FMRI as a window into adolescents' experiences with peer rejection
By Carrie Masten
For many of us, it is easy to remember a time when we were rejected by peers during our childhood or adolescence. Whether we were chosen last in gym class, ridiculed by the ‘popular’ kids in high school, or discriminated against because of our race or gender, these memories often trigger unpleasant emotions and may even be painful to recall. Indeed, developmental research has shown that during adolescence in particular, it is common to spend increased time with peers, to place greater importance on peers’ approval and opinions, and to value peer group membership (Brown, 2004). However, once peer groups are formed, peer rejection becomes increasingly prevalent as ‘cliques’ form, and isolating and ridiculing classmates becomes associated with perceived popularity (Juvonen, Graham, & Schuster, 2003). In this social climate, the negative treatment of peers is likely to be highly anticipated due to its frequency and its potential impact on one’s social status. Thus, it is not surprising that peer rejection, whether it is experienced firsthand or just witnessed among one’s peers, has well documented links with psychopathology, including anxiety and depression, that can last long-term across development (Nishina & Juvonen, 2005; Prinstein & Aikins, 2004; Prinstein, Sheah, & Guyer, 2005; Rigby, 2003).
Despite these implications of both firsthand and observed rejection experiences for adolescents’ development and mental health, previous research has focused almost exclusively on firsthand experiences with peer rejection, using behavioral and self-report methods. The goal of my dissertation was to expand knowledge of peer rejection and related psychopathological outcomes during adolescence by implementing a translational program of research designed to examine both firsthand and observed rejection experiences using a combination of neuroimaging and behavioral techniques. Specifically, in a series of three studies I examined adolescents’ neural responses during both direct and observed experiences of peer rejection, as well as how these neural responses related to a series of self-, parent-, and observer-rated behavioral indices spanning traitlevel individual differences, state measures of reactivity, concurrent and longitudinal indicators of depressive symptomatology, and behavioral outcomes.
Study 1: Neural responses to firsthand peer rejection among adolescents
The goal of Study 1 was to establish the neural networks involved in adolescents’ firsthand experiences with peer rejection, and to examine how neural activity during these experiences related to adolescents’ subjective distress resulting from peer rejection experiences. Although peer relations research had clearly demonstrated negative outcomes related to peer rejection, and neuroimaging research with adults had revealed distinct neural networks involved in the experience of social exclusion (e.g., Eisenberger, Lieberman, & Williams, 2003), little was known about the neural networks involved in adolescents’ responses to peer rejection when I began this work. To begin to understand these neural processes, I performed a study in which 23 adolescents were ostensibly excluded by peers during an online ball tossing game called “Cyberball” (Williams et al., 2002; see figure 1), while they underwent an fMRI scan. During Cyberball, participants believe that they are playing with two other real adolescent players. These “players” first include the participant in the game, and then subsequently exclude the participant so that they are left out and excluded from the remainder of the game.
After the scan, participants selfreported the distress that they felt as a result of the exclusion experience. This allowed me to examine correlations between neural activity during exclusion and selfreported distress, in order to explore the neural regions involved in responding to and regulating the distress of peer rejection. Data from this study (Masten et al., 2009) has revealed new insights that help explain how adolescents may experience peer rejection in unique ways. For example, during exclusion adolescents displayed distress-related activity in the subgenual portion of the anterior cingulate (subACC)—a region that has been linked with both rejection sensitivity (Burklund et al., 2007) and depression (e.g., Saxena et al., 2003). In addition, adolescents’ regulatory processes during rejection were supported by the ventral prefrontal cortex (VPFC), which is commonly associated with emotion regulation in adults (e.g., Eisenberger et al., 2003), but also by the ventral striatum (VS). Although most often associated with reward-processing (Knutson & Cooper, 2005), the VS has also been linked with positive reappraisals in adults (Wager et al., 2008), decreases in risk-taking and susceptibility to peer influence in adolescence (Pfeifer et al., 2011), and emotion regulation in individuals with atypical prefrontal cortex functioning (e.g. Dickstein, & Leibenluft, 2006). Given that the prefrontal cortex is not fully developed until adulthood (Gogtay et al., 2004), the VS may help regulate adolescents’ affective responses to threatening stimuli during this period of development, and help compensate for an immature prefrontal cortex. In general, these types of discrepancies in regulatory processing may help explain why certain emotional experiences, like peer rejection, seem to have a developmental period in which they are particularly salient.
Study 2: Subgenual anterior cingulate responses to peer rejection: A marker of adolescents’ risk for depression
Given developmental literature linking peer rejection with depression disorders, the goal of my second dissertation study was to examine how adolescents’ neural responses during peer rejection relate to the development of depressive symptoms over time. Findings from Study 1 indicated that the subgenual anterior cingulate cortex (subACC) is a key region involved in adolescents’ distress responses during experiences with peer rejection. Of interest, this region has also been consistently implicated in studies examining the neural substrates of depression, suggesting a possible neural link between depression and responses to peer rejection that could help explain why peer rejection can lead to depressive disorders.
Thus, in Study 2 I used a subsample of 20 adolescents from Study 1 and examined whether heightened subACC activity in response to peer rejection related to increases in depressive symptoms across a one-year period. My findings demonstrated that adolescents displaying greater subACC activation in response to peer rejection were more likely to show elevated depressive symptom levels across the following year (Masten et al., 2011).
A key implication of these findings is that they demonstrate a potential biological mechanism linking peer rejection and depressive symptoms during adolescence and suggest that subACC responsiveness may serve as a potential ‘marker’ of adolescents’ risk for developing depression over time.
Study 3: Witnessing peer rejection during adolescence: Neural correlates of empathy for experiences of social exclusion
The goal of Study 3 was to explore the neural correlates of adolescents’ experiences witnessing peer rejection, as well as how these neural responses relate to adolescents’ trait empathy and behavioral responses toward the rejected victim. Recently, social psychologists have begun to investigate the neural basis of empathy during observed negative experiences (e.g., seeing someone experiencing physical pain). This work has shown that unique neural networks support the affective aspect of empathy in which individuals share the emotions of another, and the cognitive or ‘mentalizing’ aspect of empathy in which individuals try to understand another’s perspective (Decety & Meyer, 2008; Singer, 2006). These studies, however, have not examined how neural responses during empathic experiences relate to subsequent prosocial actions (e.g., helping the victim), and almost none of this work has focused on adolescents. Focusing on adolescents is particularly important in this case, since witnessing peer rejection is extremely common in adolescence and can cause adolescents as much anxiety as being rejected firsthand (Nishina & Juvonen, 2005).
I scanned a new sample of twenty adolescents while they observed another adolescent their age being ostensibly rejected in order to examine neural responses during observed exclusion. Participants selfreported their trait levels of empathy so that the relation between neural responses to observed peer rejection and individual differences in empathy could be explored. In addition, adolescents wrote emails to the ‘victim’ of the exclusion following the scan, which were later rated for prosocial behavior (i.e., efforts to be comforting/supportive toward the victim), so that neural responses during observed peer rejection could be related to actual prosocial actions following the rejection episode.
Findings indicated that adolescents showed heightened neural evidence of mentalizing (e.g., DMPFC and precuneus activation) when observing a peer’s rejection, and this was particularly true among adolescents who reported high levels of trait empathy (Masten et al., 2010). Of interest, however, adolescents displaying more affective/painrelated neural activity (i.e., anterior insula) during observed rejection were the ones who subsequently wrote more prosocial emails to the excluded victims. One possibility for why heightened pain responses, rather than empathy responses, might drive subsequent prosocial behaviors is that adolescents may observe peer rejection on a daily basis and consider it commonplace—they may even feel that their own peer status would be jeopardized if they were to interfere. As a result, adolescents’ empathic ability might have little bearing on their actions in these situations, and instead greater feelings of distress (e.g., as evidenced by greater activation in pain/affective regions) might drive their prosocial actions.
Conclusion and Future Directions
As a whole, my dissertation work examining the neural correlates of firsthand and ‘empathic’ peer rejection among adolescents has expanded scientific understanding of both the neural mechanisms underlying experiences with peer rejection— whether it is directly experienced or observed among one’s peers—and longitudinal links between neural responses to peer rejection and adolescents’ risk for depression. Since completing my dissertation, I have continued to build on this program of research. I have examined peer rejection processes in adolescents with Autism Spectrum Disorders, and I have looked at neural responses to peer rejection in relation to several longitudinal indicators of physical and cognitive development, including pubertal maturation and increasing empathic ability across the transition to adolescence. In addition, several of my other research projects focus on understanding peer rejection from an intergroup perspective. For example, how are our neural and behavioral responses to firsthand or observed exclusion affected when we believe we are being rejected specifically because of a particular group membership, such as our race or gender? Overall, my continuing goal is to examine social and intergroup relationship dynamics in adolescence using a variety of methodological techniques to explore how these social interactions change across development and within varying social contexts.
Brown, B. B. (2004). Adolescents’ relationships with peers. In R. Lerner & L. Steinberg (Eds.), Handbook of adolescent psychology, pp. 363-394. Hoboken, NJ: John Wiley & Sons, Inc.
Burklund, L.J., Eisenberger, N.I., & Lieberman, M.D. (2007). The face of rejection: Rejection sensitivity moderates dorsal anterior cingulate activity to disapproving facial expressions. Social Neuroscience, 2, 238-253.
Decety, J., & Meyer, M. (2008). From emotion resonance to empathic understanding: A social developmental neuroscience account. Development and Psychopathology, 20, 1053-1080.
Dickstein, D.P., & Leibenluft, E. (2006). Emotion regulation in children and adolescents: Boundaries between normalcy and bipolar disorder. Development and Psychopathology, 18, 1105-1131.
Eisenberger, N.L., Lieberman, M.D., & Williams, K.D. (2003). Does rejection hurt? An fMRI study of social exclusion. Science, 302, 290-292.
Gogtay, N., Giedd, J.N., Lusk, L., Hayashi, K.M., Greenstein, D., Vaituzis, A.C., Nugent, T.F., Herman, D.H., Clasen, L.S., Toga, A.W., Rapoport, J.L., & Thompson, P.M. (2004). Dynamic mapping of human cortical development during childhood through early adulthood. Proceedings of the National Academy of Sciences USA, 101, 8174-8179.
Juvonen, J., Graham, S., & Schuster, M.A. (2003). Bullying among young adolescents: the strong, the weak, and the troubled. Pediatrics, 112, 1231-1237.
Knutson, B., & Cooper, J.C. (2005). Functional magnetic resonance imaging of reward prediction. Current Opinions in Neurology, 18, 411- 417.
Masten, C.L., Eisenberger, N.I., Borofsky, L.A., McNealy, K., Pfeifer, J.H., & Dapretto, M. (2011). Subgenual anterior cingulate responses to peer rejection: A marker of adolescents’ risk for depression. Development and Psychopathology, 23, 283-292. Masten, C.L., Eisenberger, N.I., Borofsky, L.A., Pfeifer, J.H., McNealy, K.,
Mazziotta, J. & Dapretto, M. (2009). Neural correlates of social exclusion during adolescence: Understanding the distress of peer rejection. Social Cognitive and Affective Neuroscience, 4, 143-157.
Masten, C.L., Eisenberger, N.I., Pfeifer, J., & Dapretto, M. (2010). Witnessing peer rejection during adolescence: Neural correlates of empathy for experiences of social exclusion. Social Neuroscience, 5, 496-507.
Nishina, A., & Juvonen, J. (2005). Daily reports of witnessing and experiencing peer harassment in middle school. Child Development, 76, 435- 450.
Pfeifer, J.H., Masten, C.L., Moore, W.E., Oswald, T.M., Iacoboni, M., Mazziotta, J.C., & Dapretto, M. (2011). Entering adolescence: Resistance to peer influence, risky behavior, and neural changes in emotion reactivity. Neuron, 69, 1029 -1036.
Prinstein, M.J., & Aikins, J.W. (2004). Cognitive moderators of the longitudinal association between peer rejection and adolescent depressive symptoms. Journal of Abnormal Child Psychology, 32, 147-158.
Prinstein, M.J., Sheah, C.S., & Guyer, A.E. (2005). Peer victimization, cue interpretation, and internalizing symptoms: Preliminary concurrent and longitudinal findings for children and adolescents. Journal of Clinical Child and Adolescent Psychology, 34, 11-24.
Rigby, K. (2003). Consequences of bullying in schools. Canadian Journal of Psychiatry, 48, 583-590.
Saxena, S., Brody, A. L., Ho, M.L., Zohrabi, N., Maidment, K. M., & Baxter, L. R. (2003). Differential brain metabolic predictors of response to paroxe??ne in obsessivecompulsive disorder versus major depression. American Journal of Psychiatry, 160, 522-532.
Singer, T. (2006). The neuronal basis and ontogeny of empathy and mind reading: Review of literature and implications for future research. Neuroscience & Biobehavioral Reviews, 30, 855-863.
Wager, T.D., M.L, Davidson, B.L., Hughes, M.A., Lindquist, and Ochsner, K.N. (2008). Prefrontal- Subcortical Pathways Mediating Successful Emotion Regulation. Neuron, 59, 1037-1050.
Williams, K. D., Govan, C. L., Croker, V., Tynan, D., Cruickshank, M., & Lam, A. (2002). Investigations into differences between social- and cyberostracism. Group Dynamics: Theory Research, and Practice. Special Issue: Groups and Internet, 6, 65-77.