Abstract
Neural underpinnings of emotion dysregulation in borderline personality disorder (BPD) are characterized by limbic hyperactivity and disturbed prefrontal activity. It is unknown whether neural correlates of emotion regulation change after a psychotherapy which has the goal to improve emotion dysregulation in BPD, such as dialectical behavioral therapy (DBT). We investigated distraction as a main emotion regulation strategy before and after DBT in female patients with BPD. Thirty-one BPD patients were instructed to either passively view or memorize letters before being confronted with negative or neutral pictures in a distraction task during functional magnetic resonance imaging. This paradigm was applied before and after a 12-week residential DBT-based treatment program. We compared the DBT group to 15 BPD control patients, who continued their usual, non-DBT-based treatment or did not have any treatment, and 22 healthy participants. Behaviorally, BPD groups and healthy participants did not differ significantly with respect to alterations over time. On the neural level, BPD patients who received DBT-based treatment showed an activity decrease in the right inferior parietal lobe/supramarginal gyrus during distraction from negative rather than neutral stimuli when compared to both control groups. This decrease was correlated with improvement in self-reported borderline symptom severity. DBT responders exhibited decreased right perigenual anterior cingulate activity when viewing negative (rather than neutral) pictures. In conclusion, our findings reveal changes in neural activity associated with distraction during emotion processing after DBT in patients with BPD. These changes point to lower emotional susceptibility during distraction after BPD symptom improvement.
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References
Glenn CR, Klonsky ED (2009) Emotion dysregulation as a core feature of borderline personality disorder. J Personal Disord 23(1):20–28. doi:10.1521/pedi.2009.23.1.20
Schmahl C, Herpertz S, Bertsch K, Ende G, Flor H, Kirsch P, Lis S, Meyer-Lindenberg A, Rietschel M, Schneider M, Spanagel R, Treede R-D, Bohus M (2014) Mechanisms of disturbed emotion processing and social interaction in borderline personality disorder: state of knowledge and research agenda of the German Clinical Research Unit. Borderline Personal Disord Emot Dysregul 1(1):1–17. doi:10.1186/2051-6673-1-12
Wagner AW, Linehan MM (1999) Facial expression recognition ability among women with borderline personality disorder: implications for emotion regulation. J Personal Disord 13(4):329–344. doi:10.1521/pedi.1999.13.4.329
Lynch TR, Rosenthal MZ, Kosson DS, Cheavens JS, Lejuez CW, Blair RJ (2006) Heightened sensitivity to facial expressions of emotion in borderline personality disorder. Emotion 6(4):647–655. doi:10.1037/1528-3542.6.4.647
Santangelo P, Reinhard I, Mussgay L, Steil R, Sawitzki G, Klein C, Trull TJ, Bohus M, Ebner-Priemer UW (2014) Specificity of affective instability in patients with borderline personality disorder compared to posttraumatic stress disorder, bulimia nervosa, and healthy controls. J Abnorm Psychol 123(1):258–272. doi:10.1037/a0035619
Schulze L, Schmahl C, Niedtfeld I (2016) Neural correlates of disturbed emotion processing in borderline personality disorder: a multimodal meta-analysis. Biol Psychiatry 79(2):97–106. doi:10.1016/j.biopsych.2015.03.027
Ochsner KN, Silvers JA, Buhle JT (2012) Functional imaging studies of emotion regulation: a synthetic review and evolving model of the cognitive control of emotion. Ann NY Acad Sci 1251:E1–E24. doi:10.1111/j.1749-6632.2012.06751.x
Kohn N, Eickhoff SB, Scheller M, Laird AR, Fox PT, Habel U (2014) Neural network of cognitive emotion regulation—an ALE meta-analysis and MACM analysis. Neuroimage 87:345–355. doi:10.1016/j.neuroimage.2013.11.001
Koenigsberg HW, Siever LJ, Lee H, Pizzarello S, New AS, Goodman M, Cheng H, Flory J, Prohovnik I (2009) Neural correlates of emotion processing in borderline personality disorder. Psychiatry Res 172(3):192–199. doi:10.1016/j.pscychresns.2008.07.010
Minzenberg MJ, Fan J, New AS, Tang CY, Siever LJ (2007) Fronto-limbic dysfunction in response to facial emotion in borderline personality disorder: an event—related fMRI study. Psychiatry Res 155(3):231–243. doi:10.1016/j.pscychresns.2007.03.006
Schulze L, Domes G, Kruger A, Berger C, Fleischer M, Prehn K, Schmahl C, Grossmann A, Hauenstein K, Herpertz SC (2011) Neuronal correlates of cognitive reappraisal in borderline patients with affective instability. Biol Psychiatry 69(6):564–573. doi:10.1016/j.biopsych.2010.10.025
Goodman M, Carpenter D, Tang CY, Goldstein KE, Avedon J, Fernandez N, Mascitelli KA, Blair NJ, New AS, Triebwasser J, Siever LJ, Hazlett EA (2014) Dialectical behavior therapy alters emotion regulation and amygdala activity in patients with borderline personality disorder. J Psychiatry Res 57:108–116. doi:10.1016/j.jpsychires.2014.06.020
Schnell K, Herpertz SC (2007) Effects of dialectic-behavioral-therapy on the neural correlates of affective hyperarousal in borderline personality disorder. J Psychiatry Res 41(10):837–847. doi:10.1016/j.jpsychires.2006.08.011
Linehan MM (1993) Cognitive-behavioral treatment of borderline personality disorder. Guilford Press, New York
Linehan MM (1993) Skills training manual for treating borderline personality disorder. Guilford Press, New York
Bohus M (2004) Effectiveness of inpatient dialectical behavioral therapy for borderline personality disorder: a controlled trial. Behav Res Ther 42(5):487–499. doi:10.1016/s0005-7967(03)00174-8
Kliem S, Kroger C, Kosfelder J (2010) Dialectical behavior therapy for borderline personality disorder: a meta-analysis using mixed-effects modeling. J Consult Clin Psychol 78(6):936–951. doi:10.1037/a0021015
Stoffers JM, Vollm BA, Rucker G, Timmer A, Huband N, Lieb K (2012) Psychological therapies for people with borderline personality disorder. Cochrane Database Syst Rev 8:CD005652. doi:10.1002/14651858.CD005652.pub2
Thiruchselvam R, Blechert J, Sheppes G, Rydstrom A, Gross JJ (2011) The temporal dynamics of emotion regulation: an EEG study of distraction and reappraisal. Biol Psychol 87(1):84–92. doi:10.1016/j.biopsycho.2011.02.009
Schonfelder S, Kanske P, Heissler J, Wessa M (2013) Time course of emotion-related responding during distraction and reappraisal. Soc Cogn Affect Neurosci 9(9):1310–1319. doi:10.1093/scan/nst116
McRae K, Hughes B, Chopra S, Gabrieli JD, Gross JJ, Ochsner KN (2010) The neural bases of distraction and reappraisal. J Cogn Neurosci 22(2):248–262. doi:10.1162/jocn.2009.21243
Kanske P, Heissler J, Schonfelder S, Bongers A, Wessa M (2011) How to regulate emotion? Neural networks for reappraisal and distraction. Cereb Cortex 21(6):1379–1388. doi:10.1093/cercor/bhq216
Lieberman MD, Inagaki TK, Tabibnia G, Crockett MJ (2011) Subjective responses to emotional stimuli during labeling, reappraisal, and distraction. Emotion 11(3):468–480. doi:10.1037/a0023503
Sheppes G, Meiran N (2007) Better late than never? On the dynamics of online regulation of sadness using distraction and cognitive reappraisal. Personal Soc Psychol Bull 33(11):1518–1532. doi:10.1177/0146167207305537
Erk S, Kleczar A, Walter H (2007) Valence-specific regulation effects in a working memory task with emotional context. Neuroimage 37(2):623–632. doi:10.1016/j.neuroimage.2007.05.006
Dorfel D, Lamke JP, Hummel F, Wagner U, Erk S, Walter H (2014) Common and differential neural networks of emotion regulation by detachment, reinterpretation, distraction, and expressive suppression: a comparative fMRI investigation. Neuroimage. doi:10.1016/j.neuroimage.2014.06.051
Kellermann TS, Sternkopf MA, Schneider F, Habel U, Turetsky BI, Zilles K, Eickhoff SB (2011) Modulating the processing of emotional stimuli by cognitive demand. Soc Cogn Affect Neurosci 7(3):263–273. doi:10.1093/scan/nsq104
Krause-Utz A, Oei NY, Niedtfeld I, Bohus M, Spinhoven P, Schmahl C, Elzinga BM (2012) Influence of emotional distraction on working memory performance in borderline personality disorder. Psychol Med 42(10):2181–2192. doi:10.1017/S0033291712000153
Silbersweig D, Clarkin JF, Goldstein M, Kernberg OF, Tuescher O, Levy KN, Brendel G, Pan H, Beutel M, Pavony MT, Epstein J, Lenzenweger MF, Thomas KM, Posner MI, Stern E (2007) Failure of frontolimbic inhibitory function in the context of negative emotion in borderline personality disorder. Am J Psychiatry 164(12):1832–1841. doi:10.1176/appi.ajp.2007.06010126
Prehn K, Schulze L, Rossmann S, Berger C, Vohs K, Fleischer M, Hauenstein K, Keiper P, Domes G, Herpertz SC (2013) Effects of emotional stimuli on working memory processes in male criminal offenders with borderline and antisocial personality disorder. World J Biol Psychiatry 14(1):71–78. doi:10.3109/15622975.2011.584906
Wingenfeld K, Rullkoetter N, Mensebach C, Beblo T, Mertens M, Kreisel S, Toepper M, Driessen M, Woermann FG (2009) Neural correlates of the individual emotional Stroop in borderline personality disorder. Psychoneuroendocrinology 34(4):571–586. doi:10.1016/j.psyneuen.2008.10.024
Dolcos F, Wang L, Mather M (2014) Current research and emerging directions in emotion–cognition interactions. Front Integr Neurosci 8:83. doi:10.3389/fnint.2014.00083
Carretie L (2014) Exogenous (automatic) attention to emotional stimuli: a review. Cogn Affect Behav Neurosci 14(4):1228–1258. doi:10.3758/s13415-014-0270-2
Winter D, Krause-Utz A, Lis S, Chiu CD, Lanius RA, Schriner F, Bohus M, Schmahl C (2015) Dissociation in borderline personality disorder: disturbed cognitive and emotional inhibition and its neural correlates. Psychiatry Res 233(3):339–351. doi:10.1016/j.pscychresns.2015.05.018
Loranger AW (1999) International Personality Disorder Examination (IPDE): DSM-IV and ICD-10 modules. Psychological Assessment Resources, Odessa
Wittchen HU, Wunderlich U, Gruschwitz S (1997) SKID. Strukturiertes Klinisches Interview für DSM-IV Achse I. Hogrefe, Göttingen
Zanarini MC, Vujanovic AA, Parachini EA, Boulanger JL, Frankenburg FR, Hennen J (2003) Zanarini Rating Scale for Borderline Personality Disorder (ZAN-BPD): a continuous measure of DSM-IV borderline psychopathology. J Personal Disord 17(3):233–242. doi:10.1521/pedi.17.3.233.22147
Bohus M, Limberger MF, Frank U, Chapman AL, Kuhler T, Stieglitz RD (2007) Psychometric properties of the Borderline Symptom List (BSL). Psychopathology 40(2):126–132. doi:10.1159/000098493
Gratz KL, Roemer L (2004) Multidimensional assessment of emotion regulation and dysregulation: development, factor structure, and initial validation of the difficulties in emotion regulation scale. J Psychopathol Behav 26(1):41–54. doi:10.1007/s10862-008-9102-4
Bohus M, Haaf B, Stiglmayr C, Pohl U, Boehme R, Linehan MM (2000) Evaluation of inpatient dialectical-behavioral therapy for borderline personality disorder—a prospective study. Behav Res Ther 38(9):875–887. doi:10.1016/S0005-7967(99)00103-5
Bohus M, Wolf M (2009) Interaktives Fertigkeitentraining für Borderline-Störungen. Schattauer Verlag, Stuttgart
Kleindienst N, Limberger MF, Schmahl C, Steil R, Ebner-Priemer UW, Bohus M (2008) Do improvements after inpatient dialectial behavioral therapy persist in the long term? A naturalistic follow-up in patients with borderline personality disorder. J Nerv Ment Dis 196(11):847–851. doi:10.1097/NMD.0b013e31818b481d
Lang PJ, Bradley MM, Cuthbert BN (1997) International Affective Picture System (IAPS): technical manual and affective ratings. The Center for Research in Psychophysiology, University of Florida, Gainesville
Wessa M, Kanske P, Neumeister P, Bode K, Heissler J, Schönfelder S (2010) EmoPics: subjektive und psychophysiologische Evaluationen neuen Bildmaterials für die klinisch-bio-psychologische Forschung. Z Kl Psych Psychoth 39(Suppl. 1/11):77
Volman I, Toni I, Verhagen L, Roelofs K (2011) Endogenous testosterone modulates prefrontal–amygdala connectivity during social emotional behavior. Cereb Cortex 21(10):2282–2290. doi:10.1093/cercor/bhr001
Lieberman MD, Cunningham WA (2009) Type I and Type II error concerns in fMRI research: re-balancing the scale. Soc Cogn Affect Neurosci 4(4):423–428. doi:10.1093/scan/nsp052
Jacobson NS, Truax P (1991) Clinical significance: a statistical approach to defining meaningful change in psychotherapy research. J Consult Clin Psychol 59(1):12–19. doi:10.1037/0022-006X.59.1.12
Winecoff A, Clithero JA, Carter RM, Bergman SR, Wang L, Huettel SA (2013) Ventromedial prefrontal cortex encodes emotional value. J Neurosci 33(27):11032–11039. doi:10.1523/jneurosci.4317-12.2013
Ochsner KN, Ray RD, Cooper JC, Robertson ER, Chopra S, Gabrieli JD, Gross JJ (2004) For better or for worse: neural systems supporting the cognitive down- and up-regulation of negative emotion. Neuroimage 23(2):483–499. doi:10.1016/j.neuroimage.2004.06.030
Goldstein M, Brendel G, Tuescher O, Pan H, Epstein J, Beutel M, Yang Y, Thomas K, Levy K, Silverman M, Clarkin J, Posner M, Kernberg O, Stern E, Silbersweig D (2007) Neural substrates of the interaction of emotional stimulus processing and motor inhibitory control: an emotional linguistic go/no-go fMRI study. Neuroimage 36(3):1026–1040. doi:10.1016/j.neuroimage.2007.01.056
Carvajal F, Rubio S, Serrano JM, Rios-Lago M, Alvarez-Linera J, Pacheco L, Martin P (2013) Is a neutral expression also a neutral stimulus? A study with functional magnetic resonance. Exp Brain Res 228(4):467–479. doi:10.1007/s00221-013-3578-1
Radua J, Phillips ML, Russell T, Lawrence N, Marshall N, Kalidindi S, El-Hage W, McDonald C, Giampietro V, Brammer MJ, David AS, Surguladze SA (2010) Neural response to specific components of fearful faces in healthy and schizophrenic adults. Neuroimage 49(1):939–946. doi:10.1016/j.neuroimage.2009.08.030
Mitchell JP (2008) Activity in right temporo-parietal junction is not selective for theory-of-mind. Cereb Cortex 18(2):262–271. doi:10.1093/cercor/bhm051
Silani G, Lamm C, Ruff CC, Singer T (2013) Right supramarginal gyrus is crucial to overcome emotional egocentricity bias in social judgments. J Neurosci 33(39):15466–15476. doi:10.1523/jneurosci.1488-13.2013
Saxe R, Kanwisher N (2003) People thinking about thinking people. The role of the temporo-parietal junction in “theory of mind”. Neuroimage 19(4):1835–1842. doi:10.1016/S1053-8119(03)00230-1
Kurth F, Zilles K, Fox PT, Laird AR, Eickhoff SB (2010) A link between the systems: functional differentiation and integration within the human insula revealed by meta-analysis. Brain Struct Funct 214(5–6):519–534. doi:10.1007/s00429-010-0255-z
Touroutoglou A, Hollenbeck M, Dickerson BC, Feldman Barrett L (2012) Dissociable large-scale networks anchored in the right anterior insula subserve affective experience and attention. Neuroimage 60(4):1947–1958. doi:10.1016/j.neuroimage.2012.02.012
Craig AD (2009) How do you feel–now? The anterior insula and human awareness. Nat Rev Neurosci 10(1):59–70. doi:10.1038/nrn2555
Phillips M, Ladouceur C, Drevets W (2008) A neural model of voluntary and automatic emotion regulation: implications for understanding the pathophysiology and neurodevelopment of bipolar disorder. Mol Psychiatry 13(9):829–857. doi:10.1038/mp.2008.65
Thayer JF (2006) On the importance of inhibition: central and peripheral manifestations of nonlinear inhibitory processes in neural systems. Dose-Response 4(1):2–21. doi:10.2203/dose-response.004.01.002.Thayer
Thayer JF, Brosschot JF (2005) Psychosomatics and psychopathology: looking up and down from the brain. Psychoneuroendocrinology 30(10):1050–1058. doi:10.1016/j.psyneuen.2005.04.014
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We thank Indre Ciurlyte, Michael Rieß, Claudia Stief, and Miriam Weiß for their help with data collection and for supporting the MRI measurements. This work was funded by the German Research Foundation (C.S., SCHM 1526/8-2; S.C.H., HE 2660/7-2).
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The authors assert that all procedures contributing to this work comply with the ethical standard of the relevant national and institutional committees on human experimentation and with the Helsinki Declaration of 1975, as revised in 2008. The Research Ethics Board II of the University of Heidelberg, Germany, approved the study. All participants were informed about the study procedures and gave written informed consent (capacity assessed via clinical interview). We registered the study as clinical trial (DRKS-ID = DRKS00000778).
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Christian Schmahl and Sabine C. Herpertz have contributed equally to this work.
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Winter, D., Niedtfeld, I., Schmitt, R. et al. Neural correlates of distraction in borderline personality disorder before and after dialectical behavior therapy. Eur Arch Psychiatry Clin Neurosci 267, 51–62 (2017). https://doi.org/10.1007/s00406-016-0689-2
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DOI: https://doi.org/10.1007/s00406-016-0689-2