Elsevier

Psychiatry Research

Volume 268, October 2018, Pages 263-271
Psychiatry Research

Neural processing of social exclusion in individuals with psychopathic traits: Links to anger and aggression

https://doi.org/10.1016/j.psychres.2018.07.024Get rights and content

Highlights

  • We measured a neural index of elaborative processing during a Cyberball task.

  • Psychopathic traits were related to greater elaborative processing of ambiguous exclusion.

  • Psychopathic traits were related to less elaborative processing of social inclusion.

  • Elaborative processing interacted with psychopathic traits to predict anger and aggression.

  • Aberrant processing of exclusion may drive aggression in those with psychopathic traits.

Abstract

Psychopathy is a cluster of personality traits associated with high rates of aggression. While research on psychopathic traits largely focuses on neurobiological factors implicated in aggression, other research suggests that contextual factors, such as social exclusion, also contribute to promoting aggression. Yet, the relationships among psychopathic traits, neural processing of exclusion, and aggression remain unknown. A sample of 76 adolescents and young adults completed Cyberball, a task involving conditions of social inclusion, ambiguous exclusion, and unambiguous exclusion. During Cyberball, a slow wave (SW) event-related potential (an index of elaborative processing) and self-reported anger were measured. Additionally, acts of real-world aggression were assessed. Results indicated that as psychopathic traits increased, SW during ambiguous exclusion also increased, but SW during inclusion decreased. However, the combination of smaller SW during ambiguous exclusion and higher psychopathic traits predicted heightened anger following Cyberball and more frequent real-world aggression. This response to social exclusion among individuals with elevated psychopathic traits may represent an unreflective, reactive style that exacerbates anger and aggression in certain contexts. These data suggest that neurobiological dysfunction in elaborative processing is related to psychopathic traits, and social context comprises another important influence on the aggression of individuals with elevated psychopathic traits.

Introduction

Aggression is hostile, unfriendly behavior that often results in physical, social, and/or emotional harm. Aggressive acts entail not only tangible costs (e.g., financial; Corso et al., 2007, Waters et al., 2005), but also intangible costs (e.g., psychological; McCollister et al., 2010). A host of factors (e.g., personality traits, environmental conditions, neural dysfunction, genetics) are known to influence risk for engaging in aggression. One factor reliably linked to higher rates and severity of aggression is psychopathy (Hare and McPherson, 1984, Kruh et al., 2005, Murrie et al., 2004, Salekin et al., 1996, Serin and Amos, 1995), a disorder characterized by a set of traits including callousness, manipulativeness, and impulsivity. Longitudinal research shows that elevated psychopathic traits in adolescence predict aggression and violent crime in adulthood (Gretton et al., 2004). Therefore, psychopathy represents a key risk factor in the development and persistence of aggressive behavior. Although there is substantial evidence that individuals with elevated psychopathic traits are more aggressive, research is lacking regarding the contexts in which they behave aggressively.

Social exclusion, sometimes referred to as ostracism or peer rejection, is a particularly powerful context that can lead to negative affect, hostility, anger, and aggression (Lansford et al., 2010, Williams, 2001, Leary et al., 2006). In a series of longitudinal studies, Dodge et al. (2003) reported that for both boys and girls social exclusion by peers around age 6 was a strong predictor of aggressive behavior around age 8, particularly for those who were already above the median on aggression at age 6. Consistent with this finding, studies focused on adolescence show that social rejection can lead to negative affect (Sebastian et al., 2010) and aggression (Reijntjes et al., 2011). The experience of social exclusion unleashes a cascade of negative consequences that span cognitive (Buelow et al., 2015), emotional, and behavioral domains (e.g., self-regulation; Baumeister et al., 2005, Chester and DeWall, 2014; risky behavior; Peake et al., 2013, Svetieva et al., 2016). Unsurprisingly, exclusion also affects interpersonal functioning, such that individuals who have been excluded are less likely to engage in prosocial behavior (Twenge et al., 2007, Will et al., 2016, Moor et al., 2012) and are more likely to attribute hostile intent to others (DeWall et al., 2009a, Reijntjes et al., 2011). Thus, exclusion may heighten risk for aggression through multiple psychosocial avenues.

Social exclusion also impacts neurobiological processes, with evidence for altered perceptual and attentional processing of social cues following exclusion (Chester et al., 2014, Kawamoto et al., 2014, DeWall et al., 2009b). In a laboratory-induced form of social exclusion (i.e., the Cyberball task), the slow-wave (SW) event-related potential (ERP) is a widely studied and validated measure of cognitive-affective processing of this social context (Crowley et al., 2009, Crowley et al., 2010, White et al., 2012, Sreekrishnan et al., 2014, Baddam et al., 2016). Broadly, the SW, which is maximal at centroparietal sites and is evident from as early as 300 ms following stimulus presentation, indexes the extent to which individuals engage in elaborative processing, particularly of intrinsically motivating stimuli (Cuthbert et al., 2000, Hajcak et al., 2010, Ruchkin et al., 1992, Schupp et al., 2004). More specifically, in the Cyberball task, enhanced SW is related to experiences of heightened threat to basic needs (e.g., control, self-esteem) following exclusion (Crowley et al., 2010, Sreekrishnan et al., 2014). The SW responses to both unambiguous, clear slights (being continuously excluded by peers) and ambiguous slights (being subtly excluded in the context of overall inclusion) track cognitive-affective reactions to Cyberball (Crowley et al., 2010, Crowley et al., 2009). However, only a small number of studies examined how neural processing during exclusion relates to aggression (e.g., Chester et al., 2014, Eisenberger et al., 2007), and no studies used ERP for this purpose, despite the advantageousness of ERP for measuring how individuals process rapidly unfolding social interactions.

Moreover, no research has examined neural processing of social exclusion as it relates to psychopathic traits. There is some evidence that children with elevated psychopathic traits are at higher risk for experiencing exclusion in the first place (Waller et al., 2017) and that social exclusion mediates the relationship between psychopathic traits and later affiliation with antisocial peers (Kimonis et al., 2004). However, it is unclear if individuals with elevated psychopathic traits process the experience of exclusion differently from individuals with lower levels of these traits, and whether these potential variations in information processing are associated with engagement in real-world aggression. Exploring the relationships among psychopathic traits, neural processing of social exclusion, and aggression is especially important, as it is precisely the way in which psychopathic individuals process information that is implicated in their deviant behavior (Baskin-Sommers and Newman, 2012, Brennan et al., 2017, Blair, 2010).

To examine the relationships among psychopathic traits, social exclusion, and emotional-behavioral outcomes, we used a Cyberball social exclusion task paired with dense-array electroencephalography (EEG) in an at-risk sample of adolescents and young adults. The goals of the study were three-fold. First, we were interested in the relationship between psychopathic traits and neural responses to social exclusion, specifically the SW ERP. Based on research suggesting that neural responses to ambiguous and unambiguous social exclusion index overlapping yet separable cognitive-affective reactions to the Cyberball task (Crowley et al., 2009, van Noordt et al., 2015), we examined responses to both types of exclusion events. Second, the feeling of anger is a key aspect of the exclusion-aggression link (Chow et al., 2008, Zimmer-Gembeck et al., 2016); however, since not all individuals experience exclusion in the same way, we were interested in assessing for whom this relationship was strongest. Specifically, we examined whether the relationship between SW and anger following the Cyberball task varied depending on level of psychopathic traits. Finally, given the association between exclusion and aggression (Lansford et al., 2010, Leary et al., 2006), we also examined whether psychopathic traits moderated the relationship between SW and real-world aggression. Delineating the relationship between psychopathic traits and responses to social exclusion is crucial for shedding light on whether aberrant processing of social contexts underlies the aggression that renders psychopathy so impairing and destructive.

Section snippets

Participants

Participants were recruited from the New Haven community. A prescreen phone interview was completed to exclude individuals who self-reported a history of schizophrenia, bipolar disorder, or psychosis, not otherwise specified; a family history of psychosis; or a history of medical problems (e.g., uncorrectable auditory or visual deficits, head injury with loss of consciousness greater than 30 min) that may have impacted their comprehension of the materials or performance on the task. In the

Slow wave and psychopathic traits

SW amplitude was analyzed in a repeated measures general linear model (GLM) with trial type (favorable, microrejection, rejection) as a within-subjects categorical factor and YPI total score (mean-centered and standardized) as a between-subjects quantitative factor. Follow-up simple interaction contrasts, with favorable SW amplitude as the reference category, were used to yield the following comparisons: microrejection versus favorable and rejection versus favorable.

The trial type x

Discussion

This study was the first to examine associations between psychopathic traits and neural responses to social exclusion. We used high-density EEG while participants played the Cyberball task in order to assess SW ERP in response to being included and excluded, both ambiguously, during fair play, and unambiguously, during the subsequent exclusion block. Additionally, we explored whether psychopathic traits moderated the associations between task-related SW and anger, and between task-related SW

Declarations of interest

None

References (102)

  • W.G. Manning et al.

    Estimating log models: to transform or not to transform?

    J. Health Econ

    (2001)
  • E.A. Martin et al.

    An electrophysiological investigation of emotional abnormalities in groups at risk for schizophrenia-spectrum personality disorders

    Biol. Psychol.

    (2017)
  • K.E. McCollister et al.

    The cost of crime to society: New crime-specific estimates for policy and program evaluation

    Drug Alcohol Depend.

    (2010)
  • M.M. McDonald et al.

    Is ostracism a strong situation? The influence of personality in reactions to rejection

    J. Res. Pers.

    (2012)
  • S.J. Peake et al.

    Risk-taking and social exclusion in adolescence: neural mechanisms underlying peer influences on decision-making

    Neuroimage

    (2013)
  • D.S. Ruchkin et al.

    Distinctions and similarities among working memory processes: an event-related potential study

    Cogn. Brain Res.

    (1992)
  • C. Sebastian et al.

    Social brain development and the affective consequences of ostracism in adolescence

    Brain Cogn.

    (2010)
  • R.C. Serin et al.

    The role of psychopathy in the assessment of dangerousness

    Int. J. Law Psychiatry

    (1995)
  • J.T. Tedeschi et al.

    Limitations of laboratory paradigms for studying aggression

    Aggress. Violent Behav.

    (1996)
  • S.J.R. van Noordt et al.

    Social exclusion modulates event-related frontal theta and tracks ostracism distress in children

    Neuroimage

    (2015)
  • H.R. Waters et al.

    The costs of interpersonal violence—An international review

    Health Policy

    (2005)
  • B.M. Wilkowski et al.

    Tracking the evil eye: trait anger and selective attention within ambiguously hostile scenes

    J. Res. Pers.

    (2007)
  • G.J. Will et al.

    Neural correlates of retaliatory and prosocial reactions to social exclusion: associations with chronic peer rejection

    Dev. Cogn. Neurosci.

    (2016)
  • H. Andershed et al.

    Convergent validity of the youth psychopathic traits inventory (YPI): association with the psychopathy checklist: youth Version (PCL:YV)

    Assessment

    (2007)
  • H. Andershed et al.

    Understanding the abnormal by studying the normal

    Acta Psychiatr. Scand.

    (2002)
  • H. Andershed et al.

    Psychopathic traits in non-referred youths: a new assessment tool

  • C.A. Anderson et al.

    External validity of “trivial” experiments: the case of laboratory aggression

    Rev. Gen. Psychol.

    (1997)
  • C.A. Anderson et al.

    Human aggression

    Ann. Rev. Psychol.

    (2002)
  • S. Baddam et al.

    What they bring: baseline psychological distress differentially predicts neural response in social exclusion by children's friends and strangers in best friend dyads

    Soc. Cogn. Affect. Neurosci.

    (2016)
  • A.R. Baskin-Sommers et al.

    The intersectionality of sex, race, and psychopathology in predicting violent crimes

    Crim. Justice Behav.

    (2013)
  • A.R. Baskin-Sommers et al.

    Cognition–emotion interactions in psychopathy: implications for theory and practice

  • R.J.R. Blair

    Neuroimaging of psychopathy and antisocial behavior: a targeted review

    Curr. Psychiatry Rep.

    (2010)
  • R.F. Baumeister et al.

    Social exclusion impairs self-regulation

    J. Pers. Soc. Psychol

    (2005)
  • L. Berkowitz et al.

    Toward an understanding of the determinants of anger

    Emotion

    (2004)
  • R. Blackburn et al.

    Reactions of primary and secondary psychopaths to anger-evoking situations

    Br. J. Clin. Psychol.

    (1985)
  • J.E. Brown et al.

    Comparisons of tobit, linear, and poisson-gamma regression models: an application of time use data

    Sociol. Methods Res.

    (2011)
  • B.J. Bushman et al.

    Do people aggress to improve their mood? Catharsis beliefs, affect regulation opportunity, and aggressive responding

    J. Pers. Soc. Psychol

    (2001)
  • D.S. Chester et al.

    The interactive effect of social pain and executive functioning on aggression: an fMRI experiment

    Soc. Cogn. Affect. Neurosci.

    (2014)
  • P.S. Corso et al.

    Medical costs and productivity losses due to interpersonal and self-directed violence in the United States

    Am. J. Prev. Med.

    (2007)
  • M.J. Crowley et al.

    Exclusion and micro-rejection: event-related potential response predicts mitigated distress

    Neuroreport

    (2009)
  • M.J. Crowley et al.

    Social exclusion in middle childhood: rejection events, slow-wave neural activity, and ostracism distress

    Soc. Neurosci.

    (2010)
  • J.J. Curtin

    PhysBox: the psychophysiology toolbox. An open source toolbox for psychophysiological data reduction within EEGLab

  • C.N. DeWall et al.

    Social exclusion and early-stage interpersonal perception: selective attention to signs of acceptance

    J. Pers. Soc. Psychol.

    (2009)
  • C.N. DeWall et al.

    It's the thought that counts: the role of hostile cognition in shaping aggressive responses to social exclusion

    J. Pers. Soc. Psychol.

    (2009)
  • K.A. Dodge

    Social cognition and children's aggressive behaviors

    Child Dev

    (1980)
  • K.A. Dodge et al.

    Peer rejection and social information-processing factors in the development of aggressive behavior problems in children

    Child Dev.

    (2003)
  • K.A. Dodge et al.

    Biased decision-making processes in aggressive boys

    J. Abnorm. Psychol.

    (1981)
  • K.A. Dodge et al.

    Hostile attributional biases among aggressive boys are exacerbated under conditions of threats to the self

    Child Dev.

    (1987)
  • V. Dupéré et al.

    Affiliation to youth gangs during adolescence: the interaction between childhood psychopathic tendencies and neighborhood disadvantage

    J. Abnorm. Child Psychol.

    (2007)
  • S.M. Gillespie et al.

    Does affective theory of mind contribute to proactive aggression in boys with conduct problems and psychopathic tendencies?

    Child Psychiatry Hum. Dev.

    (2018)
  • Cited by (11)

    • Resisting aggression in social contexts: The influence of life-course persistent antisocial behavior on behavioral and neural responses to social feedback

      2022, NeuroImage: Clinical
      Citation Excerpt :

      This pattern also speaks to prior studies noting that a dimensional approach can provide a more sensitive index compared to a categorical approach of DSM diagnoses (Garvey et al., 2016). However, it should be noted that these associations between psychopathic traits and reactive aggression were small in size, and no longer significant when correcting for multiple testing, or when social feedback was added to the ANOVA model, signaling that future research is warranted to better understand how social context influences the link between psychopathy and aggression (Brennan et al., 2018; Van Baardewijk et al., 2009). In addition, the similarity in behavioral patterns between groups raises the question whether future studies should employ stronger social context manipulations that result in more pronounced differences between groups.

    • Psychopathy and neurodynamic brain functioning: A review of EEG research

      2019, Neuroscience and Biobehavioral Reviews
      Citation Excerpt :

      Tasks common for this ERP are wide ranging and can include, for example, oddball, repetition and recognition paradigms (e.g., old and new word lists), and emotional paradigms (e.g., auditory and visual emotional stimuli). Seventeen studies tested the LPP or SW in relation to psychopathic traits (Anderson and Stanford, 2012; Anderson et al., 2015; Baskin-Sommers et al., 2013; Brennan et al., 2018; Brislin et al., 2018; Carolan et al., 2014; Cheng et al., 2012; Decety et al., 2015; Eisenbarth et al., 2013; Howard and McCullagh, 2007; Jutai et al., 1987; Medina et al., 2016; Rothemund et al., 2012; Sadeh and Verona, 2012; van Dongen et al., 2018; Venables et al., 2015; Williamson et al., 1991). Four studies found an elevated LPP (Anderson and Stanford, 2012; Cheng et al., 2012; Jutai et al., 1987; Medina et al., 2016).

    • Social anxiety, posterior insula activation, and autonomic response during self-initiated action in a Cyberball game

      2019, Journal of Affective Disorders
      Citation Excerpt :

      Many studies have employed a Cyberball task (Eisenberger et al., 2003; Williams and Jarvis, 2006) to investigate the neural correlates of perceived social exclusion in healthy adults (Gonzalez et al., 2014; McIver et al., 2019; van der Meulen et al., 2017; Wasylyshyn et al., 2018) and in individuals with a neuropsychiatric condition (Brennan et al., 2018; Domsalla et al., 2013; Jankowski et al., 2018; Kumar et al., 2017; Malejko et al., 2018).

    View all citing articles on Scopus

    This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

    View full text