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Rejection Distress Suppresses Medial Prefrontal Cortex in Borderline Personality Disorder

Published:December 02, 2022DOI:https://doi.org/10.1016/j.bpsc.2022.11.006

      Abstract

      Background

      Borderline personality disorder (BPD) is characterized by an elevated distress response to social exclusion (i.e., rejection distress), whose neural mechanisms remain unclear. fMRI studies of social exclusion have relied on the classic version of the Cyberball task, which is not optimized for fMRI. Our goal was to clarify the neural substrates of rejection distress in BPD using a modified version of Cyberball, which allowed us to dissociate the neural response to exclusion events from its modulation by exclusionary context.

      Methods

      Twenty-three women with BPD and 22 healthy controls completed a novel fMRI modification of Cyberball with five runs of varying exclusion probability and rated their rejection distress after each run. We tested group differences in the whole-brain response to exclusion events and in the parametric modulation of that response by rejection distress using mass univariate analysis.

      Results

      Although rejection distress was higher in participants with BPD, F(1,40)=5.25, p=0.027, η2=0.12, both groups showed similar neural responses to exclusion events. However, as rejection distress increased, the rostro-medial prefrontal cortex (rmPFC) response to exclusion events decreased in the BPD group but not in controls. Stronger modulation of the rmPFC response by rejection distress was associated with higher trait rejection expectation, r=-0.30, p=0.050.

      Conclusions

      Heightened rejection distress in BPD might stem from a failure to maintain or upregulate the activity of the rmPFC, a key node of the mentalization network. Inverse coupling between rejection distress and mentalization-related brain activity might contribute to heightened rejection expectation in BPD.

      Keywords

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      References

        • Maslow A.H.
        A theory of human motivation.
        Psychological Review. 1943; 50: 370-396
        • Taormina R.J.
        • Gao J.H.
        Maslow and the motivation hierarchy: measuring satisfaction of the needs.
        Am J Psychol. 2013; 126: 155-177
        • Kenrick D.T.
        • Griskevicius V.
        • Neuberg S.L.
        • Schaller M.
        Renovating the Pyramid of Needs: Contemporary Extensions Built Upon Ancient Foundations.
        Perspect Psychol Sci. 2010; 5: 292-314
      1. Pickett CL, Gardner WL (2005): The Social Monitoring System: Enhanced Sensitivity to Social Cues as an Adaptive Response to Social Exclusion. The social outcast: Ostracism, social exclusion, rejection, and bullying. New York, NY, US: Psychology Press, pp 213-226.

        • van Beest I.
        • Williams K.D.
        When inclusion costs and ostracism pays, ostracism still hurts.
        J Pers Soc Psychol. 2006; 91: 918-928
        • Fertuck E.A.
        • Fischer S.
        • Beeney J.
        Social Cognition and Borderline Personality Disorder: Splitting and Trust Impairment Findings.
        Psychiatr Clin North Am. 2018; 41: 613-632
        • Gunderson J.G.
        • Lyons-Ruth K.
        BPD's interpersonal hypersensitivity phenotype: a gene-environment-developmental model.
        J Pers Disord. 2008; 22: 22-41
        • Miano A.
        • Fertuck E.A.
        • Arntz A.
        • Stanley B.
        Rejection sensitivity is a mediator between borderline personality disorder features and facial trust appraisal.
        J Pers Disord. 2013; 27: 442-456
        • Staebler K.
        • Helbing E.
        • Rosenbach C.
        • Renneberg B.
        Rejection sensitivity and borderline personality disorder.
        Clin Psychol Psychother. 2011; 18: 275-283
        • Stanley B.
        • Siever L.J.
        The interpersonal dimension of borderline personality disorder: toward a neuropeptide model.
        Am J Psychiatry. 2010; 167: 24-39
        • Gutz L.
        • Renneberg B.
        • Roepke S.
        • Niedeggen M.
        Neural processing of social participation in borderline personality disorder and social anxiety disorder.
        Journal of abnormal psychology. 2015; 124: 421-431
        • Seidl E.
        • Padberg F.
        • Bauriedl-Schmidt C.
        • Albert A.
        • Daltrozzo T.
        • Hall J.
        • et al.
        Response to ostracism in patients with chronic depression, episodic depression and borderline personality disorder a study using Cyberball.
        J Affect Disord. 2020; 260: 254-262
        • Drapeau M.
        • Perry J.C.
        • Korner A.
        Interpersonal patterns in borderline personality disorder.
        J Pers Disord. 2012; 26: 583-592
        • Gunderson J.
        • Masland S.
        • Choi-Kain L.
        Good psychiatric management: a review.
        Curr Opin Psychol. 2018; 21: 127-131
        • Brodsky B.S.
        • Groves S.A.
        • Oquendo M.A.
        • Mann J.J.
        • Stanley B.
        Interpersonal precipitants and suicide attempts in borderline personality disorder.
        Suicide Life Threat Behav. 2006; 36: 313-322
        • Williams K.D.
        • Cheung C.K.
        • Choi W.
        Cyberostracism: effects of being ignored over the Internet.
        Journal of personality and social psychology. 2000; 79: 748
        • Eisenberger N.I.
        The neural bases of social pain: evidence for shared representations with physical pain.
        Psychosom Med. 2012; 74: 126-135
        • Somerville L.H.
        • Heatherton T.F.
        • Kelley W.M.
        Anterior cingulate cortex responds differentially to expectancy violation and social rejection.
        Nat Neurosci. 2006; 9: 1007-1008
        • Wang W.
        • Zhornitsky S.
        • Li C.S.
        • Zhang S.
        • Ide J.S.
        • Joormann J.
        • et al.
        Cerebral responses to self-initiated action during social interactions.
        Cogn Affect Behav Neurosci. 2019; 19: 1521-1535
        • Woo C.W.
        • Koban L.
        • Kross E.
        • Lindquist M.A.
        • Banich M.T.
        • Ruzic L.
        • et al.
        Separate neural representations for physical pain and social rejection.
        Nat Commun. 2014; 5: 5380
        • Brown R.C.
        • Plener P.L.
        • Groen G.
        • Neff D.
        • Bonenberger M.
        • Abler B.
        Differential Neural Processing of Social Exclusion and Inclusion in Adolescents with Non-Suicidal Self-Injury and Young Adults with Borderline Personality Disorder.
        Front Psychiatry. 2017; 8: 267
        • Domsalla M.
        • Koppe G.
        • Niedtfeld I.
        • Vollstadt-Klein S.
        • Schmahl C.
        • Bohus M.
        • et al.
        Cerebral processing of social rejection in patients with borderline personality disorder.
        Soc Cogn Affect Neurosci. 2014; 9: 1789-1797
        • Malejko K.
        • Neff D.
        • Brown R.C.
        • Plener P.L.
        • Bonenberger M.
        • Abler B.
        • et al.
        Neural Signatures of Social Inclusion in Borderline Personality Disorder Versus Non-suicidal Self-injury.
        Brain Topogr. 2019; 32: 753-761
        • Ruocco A.C.
        • Medaglia J.D.
        • Tinker J.R.
        • Ayaz H.
        • Forman E.M.
        • Newman C.F.
        • et al.
        Medial prefrontal cortex hyperactivation during social exclusion in borderline personality disorder.
        Psychiatry Res. 2010; 181: 233-236
        • Wrege J.S.
        • Ruocco A.C.
        • Euler S.
        • Preller K.H.
        • Busmann M.
        • Meya L.
        • et al.
        Negative affect moderates the effect of social rejection on frontal and anterior cingulate cortex activation in borderline personality disorder.
        Cogn Affect Behav Neurosci. 2019; 19: 1273-1285
        • Cacioppo S.
        • Frum C.
        • Asp E.
        • Weiss R.M.
        • Lewis J.W.
        • Cacioppo J.T.
        A quantitative meta-analysis of functional imaging studies of social rejection.
        Sci Rep. 2013; 3: 2027
        • Eisenberger N.I.
        • Lieberman M.D.
        • Williams K.D.
        Does rejection hurt? An FMRI study of social exclusion.
        Science. 2003; 302: 290-292
        • Mwilambwe-Tshilobo L.
        • Spreng R.N.
        Social exclusion reliably engages the default network: A meta-analysis of Cyberball.
        Neuroimage. 2021; 227117666
        • Vijayakumar N.
        • Cheng T.W.
        • Pfeifer J.H.
        Neural correlates of social exclusion across ages: A coordinate-based meta-analysis of functional MRI studies.
        Neuroimage. 2017; 153: 359-368
        • Malejko K.
        • Neff D.
        • Brown R.
        • Plener P.L.
        • Bonenberger M.
        • Abler B.
        • et al.
        Neural Correlates of Social Inclusion in Borderline Personality Disorder.
        Front Psychiatry. 2018; 9: 653
        • Caplan D.
        • Moo L.
        Cognitive conjunction and cognitive functions.
        Neuroimage. 2004; 21: 751-756
        • He B.J.
        Scale-free properties of the functional magnetic resonance imaging signal during rest and task.
        J Neurosci. 2011; 31: 13786-13795
        • Tong Y.
        • Hocke L.M.
        • Frederick B.B.
        Low Frequency Systemic Hemodynamic "Noise" in Resting State BOLD fMRI: Characteristics, Causes, Implications, Mitigation Strategies, and Applications.
        Front Neurosci. 2019; 13: 787
        • Spitzer R.L.
        • Williams J.B.
        • Gibbon M.
        • First M.B.
        The Structured Clinical Interview for DSM-III-R (SCID). I: History, rationale, and description.
        Arch Gen Psychiatry. 1992; 49: 624-629
      2. First MB, Gibbon M, Spitzer RL, Williams JB, Benjamin LS (2007): Structured Clinical Interview for DSM-IV Axis II Personality Disorders, Non-Patient Edition. Washington D.C.: American Psychiatric Press.

      3. Wechsler D (2008): Wechsler adult intelligence scale–Fourth Edition (WAIS–IV). San Antonio, TX: NCS Pearson. 22:816-827.

        • Downey G.
        • Feldman S.I.
        Implications of rejection sensitivity for intimate relationships.
        J Pers Soc Psychol. 1996; 70: 1327-1343
        • Zadro L.
        • Williams K.D.
        • Richardson R.
        How low can you go? Ostracism by a computer is sufficient to lower self-reported levels of belonging, control, self-esteem, and meaningful existence.
        Journal of Experimental Social Psychology. 2004; 40: 560-567
        • Nadis S.
        Neuroimaging: the sight of two brains talking.
        Nature. 2002; 416: 364
        • Grinband J.
        • Wager T.D.
        • Lindquist M.
        • Ferrera V.P.
        • Hirsch J.
        Detection of time-varying signals in event-related fMRI designs.
        Neuroimage. 2008; 43: 509-520
        • Fertuck E.A.
        • Grinband J.
        • Mann J.J.
        • Hirsch J.
        • Ochsner K.
        • Pilkonis P.
        • et al.
        Trustworthiness appraisal deficits in borderline personality disorder are associated with prefrontal cortex, not amygdala, impairment.
        Neuroimage Clin. 2019; 21101616
        • Grinband J.
        • Savitskaya J.
        • Wager T.D.
        • Teichert T.
        • Ferrera V.P.
        • Hirsch J.
        The dorsal medial frontal cortex is sensitive to time on task, not response conflict or error likelihood.
        Neuroimage. 2011; 57: 303-311
        • Grinband J.
        • Savitskaya J.
        • Wager T.D.
        • Teichert T.
        • Ferrera V.P.
        • Hirsch J.
        Conflict, error likelihood, and RT: Response to Brown & Yeung et al.
        Neuroimage. 2011; 57: 320-322
        • Yarkoni T.
        • Barch D.M.
        • Gray J.R.
        • Conturo T.E.
        • Braver T.S.
        BOLD correlates of trial-by-trial reaction time variability in gray and white matter: a multi-study fMRI analysis.
        PLoS One. 2009; 4e4257
        • Smallwood J.
        • Bernhardt B.C.
        • Leech R.
        • Bzdok D.
        • Jefferies E.
        • Margulies D.S.
        The default mode network in cognition: a topographical perspective.
        Nat Rev Neurosci. 2021; 22: 503-513
        • Moran J.M.
        • Kelley W.M.
        • Heatherton T.F.
        What Can the Organization of the Brain's Default Mode Network Tell us About Self-Knowledge?.
        Front Hum Neurosci. 2013; 7: 391
        • Waytz A.
        • Mitchell J.P.
        Two mechanisms for simulating other minds: Dissociations between mirroring and self-projection.
        Current Directions in Psychological Science. 2011; 20: 197-200
        • Schaafsma S.M.
        • Pfaff D.W.
        • Spunt R.P.
        • Adolphs R.
        Deconstructing and reconstructing theory of mind.
        Trends Cogn Sci. 2015; 19: 65-72
        • Nemeth N.
        • Matrai P.
        • Hegyi P.
        • Czeh B.
        • Czopf L.
        • Hussain A.
        • et al.
        Theory of mind disturbances in borderline personality disorder: A meta-analysis.
        Psychiatry Res. 2018; 270: 143-153
        • Fertuck E.A.
        • Grinband J.
        • Stanley B.
        Facial trust appraisal negatively biased in borderline personality disorder.
        Psychiatry Res. 2013; 207: 195-202
        • Knowles M.L.
        Social rejection increases perspective taking.
        Journal of Experimental Social Psychology. 2014; 55: 126-132
        • Maner J.K.
        • DeWall C.N.
        • Baumeister R.F.
        • Schaller M.
        Does social exclusion motivate interpersonal reconnection? Resolving the "porcupine problem.
        J Pers Soc Psychol. 2007; 92: 42-55
        • Carter‐Sowell A.R.
        • Chen Z.
        • Williams K.D.
        Ostracism increases social susceptibility.
        Social Influence. 2008; 3: 143-153
        • Jamieson J.P.
        • Harkins S.G.
        • Williams K.D.
        Need threat can motivate performance after ostracism.
        Pers Soc Psychol Bull. 2010; 36: 690-702
        • Mead N.L.
        • Baumeister R.F.
        • Stillman T.F.
        • Rawn C.D.
        • Vohs K.D.
        Social Exclusion Causes People to Spend and Consume Strategically in the Service of Affiliation.
        Journal of Consumer Research. 2011; 37: 902-919
        • Romero-Canyas R.
        • Downey G.
        • Reddy K.S.
        • Rodriguez S.
        • Cavanaugh T.J.
        • Pelayo R.
        Paying to belong: when does rejection trigger ingratiation?.
        J Pers Soc Psychol. 2010; 99: 802-823
        • White L.O.
        • Klein A.M.
        • von Klitzing K.
        • Graneist A.
        • Otto Y.
        • Hill J.
        • et al.
        Putting Ostracism into Perspective: Young Children Tell More Mentalistic Stories after Exclusion, But Not When Anxious.
        Front Psychol. 2016; 7: 1926
        • Luyten P.
        • Campbell C.
        • Allison E.
        • Fonagy P.
        The Mentalizing Approach to Psychopathology: State of the Art and Future Directions.
        Annu Rev Clin Psychol. 2020; 16: 297-325
        • Luyten P.
        • Fonagy P.
        The neurobiology of mentalizing.
        Personal Disord. 2015; 6: 366-379
      4. Bateman A, Fonagy P (2004): Psychotherapy for borderline personality disorder : mentalization-based treatment. Oxford ; New York: Oxford University Press.

        • Fonagy P.
        • Luyten P.
        • Bateman A.
        Translation: Mentalizing as treatment target in borderline personality disorder.
        Personal Disord. 2015; 6: 380-392
      5. Luyten P, Malcorps S, Fonagy P, Ensink K (2019): Assessment of mentalizing. Handbook of mentalizing in mental health practice.37-62.

        • Grinband J.
        • Steffener J.
        • Razlighi Q.R.
        • Stern Y.
        BOLD neurovascular coupling does not change significantly with normal aging.
        Hum Brain Mapp. 2017; 38: 3538-3551