Brain Imaging and Behavior

, Volume 12, Issue 1, pp 217–228 | Cite as

Orbitofrontal overactivation in reward processing in borderline personality disorder: the role of non-suicidal self-injury

  • Daniel Vega
  • Pablo Ripollés
  • Àngel Soto
  • Rafael Torrubia
  • Joan Ribas
  • Jose Antonio Monreal
  • Juan Carlos Pascual
  • Raymond Salvador
  • Edith Pomarol-Clotet
  • Antoni Rodríguez-Fornells
  • Josep Marco-Pallarés
Original Research

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.

Keywords

Borderline personality disorder Non-suicidal self-injury Reward Neuroimaging Functional connectivity Gambling 

Notes

Compliance with ethical standards

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.

Funding

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.

Conflict of interest

The authors declare that they have no conflict of interest.

Informed consent

Informed consent was obtained from all individual participants included in the study.

Supplementary material

11682_2017_9687_MOESM1_ESM.doc (72 kb)
ESM 1 (DOC 71 kb)

References

  1. 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.CrossRefGoogle Scholar
  2. Ashburner, J. (2007). A fast diffeomorphic image registration algorithm. NeuroImage, 38, 95–113.CrossRefPubMedGoogle Scholar
  3. Ashburner, J., & Friston, K. J. (2005). Unified segmentation. NeuroImage, 26, 839–851.CrossRefPubMedGoogle Scholar
  4. 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.PubMedGoogle Scholar
  5. Berridge, K. C., & Kringelbach, M. L. (2008). Affective neuroscience of pleasure: reward in humans and animals. Psychopharmacology, 199, 457–480.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 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.CrossRefPubMedGoogle Scholar
  7. Bresin, K., & Gordon, K. H. (2013). Endogenous opioids and nonsuicidal self-injury: a mechanism of affect regulation. Neuroscience & Biobehavioral Reviews, 37, 374–383.CrossRefGoogle Scholar
  8. Buss, A. H., & Perry, M. (1992). The aggression questionnaire. Journal of Personality and Social Psychology, 63, 452–459.CrossRefPubMedGoogle Scholar
  9. Camara, E., Rodriguez-Fornells, A., & Münte, T. F. (2008). Functional connectivity of reward processing in the brain. Frontiers in Human Neuroscience, 2, 19.CrossRefPubMedGoogle Scholar
  10. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  11. 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.CrossRefPubMedGoogle Scholar
  12. 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.CrossRefPubMedGoogle Scholar
  13. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  14. Eichenbaum, H. (2000). A cortical-hippocampal system for declarative memory. Nature Reviews Neuroscience, 1, 41–50.CrossRefPubMedGoogle Scholar
  15. 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.CrossRefPubMedGoogle Scholar
  16. 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.CrossRefPubMedGoogle Scholar
  17. Gehring, W. J., & Willoughby, A. R. (2002). The medial frontal cortex and the rapid processing of monetary gains and losses. Science, 295, 2279–2282.CrossRefPubMedGoogle Scholar
  18. Glenn, C. R., & Klonsky, E. D. (2009). Emotion dysregulation as a core feature of borderline personality disorder. Journal of Personality Disorders, 23, 20–28.CrossRefPubMedGoogle Scholar
  19. Gottfried, J. A. (2003). Encoding predictive reward value in human amygdala and orbitofrontal cortex. Science, 301, 1104–1107.CrossRefPubMedGoogle Scholar
  20. 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.CrossRefPubMedGoogle Scholar
  21. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  22. 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.CrossRefPubMedGoogle Scholar
  23. Klonsky, E. D. (2007). The functions of deliberate self-injury: a review of the evidence. Clinical Psychology Review, 27, 226–239.CrossRefPubMedGoogle Scholar
  24. 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.CrossRefPubMedGoogle Scholar
  25. Koob, G. F., & Volkow, N. D. (2016). Neurobiology of addiction: a neurocircuitry analysis. Lancet Psychiatry, 3, 760–773.CrossRefPubMedGoogle Scholar
  26. Krause-Utz, A., Winter, D., Niedtfeld, I., & Schmahl, C. (2014). The latest neuroimaging findings in borderline personality disorder. Current Psychiatry Reports, 16, 438.CrossRefPubMedGoogle Scholar
  27. 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.CrossRefPubMedGoogle Scholar
  28. Lieb, K., Zanarini, M. C., Schmahl, C., Linehan, M. M., & Bohus, M. (2004). Borderline personality disorder. The Lancet, 364, 453–461.CrossRefGoogle Scholar
  29. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  30. Linehan, M. M. (1993). Cognitive-behavioral treatment of borderline personality disorder. New York: Guilford Press.Google Scholar
  31. 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.CrossRefGoogle Scholar
  32. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  33. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  34. Nock, M. K. (2010). Self-Injury. Annual Review of Clinical Psychology, 6, 339–363.CrossRefPubMedGoogle Scholar
  35. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  36. 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.CrossRefPubMedGoogle Scholar
  37. 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.CrossRefGoogle Scholar
  38. 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.CrossRefPubMedGoogle Scholar
  39. Patton, J. H., Stanford, M. S., & Barratt, E. S. (1995). Factor structure of the Barratt impulsiveness scale. Journal of Clinical Psychology, 51, 768–774.CrossRefPubMedGoogle Scholar
  40. 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.CrossRefPubMedGoogle Scholar
  41. 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.PubMedGoogle Scholar
  42. 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.CrossRefPubMedGoogle Scholar
  43. 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.CrossRefPubMedGoogle Scholar
  44. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 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.CrossRefPubMedGoogle Scholar
  46. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  47. 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.CrossRefPubMedGoogle Scholar
  48. 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.Google Scholar
  49. 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.CrossRefPubMedGoogle Scholar
  50. 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.CrossRefPubMedGoogle Scholar
  51. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 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.CrossRefPubMedGoogle Scholar
  53. 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.CrossRefPubMedGoogle Scholar
  54. 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.CrossRefPubMedGoogle Scholar
  55. 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.CrossRefPubMedGoogle Scholar
  56. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 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.CrossRefPubMedGoogle Scholar
  58. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  59. Stalnaker, T. A., Cooch, N. K., & Schoenbaum, G. (2015). What the orbitofrontal cortex does not do. Nature Neuroscience, 18, 620–627.CrossRefPubMedPubMedCentralGoogle Scholar
  60. Stanley, B., & Siever, L. J. (2010). The interpersonal dimension of borderline personality disorder: toward a neuropeptide model. American Journal of Psychiatry, 167, 24–39.CrossRefPubMedGoogle Scholar
  61. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 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.CrossRefPubMedGoogle Scholar
  63. 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.CrossRefPubMedGoogle Scholar
  64. 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.CrossRefGoogle Scholar
  65. 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.CrossRefPubMedGoogle Scholar
  66. 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.CrossRefPubMedGoogle Scholar
  67. 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.CrossRefPubMedPubMedCentralGoogle Scholar
  68. Volkow, N. D., & Fowler, J. S. (2000). Addiction, a disease of compulsion and drive: involvement of the orbitofrontal cortex. Cerebral Cortex, 10, 318–325.CrossRefPubMedGoogle Scholar
  69. 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.CrossRefPubMedGoogle Scholar
  70. 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.CrossRefPubMedGoogle Scholar
  71. 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.CrossRefPubMedGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2017

Authors and Affiliations

  • Daniel Vega
    • 1
    • 2
    • 3
  • Pablo Ripollés
    • 3
    • 4
  • Àngel Soto
    • 1
  • Rafael Torrubia
    • 2
  • Joan Ribas
    • 1
  • Jose Antonio Monreal
    • 5
    • 6
  • Juan Carlos Pascual
    • 6
    • 7
  • Raymond Salvador
    • 6
    • 8
  • Edith Pomarol-Clotet
    • 6
    • 8
  • Antoni Rodríguez-Fornells
    • 3
    • 4
    • 9
  • Josep Marco-Pallarés
    • 3
    • 4
  1. 1.Servei de Psiquiatria i Salut MentalHospital d’Igualada (Consorci Sanitari de l’Anoia) IgualadaBarcelonaSpain
  2. 2.Unitat de Psicologia Mèdica, Departament de Psiquiatria i Medicina Legal & Institut de NeurociènciesUniversitat Autònoma de BarcelonaBarcelonaSpain
  3. 3.Cognition and Brain Plasticity Group [Bellvitge Biomedical Research Institute- IDIBELL]L’Hospitalet de LlobregatBarcelonaSpain
  4. 4.Department of Cognition, Development and Educational Psychology, Campus BellvitgeUniversity of BarcelonaBarcelonaSpain
  5. 5.Corporación Sanitaria Parc Taulí, Servicio de Salud MentalBarcelonaSpain
  6. 6.Centro de Investigación Biomédica en Red de Salud Mental (CIBERSAM)BarcelonaSpain
  7. 7.Department of Psychiatry, Hospital de la Santa Creu i Sant Pau & Institut d’Investigació Biomèdica - Sant Pau (IIB-Sant Pau)Universitat Autònoma de BarcelonaBarcelonaSpain
  8. 8.FIDMAG, Germanes HospitalariesBarcelonaSpain
  9. 9.Catalan Institution for Research and Advanced Studies, ICREABarcelonaSpain

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