Elsevier

NeuroImage

Volume 59, Issue 1, 2 January 2012, Pages 708-717
NeuroImage

Social exclusion and punishment of excluders: Neural correlates and developmental trajectories

https://doi.org/10.1016/j.neuroimage.2011.07.028Get rights and content

Abstract

Social exclusion is a distressing experience and can result in a reduction of prosocial behavior. In this fMRI study we examined the neural networks involved in social exclusion and subsequent fairness considerations across adolescent development. Participants from 3 age groups (10–12, 14–16 and 19–21 year olds) participated in the study and performed two tasks; first, participants played Cyberball to induce feelings of social inclusion and exclusion, followed by a Dictator game in which participants were asked to divide coins between themselves and the players who previously included or excluded them. Results revealed a network of regions associated with social exclusion, which involve the medial prefrontal cortex (mPFC)/ventral anterior cingulate cortex (vACC), subgenual ACC and the lateral PFC, as well as the insula and the dorsal ACC. Although social exclusion generated strong distress for all age groups, 10–12 year olds showed increased activity in the subgenual ACC in the exclusion game, which has been associated in previous studies with negative affective processing. Results of the Dictator game revealed that all age groups selectively punished the excluders by making lower offers. These offers were associated with activation in the temporoparietal junction (TPJ), superior temporal sulcus (STS) and the lateral PFC. Age comparisons revealed that adults showed additional activity in the insula and dorsal ACC when making offers to the excluders. The results are discussed in the light of recent findings on neural networks involved in social exclusion and the development of social brain regions.

Highlights

► Single-trial rejection events elicited activity in a broad network of regions. ► Social exclusion elicited increased activity in the subgenual ACC in 10–12 year olds. ► Social exclusion clearly affected subsequent fairness considerations. ► Punishment of excluders was associated with activity in the TPJ, STS and the vlPFC. ► Adults showed activity in the insula and dACC when making offers to the excluders.

Introduction

Humans are strongly motivated to be included by others and to establish a sense of belonging. Indeed, social exclusion has been found to be highly distressing and to result in feelings of hurt (Baumeister and Leary, 1995, Eisenberger et al., 2003, Van Beest and Williams, 2006). The notion that social exclusion leads to strong negative feelings is further supported by neuroimaging studies which have shown that social exclusion elicits activity in brain regions involved in affective processing and physical pain (see Eisenberger and Lieberman, 2004).

Using Cyberball (Williams and Jarvis, 2006), a paradigm in which participants get ostracized by two other players during a ball-tossing game, it was shown that activation in the dorsal anterior cingulate cortex (dACC), a region involved in the experience of physical pain, correlates positively with self-reported distress during exclusion, whereas activation in the ventrolateral prefrontal cortex (vlPFC) correlates negatively with distress (Eisenberger et al., 2003). In subsequent studies, it was shown that a broader network of areas is engaged during social exclusion, including the insula, medial prefrontal cortex (mPFC), ventral ACC (vACC), subgenual ACC, and the posterior cingulate cortex (e.g., Bolling et al., 2011, DeWall et al., 2010, Kross et al., 2007, Lieberman and Eisenberger, 2009, Sebastian et al., 2011).

Given the strong need for social belonging, social exclusion is likely to influence subsequent behavior and coping. Indeed, behavioral studies have shown that social exclusion leads to an increase in reaffilitive behavior in new social encounters to enhance the opportunity for inclusion (Bernstein et al., 2008, Lakin et al., 2008). Further, studies reported a link between social exclusion and a reduction of prosocial behavior (Twenge et al., 2001, Twenge et al., 2007), and showed that behavioral responses are modulated by prior interactions; people are more willing to cooperate with others who previously included them and act less prosocially to people who excluded them (Hillebrandt et al., 2010, Maner et al., 2007). These findings indicate that humans have the need to regain a sense of control after being excluded and act less cooperative towards the excluders, which may reflect a desire to punish the excluders.

Prior neuroimaging studies have shown that fairness considerations in decision-making, as measured with a variety of economic games, are associated with activation in different neural networks (see Rilling and Sanfey, 2011). First, brain regions involved in social decision-making overlap with the (social) pain network, including the insula and dACC. In particular, these regions are believed to be responsive to social norm violations and to mediate aversive responses to inequity (Rilling and Sanfey, 2011, Sanfey et al., 2003). Second, brain regions are reported which are important for understanding the intentions of others, such as the temporoparietal junction (TPJ), and regions implicated in cognitive and emotional control, including regions of the PFC (Güroğlu et al., 2010, Sanfey et al., 2003, Van den Bos et al., 2011). Thus, it is to be expected that these networks are also involved in fairness considerations towards individuals who have previously excluded the participant. The first goal of this study was to identify the neural networks which are sensitive to social exclusion and subsequent punishment behavior.

While social exclusion is a significant social threat for all ages (Baumeister and Leary, 1995), adolescence is believed to be characterized by a heightened sensitivity to rejection by peers (e.g., Sebastian et al., 2010a). The transition into adolescence is marked by an increase in peer orientation, filling the need for peer acceptance (Steinberg and Morris, 2001). In addition, it has been suggested that adolescent changes in social orientation co-occur with structural and functional changes in the brain (e.g., Blakemore, 2008, Nelson et al., 2005). To date, only a handful of studies examined adolescents' neural responses to peer rejection (e.g., Gunther Moor et al., 2010, Masten et al., 2009, Sebastian et al., 2011). One study by Sebastian et al. (2011) demonstrated that activity in the vlPFC was higher in adults compared to adolescents during the exclusion game of Cyberball, suggesting that adults might be better able to regulate the negative feelings associated with exclusion. In another study using Cyberball in 12–13 year olds, Masten et al. (2009) showed that activity in the subgenual ACC corresponds with greater exclusion-related distress, whereas activity in the ventral striatum correlated negatively with distress; a pattern of neural activity suggested being unique to adolescents. Thus, prior studies have suggested that the neural mechanisms, which are responsive to social exclusion, differ between adolescents and adults, but the developmental time course remains poorly understood. The second goal of this study was therefore to extend these prior studies by testing the impact of social exclusion on brain activity across a broader age range, and to test whether adolescents and adults differ in the way they respond to negative peer interactions in a subsequent allocation game.

To achieve the goals of this study, participants performed two tasks in a fixed order in the MRI scanner. First, participants played Cyberball, which started with an inclusion game of fair play, followed by an exclusion game. Each game was played with two novel age-matched peers. The second task was designed to test whether fairness judgments would be modulated by previous encounters with those people who included or excluded the participants. Both tasks were administered in three age groups aiming to test for different phases across adolescent development: 10–12 year olds, 14–16 year olds and 19–21 year olds.

Characteristic for prior fMRI studies using Cyberball is that they used a block design, which provided an index of the overall exclusion experience and the overall inclusion experience. In the current study brain responses were distinguished for events on which participants did not receive the ball within the inclusion and the exclusion game (see also Crowley et al., 2010), and events on which participants received the ball. An advantage of this design is that it removes potential motor responses associated with playing the ball and that it enables us to test whether neural responses associated with ‘not receiving the ball’ would be sensitive to the context of the game. In particular, it has previously been suggested that the exclusion game may elicit a reaction of violated expectations of fair play, as well as exclusion-related distress (Eisenberger and Lieberman, 2004, Somerville et al., 2006, Somerville et al., 2010). We anticipated that rejection events in general would be associated with activity in brain regions involved in the affective processing of negative social events, such as the mPFC/vACC, subgenual ACC, and the vlPFC. These regions are also reported in Cyberball studies with alternating blocks of inclusion and exclusion, which have reduced the possibility of expectation violations (Bolling et al., 2011, Sebastian et al., 2011). Second, we hypothesized that the continuous experience of being excluded (exclusion game) would elicit stronger activity in the dACC and the insula; both regions are believed to be implicated in expectancy violations, pain processing and negative affect (e.g., Eisenberger and Lieberman, 2004, Etkin et al., 2011, Shackman et al., 2011, Somerville et al., 2006).

Cyberball was immediately followed by a Dictator game, in which participants were instructed to divide coins between themselves and the players of the inclusion game, players of the exclusion game and two novel players. Previous studies have shown that people tend to punish social norm violations (Singer et al., 2006) and are less willing to cooperate with people who have previously rejected them (Hillebrandt et al., 2010, Maner et al., 2007). Accordingly, we predicted that participants would select lower offers with higher self-gain to the players who previously excluded them and more fair offers to the players they encountered during fair play. Furthermore, we hypothesized that punishment of excluders would engage regions implicated in social-decision making, including the TPJ, dACC, insula and the lateral PFC (Rilling and Sanfey, 2011).

With regard to Cyberball, we predicted that social exclusion would result in feelings of hurt in all age groups (Sebastian et al., 2010a) that would be most pronounced in early adolescence, possibly related to the onset of puberty which is associated with a reorganization of the brain (e.g., Forbes and Dahl, 2010, Nelson et al., 2005). Further, we predicted that this increased sensitivity to peer rejection would be accompanied by increased activity in brain regions associated with the experience of negative affect (e.g., subgenual ACC: Masten et al., 2009), and/or less activation in brain regions involved in affect regulation (e.g., vlPFC: Sebastian et al., 2011, Sebastian et al., 2010b). With regard to the Dictator game we hypothesized that early adolescents would show a higher tendency to punish the excluders. This hypothesis comes from studies suggesting that with increasing age adolescents are better able to control their negative emotions related to exclusion (Sebastian et al., 2011), and to take into account the perspectives of others (e.g., Güroğlu et al., 2009, Van den Bos et al., 2010). In addition, there is evidence that brain regions involved in social-decision making, including the TPJ and regions of the PFC, show a protracted development, suggesting an increased involvement of these regions with advancing age (Van den Bos et al., 2011).

Section snippets

Participants

Fifty-three healthy, right-handed volunteers were included in the study. Data of two additional participants (10-year-old boy, 11-year-old girl) were excluded from the analyses due to excessive head movement (> 3 mm). To examine developmental changes in distinct phases of adolescent development, we recruited participants from three age groups: twenty-two 10–12 year olds (early adolescence; 15 female; mean age = 11.8, SD = .87), sixteen 14–16 year olds (mid adolescence; 8 female; mean age = 15.74, SD = .74)

Need satisfaction and mood

Self-report ratings were administered at three time-points; immediately following the inclusion game, the exclusion game and after the Dictator game. These ratings were analyzed using repeated-measures ANOVAs with condition (inclusion, exclusion, and post Dictator game) as within-subjects factor. Separate analyses for each of the four needs (belonging, control, self-esteem, and meaningful existence) resulted in main effects of condition for all needs, with lower need satisfaction after the

Neural activity during Cyberball across age groups

First, brain regions were examined that were recruited during Cyberball across ages. The first contrast compared brain activity for ‘not receiving the ball’ during the inclusion game relative to ‘receiving the ball’ during the inclusion game [no ball-inclusion game > ball-inclusion game]. Results revealed a network of regions, including the mPFC/vACC, subgenual ACC, bilateral inferior frontal gyrus (or vlPFC), and the left middle temporal gyrus. Interestingly, a largely overlapping network of

Neural activity during the Dictator game across age groups

First, brain regions were examined that were differentially sensitive to making an offer for the players who previously included (Team 1) or excluded the participants during Cyberball (Team 2). In the behavioral data, a team × offer type interaction was found; players of Team 2 received more 8–2 offers, whereas the player of Team 1 mostly received a fair split. The current fMRI analysis collapsed across different offer types for each team. The contrast that compared brain activity for Team 2 > Team

Discussion

The goal of this study was to identify the neural networks that are sensitive to social exclusion and subsequent fairness considerations, and to test for developmental differences. By administering a Dictator game following Cyberball, we were able to examine whether fairness judgments were modulated by previous encounters with those people who included or excluded the participants. Self-report ratings showed that all participants reported greater distress after exclusion, which sets the stage

Acknowledgments

The authors would like to acknowledge Carolien van Giessen, Cesco Willemse and Gert-Jan Lelieveld for assistance in recruitment of participants and assistance during testing. Further, we would like to thank Ilja van Beest and Chris de Jager for the use of their version of Cyberball. This work was supported by the Dutch Science Foundation [NWO-MaGW, grant number 400-07-066].

References (53)

  • C.L. Sebastian et al.

    Developmental influences on the neural bases of responses to social rejection: implications of social neuroscience for education

    NeuroImage

    (2011)
  • W. Van den Bos et al.

    Development of trust and reciprocity in adolescence

    Cogn. Dev.

    (2010)
  • T.M. Achenbach

    Manual for Child Behavior Checklist/4–18 and 1991 Profile

    (1991)
  • D.M. Amodio et al.

    Meeting of minds: the medial frontal cortex and social cognition

    Nat. Rev. Neurosci.

    (2006)
  • R.F. Baumeister et al.

    The need to belong: desire for interpersonal attachments as a fundamental human motivation

    Psychol. Bull.

    (1995)
  • M.J. Bernstein et al.

    Adaptive responses to social exclusion: social rejection improves detection of real and fake smiles

    Psychol. Sci.

    (2008)
  • S.J. Blakemore

    The social brain in adolescence

    Nat. Rev. Neurosci.

    (2008)
  • M.C. Brett et al.

    Region of interest analysis using an SPM toolbox

    NeuroImage

    (2002)
  • M.J. Crowley et al.

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

    Soc. Neurosci

    (2010)
  • C.N. DeWall et al.

    Acetaminophen reduces social pain: behavioral and neural evidence

    Psychol. Sci.

    (2010)
  • N.I. Eisenberger et al.

    Does rejection hurt? An fMRI study of social exclusion

    Science

    (2003)
  • E. Fehr et al.

    Altruistic punishment in humans

    Nature

    (2002)
  • B. Gunther Moor et al.

    Do you like me? Neural correlates of social evaluation and developmental trajectories

    Soc. Neurosci.

    (2010)
  • B. Güroğlu et al.

    Unfair? It depends: neural correlates of fairness in social context

    Soc. Cogn. Affect. Neurosci.

    (2010)
  • A.E. Guyer et al.

    Probing the neural correlates of anticipated peer evaluation in adolescence

    Child Dev.

    (2009)
  • H. Hillebrandt et al.

    Experimentally induced social exclusion influences behavior on trust games

    Cogn. Neurosci.

    (2010)
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