viewing aversive images (Harenski & Hamann, 2006; Kalisch et al., 2005; Kim & Hamann, 2007; Levesque et al., 2003; Ochsner, 2004; Phan et al., 2005).”

“…emotional regulation, justice vs. care-based judgments and interaction with theory of mind (Berthoz et al., 2002; Moll et al., 2002a,b; Heekeren et al., 2003; Greene et al., 2004; Heekeren et al., 2005; Borg et al., 2006; Harenski and Hamann, 2006; Robertson et al., 2007; Young et al., 2007).”

“…appliedablockeddesignwhereregulationcouldbeimplementedin a more sustained manner (as already used elsewhere, e.g., Harenski & Hamann, 2006; Phan et al., 2005) and was guided by controlled instructions (e.g., “pretend unreal” for the REAP strategy) for all stimulus…”

“…have begun investigating the neural basis of moral emotion and cognition (Greene et al., 2001, 2004; Moll et al., 2002a, 2002b; Heekeren et al., 2003, 2005; Harenski and Hamann, 2006; Schaich Borg et al., 2006), the neural basis of gender differences in moral processing has not been explored.”

“This region is one of the most consistently implicated regions in emotion regulation (Eippert et al., 2007; Harenski & Hamann, 2006; Herwig et al., 2007; Kim & Hamann, 2007; Ochsner et al., 2002; Ochsner et al., 2004; Phan et al., 2005), and although information on the role of this region in…”

“During emotion regulation, prefrontal control systems often modulate arousal of the amygdala, which detects emotionally significant stimuli (Beauregard, Levesque, & Bourgouin, 2001; Harenski & Hamann, 2006; Ochsner & Gross, 2005; Schaefer et al., 2002).”

“Notably, right IFG is critically involved in inhibitory processes during both cognitive [23] and emotional [24] conditions.”

“…Grezes, Armony, Passingham, & Dolan, 2006; Blair & Cipolotti, 2000; Cushman, Young, & Hauser, 2006; Damasio et al., 1990; Greene et al., 2004; Harenski & Hamann, 2006; Hauser, Cushman, Young, Jin, & Mikhail, 2006; Koenigs et al., 2007; Shamay-Tsoory, Tomer, Berger, Goldsher, & Aharon-Peretz,…”

“…a person violates a social norm or not, evokes increase in BOLD signal in pSTS (Greene et al., 2001; Berthoz et al., 2002; Moll et al., 2002; Heekeren et al., 2003; Greene et al., 2004; Heekeren et al., 2005; Moll et al., 2005; Borg et al., 2006; Harenski and Hamann, 2006; Prehn et al., 2008).”

“…between emotion-evoking regions such as the amygdala and its relation to other brain areas such as the prefrontal cortex (PFC), in the context of mediating change in affect regulation and in social behavior (Goldin et al. 2008; Harenski and Hamann 2006; Kanske et al. 2011; Ohira et al. 2006).”

“Moral judgments across these cases reflect a multitude of cognitive processes, including emotional responses to bad behavior and its effects (Harenski & Hamaan, 2006 ; Heekeren, Wartenburger, Schmidt, Schwintowski, & Villringer, 2003 ; Young et al, 2010 ), as well as representations of the agent's mind, including his…”

“…the amygdala, and the temporal pole, were not necessarily more active in moral (vs. nonmoral) conditions in some studies (e.g., Borg et al., 2006; Harenski & Hamann, 2006; Moll, de Oliveira-Souza, Bramati, & Grafman, 2002), contrary to results from other studies (e.g., Berthoz et al., 2006;…”

“Cognitive, Implicit, Distal, Other Robertson et al. (2007) 16 Moral > Neutral Ethical and non-ethical business problems were presented to participants.”

“, 2014), picture evaluation task with scenes with moral norm violations (Harenski and Hamann, 2006), norm violated behavior’s scenarios (Luo et al.”

“…medial prefrontal activity (BA 10) and post-scan emotional arousal ratings of moral pictures in participants who performed the implicit task. study (Harenski and Hamann, 2006), post-scan interviews indicated that the participants did not engage in moral deliberation, nor were they even aware of…”

“…location of lateral prefrontal regions that are recruited (Delgado et al., 2008; see also Ochsner and Gross, 2005); however, the regions we reported overlap with those previously linked with emotion regulation (Phan et al., 2005; Harenski and Hamann, 2006; Ohira et al., 2006; Kim and Hamann, 2007).”

“By revealing the engagement of areas such as the anterior cingulate cortex (ACC), ventromedial prefrontal cortex (VMPFC), posterior cingulate and posterior temporal cortex, and the anterior insula, these studies have highlighted the importance of domain-general functions for morality, including valuation, affective pr…”

“Regarding the moral salience aspect of the picture task used in this study, the task has been shown to reliably engage brain regions frequently implicated in moral judgment in non-clinical populations (Harenski and Hamann, 2006; Harenski et al., 2008, 2012).”

“…Hynes, Van Horn, Grafton, & Sinnott-Armstrong, 2006) and negative and positive moral emotions (Fourie, Thomas, Amodio, Warton, & Meintjes, 2014; Harenski & Hamann, 2006; Moll et al., 2005, 2007); researchers have also demonstrated the association between moral functioning and other…”

“…examining reappraisal of negative stimuli include mainly regions in the superior frontal gyrus (SFG), like the dorsolateral PFC (dlPFC; BA9/46) and the anterior cingulate cortex (ACC, BA32; Harenski and Hamann, 2006; Banks et al., 2007; Erk et al., 2010; Leiberg et al., 2012; Ochsner et al., 2012).”

“The present study utilizes a picture-viewing task with a modified design based on that used by Harenski and Hamann (2006).”

“…et al., 2010; Lane et al., 1997; Phillips et al., 1997; Schafer et al., 2005; Wicker et al., 2003) and emotion regulation (Eippert et al., 2007; Harenski and Hamann, 2006; Kober et al., 2010; Koenigsberg et al., 2010; McRae et al., 2010; Ochsner et al., 2002; Ohira et al., 2006; Schaefer et…”

“…vmPFC, posterior cingulate cortex, and cortex around the TPJ have reliably been implicated in studies of morality (Finger et al., 2006; Greene et al., 2001, 2004; Harenski & Hamann, 2006; Heekeren et al., 2003, 2005; Moll et al., 2002, 2005; Robertson et al., 2007; Schaich Borg et al., 2006, 2008).”

“Higher CD scores were associated with reduced hemodynamic responses in the ATC during judgments of morally-salient images.”

“Second, with respect to similar studies in adults, the moral dilemma paradigm has been associated with a consistent pattern of activations of the anterior medial prefrontal cortex, angular gyrus, and ventral posterior cingulate cortex [Greene and Haidt, 2002; Greene et al., 2001; Harenski and Hamann, 2006; Moll, et al…”

“regions identified by fMRI using emotion regulation tasks [12,23,42,43,44].”

“actions[12,13] or implicit associations[14]).”

“Consistently, Harenski and Hamann (2006) developed a task using pictures of real people to maximise feelings of actual involvement.”

“Several other functional neuroimaging studies in healthy individuals have since investigated moral judgments (Greene et al., 2001; Harenski and Hamann, 2006; Heekeren et al., 2003; Moll et al., 2002a, 2007, 2005, 2001) and moral reasoning (Borg et al., 2006; Greene et al., 2008, 2004), and have…”

“The inverse relationship between the vmPFC and the amygdala has been consistently reported in the literature (Phelps et al., 2004; Harenski and Hamann, 2006; Ohira et al., 2006; Urry et al., 2006).”

“, 2013) and is believed to underlie the affective component of moral judgments (Adolphs, 2009; Anderson et al., 1999; Decety et al., 2012; Greene, 2007; Harenski and Hamann, 2006; Koenigs et al., 2007; Moll and de Oliveira-Souza, 2007; Moll et al., 2002).”

“Furthermore, during some particular tasks in healthy subjects, other brain regions begin to activate in particular the anterior insula [43], the posterior superior temporal sulcus (pSTS) [54-56] the anterior cingulate gyrus [57] the inferior parietal lobes and the temporo-parietal junctions [19,20,54,58] the mesolimbi…”

“…through reappraisal led to increased activity in similar areas of the prefrontal cortex and decreased activity in limbic regions (Phan et al., 2005; see also Beauregard, Lévesque, & Bourgouin, 2001; Harenski & Hamann, 2006; Kalisch et al., 2005; Lévesque et al., 2003; Ohira et al., 2006).”

“Further, in a study by Harenski and Hamann (2006), both the SFG and cuneus were activated in the decreasemoral condition (i.e., to intentionally decrease emotional responses when viewing moral violation pictures) relative to baseline conditon.”

“Neuroimaging studies reported the modulations of frontoinsular sensorimotor networks during moral disgust (Moll et al., 2005; Harenski and Hamann, 2006; Schaich et al., 2008; Chapman and Anderson, 2013; Massau et al., 2017; Vicario et al., 2017a; Oaten et al., 2018; Ying et al., 2018).”