Abstract
Borderline Personality Disorder (BPD) is a disabling and difficult-to-treat mental disease. One of its core features is a significant difficulty in affect regulation, which is often accompanied by Non-Suicidal Self-Injury (NSSI). It is suggested that this type of behavior elicits positive emotions and mitigates emotional distress, and therefore can ultimately be reinforced and promoted. In spite of the high prevalence of NSSI behaviors (also in non-BPD samples), their role in modulating reward-related processes has not yet been investigated in BPD patients. In the present study, this lack of research was addressed. A large sample of BPD patients (N = 40), divided into two groups depending on the presence of NSSI, and a group of matched healthy controls underwent functional Magnetic Resonance Imaging (fMRI) while performing a gambling task. Patients who committed NSSI acts exhibited enhanced activation of the orbitofrontal cortex following an unexpected reward, when compared with controls and BPD patients with no NSSI behavior. In addition, the NSSI group showed diminished functional connectivity between the left orbitofrontal cortex and the right parahippocampal gyrus. These findings might suggest impaired ability to update reward associations of potential choices when both BPD and NSSI are present. We propose that the presence of NSSI involves alterations in the reward system independently of BPD, and thus can be considered as a possible phenotype for reward-related alterations.
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Andreou, C., Kleinert, J., Steinmann, S., Fuger, U., Leicht, G., & Mulert, C. (2015). Oscillatory responses to reward processing in borderline personality disorder. World Journal of Biological Psychiatry, 16, 1–12.
Ashburner, J. (2007). A fast diffeomorphic image registration algorithm. NeuroImage, 38, 95–113.
Ashburner, J., & Friston, K. J. (2005). Unified segmentation. NeuroImage, 26, 839–851.
Barrachina, J., Soler, J., Campins, M. J., Tejero, A., Pascual, J. C., Alvarez, E., et al. (2004). Validation of a Spanish version of the diagnostic interview for Bordelines-revised (DIB-R). Actas Españolas de Psiquiatría, 32, 293–298.
Berridge, K. C., & Kringelbach, M. L. (2008). Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology, 199, 457–480.
Bremner, J. D., Vythilingam, M., Vermetten, E., Nazeer, A., Adil, J., Khan, S., et al. (2002). Reduced volume of orbitofrontal cortex in major depression. Biological Psychiatry, 51, 273–279.
Bresin, K., & Gordon, K. H. (2013). Endogenous opioids and nonsuicidal self-injury: a mechanism of affect regulation. Neuroscience & Biobehavioral Reviews, 37, 374–383.
Buss, A. H., & Perry, M. (1992). The aggression questionnaire. Journal of Personality and Social Psychology, 63, 452–459.
Camara, E., Rodriguez-Fornells, A., & Münte, T. F. (2008). Functional connectivity of reward processing in the brain. Frontiers in Human Neuroscience, 2, 19.
Camara, E., Rodriguez-Fornells, A., Ye, Z., & Münte, T. F. (2009). Reward networks in the brain as captured by connectivity measures. Frontiers in Neuroscience, 3, 350–362.
Camara, E., Krämer, U. M., Cunillera, T., Marco-Pallarés, J., Cucurell, D., Nager, W., et al. (2010a). The effects of COMT (Val108/158Met) and DRD4 (SNP -521) dopamine genotypes on brain activations related to valence and magnitude of rewards. Cerebral Cortex, 20, 1985–1996.
Camara, E., Rodriguez-Fornells, A., & Münte, T. F. (2010b). Microstructural brain differences predict functional hemodynamic responses in a reward processing task. Journal of Neuroscience, 30, 11398–11402.
Crowell, S. E., Beauchaine, T. P., & Linehan, M. M. (2009). A biosocial developmental model of borderline personality: elaborating and extending Linehan’s theory. Psychological Bulletin, 135, 495–510.
Eichenbaum, H. (2000). A cortical-hippocampal system for declarative memory. Nature Reviews Neuroscience, 1, 41–50.
Enzi, B., Doering, S., Faber, C., Hinrichs, J., Bahmer, J., & Northoff, G. (2013). Reduced deactivation in reward circuitry and midline structures during emotion processing in borderline personality disorder. World Journal of Biological Psychiatry, 14, 45–56.
Friston, K. J., Buechel, C., Fink, G. R., Morris, J., Rolls, E., & Dolan, R. J. (1997). Psychophysiological and modulatory interactions in neuroimaging. NeuroImage, 6, 218–229.
Gehring, W. J., & Willoughby, A. R. (2002). The medial frontal cortex and the rapid processing of monetary gains and losses. Science, 295, 2279–2282.
Glenn, C. R., & Klonsky, E. D. (2009). Emotion dysregulation as a core feature of borderline personality disorder. Journal of Personality Disorders, 23, 20–28.
Gottfried, J. A. (2003). Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science, 301, 1104–1107.
Grant, J. E., Correia, S., Brennan-Krohn, T., Malloy, P. F., Laidlaw, D. H., & Schulz, S. C. (2007). Frontal white matter integrity in borderline personality disorder with self-injurious behavior. Journal of Neuropsychiatry and Clinical Neurosciences, 19, 383–390.
Jones, J. L., Esber, G. R., McDannald, M. A., Gruber, A. J., Hernandez, A., Mirenzi, A., & Schoenbaum, G. (2012). Orbitofrontal cortex supports behavior and learning using inferred but not cached values. Science, 338, 953–956.
Kleindienst, N., Bohus, M., Ludäscher, P., Limberger, M. F., Kuenkele, K., Ebner-Priemer, U. W., et al. (2008). Motives for nonsuicidal self-injury among women with borderline personality disorder. Journal of Nervous and Mental Disease, 196, 230–236.
Klonsky, E. D. (2007). The functions of deliberate self-injury: a review of the evidence. Clinical Psychology Review, 27, 226–239.
Klonsky, E. D., & Glenn, C. R. (2009). Assessing the functions of non-suicidal self-injury: psychometric properties of the inventory of statements about self-injury (ISAS). Journal of Psychopathology and Behavioral Assessment, 31, 215–219.
Koob, G. F., & Volkow, N. D. (2016). Neurobiology of addiction: a neurocircuitry analysis. Lancet Psychiatry, 3, 760–773.
Krause-Utz, A., Winter, D., Niedtfeld, I., & Schmahl, C. (2014). The latest neuroimaging findings in borderline personality disorder. Current Psychiatry Reports, 16, 438.
Lancaster, J. L., Woldorff, M. G., Parsons, L. M., Liotti, M., Freitas, C. S., Rainey, L., et al. (2000). Automated Talairach atlas labels for functional brain mapping. Human Brain Mapping, 10, 120–131.
Lieb, K., Zanarini, M. C., Schmahl, C., Linehan, M. M., & Bohus, M. (2004). Borderline personality disorder. The Lancet, 364, 453–461.
Lieberman, M. D., & Cunningham, W. A. (2009). Type I and type II error concerns in fMRI research: re-balancing the scale. Social Cognitive and Affective Neuroscience, 4, 423–428.
Linehan, M. M. (1993). Cognitive-behavioral treatment of borderline personality disorder. New York: Guilford Press.
Martínez-Molina, N., Mas-Herrero, E., Rodríguez-Fornells, A., Zatorre, R. J., & Marco-Pallarés, J. (2016). Neural correlates of specific musical anhedonia. Proceedings of the National Academy of Sciences, 113(46), E7337–E7345.
New, A. S., Hazlett, E. A., Newmark, R. E., Zhang, J., Triebwasser, J., Meyerson, D., et al. (2009). Laboratory induced aggression: a positron emission tomography study of aggressive individuals with borderline personality disorder. Biological Psychiatry, 66, 1107–1114.
Niedtfeld, I., Kirsch, P., Schulze, L., Herpertz, S. C., Bohus, M., & Schmahl, C. (2012). Functional connectivity of pain-mediated affect regulation in borderline personality disorder. PloS One, 7, e33293.
Nock, M. K. (2010). Self-Injury. Annual Review of Clinical Psychology, 6, 339–363.
Noonan, M. P., Mars, R. B., & Rushworth, M. F. S. (2011). Distinct roles of three frontal cortical areas in reward-guided behavior. Journal of Neuroscience, 31, 14399–14412.
Noonan, M. P., Kolling, N., Walton, M. E., & Rushworth, M. F. S. (2012). Re-evaluating the role of the orbitofrontal cortex in reward and reinforcement. European Journal of Neuroscience, 35, 997–1010.
Padrão, G., Mallorquí, A., Cucurell, D., Marco-Pallares, J., & Rodriguez-Fornells, A. (2013). Neurophysiological differences in reward processing in anhedonics. Cognitive, Affective & Behavioral Neuroscience, 13, 102–115.
Pascual, J. C., Martín-Blanco, A., Soler, J., Ferrer, A., Tiana, T., Alvarez, E., & Pérez, V. (2010). A naturalistic study of changes in pharmacological prescription for borderline personality disorder in clinical practice: from APA to NICE guidelines. International Clinical Psychopharmacology, 25, 349–355.
Patton, J. H., Stanford, M. S., & Barratt, E. S. (1995). Factor structure of the Barratt impulsiveness scale. Journal of Clinical Psychology, 51, 768–774.
Penley, J. A., Wiebe, J. S., & Nwosu, A. (2003). Psychometric properties of the Spanish Beck depression inventory-II in a medical sample. Psychological Assessment, 15, 569–577.
Perez, V., Barrachina, J., Soler, J., Pascual, J. C., Campins, M. J., Puigdemont, D., & Alvarez, E. (2007). The clinical global impression scale for borderline personality disorder patients (CGI-BPD): a scale sensible to detect changes. Actas Españolas de Psiquiatría, 35, 229–235.
Prossin, A. R., Love, T. M., Koeppe, R. A., Zubieta, J.-K., & Silk, K. R. (2010). Dysregulation of regional endogenous opioid function in borderline personality disorder. American Journal of Psychiatry, 167, 925–933.
Ramnani, N., Elliott, R., Athwal, B. S., & Passingham, R. E. (2004). Prediction error for free monetary reward in the human prefrontal cortex. NeuroImage, 23, 777–786.
Rankin, K. P., Salazar, A., Gorno-Tempini, M. L., Sollberger, M., Wilson, S. M., Pavlic, D., et al. (2009). Detecting sarcasm from paralinguistic cues: anatomic and cognitive correlates in neurodegenerative disease. NeuroImage, 47, 2005–2015.
Ripollés, P., Marco-Pallarés, J., Hielscher, U., Mestres-Missé, A., Tempelmann, C., Heinze, H.-J., et al. (2014). The role of reward in word learning and its implications for language acquisition. Current Biology, 24, 2606–2611.
Rudebeck, P. H., & Murray, E. A. (2014). The orbitofrontal oracle: cortical mechanisms for the prediction and evaluation of specific behavioral outcomes. Neuron, 84, 1143–1156.
Ruocco, A. C., Amirthavasagam, S., Choi-Kain, L. W., & McMain, S. F. (2013). Neural correlates of negative emotionality in borderline personality disorder: an activation-likelihood-estimation meta-analysis. Biological Psychiatry, 73, 153–160.
Sauder, C. L., Derbidge, C. M., & Beauchaine, T. P. (2015). Neural responses to monetary incentives among self-injuring adolescent girls. Development and Psychopathology, 28, 1–15.
Schuermann, B., Kathmann, N., Stiglmayr, C., Renneberg, B., & Endrass, T. (2011). Impaired decision making and feedback evaluation in borderline personality disorder. Psychological Medicine, 41, 1917–1927.
Schulze, L., Domes, G., Krüger, A., Berger, C., Fleischer, M., Prehn, K., et al. (2011). Neuronal correlates of cognitive reappraisal in borderline patients with affective instability. Biological Psychiatry, 69, 564–573.
Sebastian, A., Jung, P., Krause-Utz, A., Lieb, K., Schmahl, C., & Tüscher, O. (2014). Frontal dysfunctions of impulse control - a systematic review in borderline personality disorder and attention-deficit/hyperactivity disorder. Frontiers in Human Neuroscience, 8, 698.
Sescousse, G., Redouté, J., & Dreher, J.-C. (2010). The architecture of reward value coding in the human orbitofrontal cortex. Journal of Neuroscience, 30, 13095–13104.
Sescousse, G., Caldú, X., Segura, B., & Dreher, J.-C. (2013). Processing of primary and secondary rewards: a quantitative meta-analysis and review of human functional neuroimaging studies. Neuroscience and Biobehavioral Reviews, 37, 681–696.
Silbersweig, D., Clarkin, J. F., Goldstein, M., Kernberg, O. F., Tuescher, O., Levy, K. N., et al. (2007). Failure of Frontolimbic inhibitory function in the context of negative emotion in borderline personality disorder. American Journal of Psychiatry, 164, 1832–1841.
Skodol, A. E., Gunderson, J. G., Pfohl, B., Widiger, T. A., Livesley, W. J. J., & Siever, L. J. (2002). The borderline diagnosis I: psychopathology, comorbidity, and personaltity structure. Biological Psychiatry, 51, 936–950.
Soler, J., Vega, D., Feliu-Soler, A., Trujols, J., Soto, A., Elices, M., et al. (2013). Validation of the Spanish version of the borderline symptom list, short form (BSL-23). BMC Psychiatry, 13, 139.
Soloff, P. H., Meltzer, C. C., Becker, C., Greer, P. J., Kelly, T. M., & Constantine, D. (2003). Impulsivity and prefrontal hypometabolism in borderline personality disorder. Psychiatry Research, 123, 153–163.
Soloff, P. H., Pruitt, P., Sharma, M., Radwan, J., White, R., & Diwadkar, V. (2012). Structural brain abnormalities and suicidal behavior in borderline personality disorder. Journal of Psychiatric Research, 46, 516–525.
Stalnaker, T. A., Cooch, N. K., & Schoenbaum, G. (2015). What the orbitofrontal cortex does not do. Nature Neuroscience, 18, 620–627.
Stanley, B., & Siever, L. J. (2010). The interpersonal dimension of borderline personality disorder: toward a neuropeptide model. American Journal of Psychiatry, 167, 24–39.
Trull, T. J., Jahng, S., Tomko, R. L., Wood, P. K., & Sher, K. J. (2010). Revised NESARC personality disorder diagnoses: gender, prevalence, and comorbidity with substance dependence disorders. Journal of Personality Disorders, 24, 412–426.
Tzourio-Mazoyer, N., Landeau, B., Papathanassiou, D., Crivello, F., Etard, O., Delcroix, N., et al. (2002). Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage, 15, 273–289.
van Asselt, A. D. I., Dirksen, C. D., Arntz, A., & Severens, J. L. (2007). The cost of borderline personality disorder: societal cost of illness in BPD-patients. European Psychiatry, 22, 354–361.
van Zutphen, L., Siep, N., Jacob, G. a., Goebel, R., & Arntz, A. (2015). Emotional sensitivity, emotion regulation and impulsivity in borderline personality disorder: a critical review of fMRI studies. Neuroscience & Biobehavioral Reviews, 51, 64–76.
Vederman, A. C., Weisenbach, S. L., Rapport, L. J., Leon, H. M., Haase, B. D., Franti, L. M., et al. (2012). Modality-specific alterations in the perception of emotional stimuli in bipolar disorder compared to healthy controls and major depressive disorder. Cortex, 48, 1027–1034.
Vega, D., Soto, A., Amengual, J. L., Ribas, J., Torrubia, R., Rodríguez-Fornells, A., & Marco-Pallarés, J. (2013). Negative reward expectations in borderline personality disorder patients: neurophysiological evidence. Biological Psychology, 94, 388–396.
Vega, D., Vilà-Balló, A., Soto, À., Amengual, J., Ribas, J., Torrubia, R., et al. (2015). Preserved error-monitoring in borderline personality disorder patients with and without non-suicidal self-injury behaviors. PLOS ONE, 10(12), e0143994.
Volkow, N. D., & Fowler, J. S. (2000). Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex. Cerebral Cortex, 10, 318–325.
Völlm, B., Richardson, P., McKie, S., Elliott, R., Dolan, M., & Deakin, B. (2007). Neuronal correlates of reward and loss in cluster B personality disorders: a functional magnetic resonance imaging study. Psychiatry Research, 156, 151–167.
Westlund Schreiner, M., Klimes-Dougan, B., Begnel, E. D., & Cullen, K. R. (2015). Conceptualizing the neurobiology of non-suicidal self-injury from the perspective of the research domain criteria project. Neuroscience and Biobehavioral Reviews, 57, 381–391.
Wolf, R. C., Thomann, P. A., Sambataro, F., Vasic, N., Schmid, M., & Wolf, N. D. (2012). Orbitofrontal cortex and impulsivity in borderline personality disorder: an MRI study of baseline brain perfusion. European Archives of Psychiatry and Clinical Neuroscience, 262, 677–685.
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All procedures performed in this study were in accordance with the ethical standards of the institutional research committee and with the 1964 Helsinki declaration and its later amendments or comparable ethical standards. The study had been approved by the ethics committee of the Hospital de Bellvitge.
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This research was funded by the “Fundació La Marató de TV3” (2009–092410), the Spanish Ministry of Science to JMP (PSI2012–37472) and ARF (PSI2011–29219), and Catalan Government to ARF (2009 SGR 93). PR was supported by a FPU grant (AP2010–4179). This work was also supported by the Catalan Government (2009SGR211) and two Miguel Servet Research Contracts (CP07/00048 to RS and CP10/00596 to EP-C) from the Plan Nacional de I + D + I, and was co-funded by the Instituto de Salud Carlos III-Subdirección General de Evaluación y Fomento de la Investigación and the European Regional Development Fund (FEDER). The funders had no role in study design, data collection, analysis, decision to publish, or preparation of the manuscript.
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Vega, D., Ripollés, P., Soto, À. et al. Orbitofrontal overactivation in reward processing in borderline personality disorder: the role of non-suicidal self-injury. Brain Imaging and Behavior 12, 217–228 (2018). https://doi.org/10.1007/s11682-017-9687-x
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DOI: https://doi.org/10.1007/s11682-017-9687-x