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Evidence for default mode network dysfunction in borderline personality disorder

Published online by Cambridge University Press:  28 August 2019

Salvatore Aguilar-Ortiz ,
Pilar Salgado-Pineda ,
Daniel Vega ,
Juan C. Pascual ,
Josep Marco-Pallarés ,
Joaquim Soler ,
Cristina Brunel ,
Ana Martin-Blanco ,
Angel Soto  and
Joan Ribas
...Show all authors
Salvatore Aguilar-Ortiz
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain Benito Menni Complex Assistencial en Salut Mental, Sant Boi de Llobregat, Barcelona, Spain Departament de Psiquiatria i Medicina Legal, PhD Programme, Doctorat en Psiquiatria, Universitat Autònoma de Barcelona (UAB), Barcelona, Spain
Pilar Salgado-Pineda
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM, Barcelona, Spain
Daniel Vega
Affiliation:
Servei de Psiquiatria i Salut Mental, Consorci Sanitari de l'Anoia, Igualada, Spain
Juan C. Pascual
Affiliation:
CIBERSAM, Barcelona, Spain Department of Psychiatry, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain
Josep Marco-Pallarés
Affiliation:
Faculty of Psychology, University of Barcelona, Bellvitge Hospital, Barcelona, Spain
Joaquim Soler
Affiliation:
CIBERSAM, Barcelona, Spain Department of Psychiatry, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain
Cristina Brunel
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain Benito Menni Complex Assistencial en Salut Mental, Sant Boi de Llobregat, Barcelona, Spain
Ana Martin-Blanco
Affiliation:
Department of Psychiatry, Hospital de la Santa Creu i Sant Pau, Barcelona, Spain
Angel Soto
Affiliation:
Servei de Psiquiatria i Salut Mental, Consorci Sanitari de l'Anoia, Igualada, Spain
Joan Ribas
Affiliation:
Servei de Psiquiatria i Salut Mental, Consorci Sanitari de l'Anoia, Igualada, Spain
Teresa Maristany
Affiliation:
Hospital Sant Joan de Déu, Esplugues de Llobregrat, Barcelona, Spain
Salvador Sarró
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM, Barcelona, Spain
Antoni Rodríguez-Fornells
Affiliation:
Faculty of Psychology, University of Barcelona, Bellvitge Hospital, Barcelona, Spain
Raymond Salvador
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM, Barcelona, Spain
Peter J. McKenna*
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM, Barcelona, Spain
Edith Pomarol-Clotet
Affiliation:
FIDMAG Germanes Hospitalàries Research Foundation, Barcelona, Spain CIBERSAM, Barcelona, Spain
*
Author for correspondence: Peter J. Mckenna, Email: [email protected]
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Abstract

Background

Although executive and other cognitive deficits have been found in patients with borderline personality disorder (BPD), whether these have brain functional correlates has been little studied. This study aimed to examine patterns of task-related activation and de-activation during the performance of a working memory task in patients with the disorder.

Methods

Sixty-seven DSM-IV BPD patients and 67 healthy controls underwent fMRI during the performance of the n-back task. Linear models were used to obtain maps of within-group activations and areas of differential activation between the groups.

Results

On corrected whole-brain analysis, there were no activation differences between the BPD patients and the healthy controls during the main 2-back v. baseline contrast, but reduced activation was seen in the precentral cortex bilaterally and the left inferior parietal cortex in the 2-back v. 1-back contrast. The patients showed failure of de-activation affecting the medial frontal cortex and the precuneus, plus in other areas. The changes did not appear to be attributable to previous history of depression, which was present in nearly half the sample.

Conclusions

In this study, there was some, though limited, evidence for lateral frontal hypoactivation in BPD during the performance of an executive task. BPD also appears to be associated with failure of de-activation in key regions of the default mode network.

Keywords

Borderline personality disorderdefault mode networkfunctional imagingneuroimaging
Type
Original Articles
Information
Psychological Medicine , Volume 50 , Issue 10 , July 2020 , pp. 1746 - 1754
Copyright
Copyright © Cambridge University Press 2019

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References

Baczkowski, BM, van Zutphen, L, Siep, N, Jacob, GA, Domes, G, Maier, S, Sprenger, A, Senft, A, Willenborg, B, Tüscher, O, Arntz, A and van de Ven, V (2017) Deficient amygdala–prefrontal intrinsic connectivity after effortful emotion regulation in borderline personality disorder. European Archives of Psychiatry and Clinical Neuroscience 267, 551–565.CrossRefGoogle ScholarPubMed
Barrachina, J, Soler, J, Campins, MJ, Tejero, A, Pascual, JC, Alvarez, E, Zanarini, MC, Pérez Sola, V (2004) Validation of a Spanish version of the Diagnostic Interview for Borderlines-Revised (DIB-R). Actas Españolas de Psiquiatría 32, 293–298.Google Scholar
Beblo, T, Saavedra, AS, Mensebach, C, Lange, W, Markowitsch, H-J, Rau, H, Woermann, FG and Driessen, M (2006) Deficits in visual functions and neuropsychological inconsistency in borderline personality disorder. Psychiatry Research 145, 127–135.CrossRefGoogle ScholarPubMed
Beckmann, CF, Jenkinson, M, Woolrich, MW, Behrens, TEJ, Flitney, DE, Devlin, JT and Smith, SM (2006) Applying FSL to the FIAC data: model-based and model-free analysis of voice and sentence repetition priming. Human Brain Mapping 27, 380–391.CrossRefGoogle ScholarPubMed
Boccia, M, Dacquino, C, Piccardi, L, Cordellieri, P, Guariglia, C, Ferlazzo, F, Ferracuti, S and Giannini, AM (2017) Neural foundation of human moral reasoning: an ALE meta-analysis about the role of personal perspective. Brain Imaging and Behavior 11, 278–292.CrossRefGoogle ScholarPubMed
Broyd, SJ, Demanuele, C, Debener, S, Helps, SK, James, CJ and Sonuga-Barke, EJS (2009) Default-mode brain dysfunction in mental disorders: a systematic review. Neuroscience and Biobehavioral Reviews 33, 279–296.CrossRefGoogle ScholarPubMed
Buckner, RL (2012) The serendipitous discovery of the brain's default network. NeuroImage 62, 1137–1145.CrossRefGoogle ScholarPubMed
Buckner, RL, Andrews-Hanna, JR and Schacter, DL (2008) The brain's default network. Annals of the New York Academy of Sciences 1124, 1–38.CrossRefGoogle ScholarPubMed
Dreher, J-C, Koch, P, Kohn, P, Apud, J, Weinberger, DR and Berman, KF (2012) Common and differential pathophysiological features accompany comparable cognitive impairments in medication-free patients with schizophrenia and in healthy aging subjects. Biological Psychiatry 71, 890–897.CrossRefGoogle ScholarPubMed
Drevets, WC (2000) Functional anatomical abnormalities in limbic and prefrontal cortical structures in major depression. Progress in Brain Research 126, 413–431.CrossRefGoogle ScholarPubMed
Fernández-Corcuera, P, Salvador, R, Monté, GC, Salvador Sarró, S, Goikolea, JM, Amann, B, Moro, N, Sans-Sansa, B, Ortiz-Gil, J, Vieta, E, Maristany, T, McKenna, PJ and Pomarol-Clotet, E (2013) Bipolar depressed patients show both failure to activate and failure to de-activate during performance of a working memory task. Journal of Affective Disorders 148, 170–178.CrossRefGoogle ScholarPubMed
First, MB (1999) Entrevista Clínica Estructurada para los Trastornos del Eje I del DSM-IV- SCID-I. Barcelona: Masson.Google Scholar
Gevins, A and Cutillo, B (1993) Spatiotemporal dynamics of component processes in human working memory. Electroencephalography and Clinical Neurophysiology 87, 128–143.CrossRefGoogle ScholarPubMed
Green, DM and Swets, J (1966) Signal Detection Theory and Psychophysics. New York: Krieger.Google Scholar
Grimm, S, Boesiger, P, Beck, J, Schuepbach, D, Bermpohl, F, Walter, M, Ernst, J, Hell, D, Boeker, H and Northoff, G (2009) Altered negative BOLD responses in the default-mode network during emotion processing in depressed subjects. Neuropsychopharmacology 34, 932–943.CrossRefGoogle ScholarPubMed
Gunderson, JG and Zanarini, MC (1987) Current overview of the borderline diagnosis. Journal of Clinical Psychiatry 48 Suppl, 5–14.Google ScholarPubMed
Gusnard, DA and Raichle, ME (2001) Searching for a baseline: functional imaging and the resting human brain. Nature reviews. Neuroscience 2, 685–694.CrossRefGoogle ScholarPubMed
Haaland, VØ, Esperaas, L and Landrø, NI (2009) Selective deficit in executive functioning among patients with borderline personality disorder. Psychological Medicine 39, 1733–1743.CrossRefGoogle ScholarPubMed
Hagenhoff, M, Franzen, N, Koppe, G, Baer, N, Scheibel, N, Sammer, G, Gallhofer, B and Lis, S (2013) Executive functions in borderline personality disorder. Psychiatry Research 210, 224–231.CrossRefGoogle ScholarPubMed
Holtmann, J, Herbort, MC, Wüstenberg, T, Soch, J, Richter, S, Walter, H, Roepke, S and Schott, BH (2013) Trait anxiety modulates fronto-limbic processing of emotional interference in borderline personality disorder. Frontiers in Human Neuroscience 7, 54.CrossRefGoogle ScholarPubMed
Jacob, G, Zvonik, K, Kamphausen, S, Sebastian, A, Maier, S, Philipsen, A, Tebartz van Elst, L, Lieb, K and Tüscher, O (2013) Emotional modulation of motor response inhibition in women with borderline personality disorder: an fMRI study. Journal of Psychiatry and Neuroscience 38, 164–172.CrossRefGoogle ScholarPubMed
Kennedy, DP and Courchesne, E (2008) Functional abnormalities of the default network during self- and other-reflection in autism. Social Cognitive and Affective Neuroscience 3, 177–190.CrossRefGoogle ScholarPubMed
Koenigsberg, HW, Anwunah, I, New, AS, Mitropoulou, V, Schopick, F and Siever, LJ (1999) Relationship between depression and borderline personality disorder. Depression and Anxiety 10, 158–167.3.0.CO;2-B>CrossRefGoogle ScholarPubMed
Krause-Utz, A, Oei, NYL, Niedtfeld, I, Bohus, M, Spinhoven, P, Schmahl, C and Elzinga, BM (2012) Influence of emotional distraction on working memory performance in borderline personality disorder. Psychological Medicine 42, 2181–2192.CrossRefGoogle ScholarPubMed
LeGris, J and van Reekum, R (2006) The neuropsychological correlates of borderline personality disorder and suicidal behaviour. Canadian Journal of Psychiatry 51, 131–142.CrossRefGoogle ScholarPubMed
Lei, X, Zhong, M, Liu, Y, Jin, X, Zhou, Q, Xi, C, Tan, C, Zhu, X, Yao, S and Yi, J (2017) A resting-state fMRI study in borderline personality disorder combining amplitude of low frequency fluctuation, regional homogeneity and seed based functional connectivity. Journal of Affective Disorders 218, 299–305.CrossRefGoogle ScholarPubMed
Leichsenring, F, Leibing, E, Kruse, J, New, AS and Leweke, F (2011) Borderline personality disorder. Lancet 377, 74–84.CrossRefGoogle ScholarPubMed
Lis, E, Greenfield, B, Henry, M, Guilé, JM and Dougherty, G (2007) Neuroimaging and genetics of borderline personality disorder: a review. Journal of Psychiatry and Neuroscience 32, 162–173.Google ScholarPubMed
Mannell, MV, Franco, AR, Calhoun, VD, Cañive, JM, Thoma, RJ and Mayer, AR (2010) Resting state and task-induced deactivation: a methodological comparison in patients with schizophrenia and healthy controls. Human Brain Mapping 31, 424–437.Google ScholarPubMed
Marchetti, I, Koster, EHW, Sonuga-Barke, EJ and De Raedt, R (2012) The default mode network and recurrent depression: a neurobiological model of cognitive risk factors. Neuropsychology Review 22, 229–251.CrossRefGoogle ScholarPubMed
Mensebach, C, Beblo, T, Driessen, M, Wingenfeld, K, Mertens, M, Rullkoetter, N, Lange, W, Markowitsch, HJ, Ollech, I, Saveedra, AS, Rau, H and Woermann, FG (2009) Neural correlates of episodic and semantic memory retrieval in borderline personality disorder: an fMRI study. Psychiatry Research 171, 94–105.CrossRefGoogle ScholarPubMed
Minzenberg, MJ, Fan, J, New, AS, Tang, CY and Siever, LJ (2007) Fronto-limbic dysfunction in response to facial emotion in borderline personality disorder: an event-related fMRI study. Psychiatry Research 155, 231–243.CrossRefGoogle ScholarPubMed
Murray, RJ, Schaer, M and Debbané, M (2012) Degrees of separation: a quantitative neuroimaging meta-analysis investigating self-specificity and shared neural activation between self- and other-reflection. Neuroscience and Biobehavioral Reviews 36, 1043–1059.CrossRefGoogle ScholarPubMed
Nickerson, LD, Smith, SM, Öngür, D and Beckmann, CF (2017) Using dual regression to investigate network shape and amplitude in functional connectivity analyses. Frontiers in Neuroscience 11, 115.CrossRefGoogle ScholarPubMed
Nunes, PM, Wenzel, A, Borges, KT, Porto, CR, Caminha, RM and de Oliveira, IR (2009) Volumes of the hippocampus and amygdala in patients with borderline personality disorder: a meta-analysis. Journal of Personality Disorders 23, 333–345.CrossRefGoogle ScholarPubMed
Owen, AM, McMillan, KM, Laird, AR and Bullmore, E (2005) N-back working memory paradigm: a meta-analysis of normative functional neuroimaging studies. Human Brain Mapping 25, 46–59.CrossRefGoogle ScholarPubMed
Pearse, LJ, Dibben, C, Ziauddeen, H, Denman, C and McKenna, PJ (2014) A study of psychotic symptoms in borderline personality disorder. The Journal of Nervous and Mental Disease 202, 368–371.CrossRefGoogle ScholarPubMed
Piccoli, T, Valente, G, Linden, DEJ, Re, M, Esposito, F, Sack, AT and Di Salle, F (2015) The default mode network and the working memory network are not anti-correlated during all phases of a working memory task. PLoS One 10, e0123354.CrossRefGoogle Scholar
Pomarol-Clotet, E, Salvador, R, Sarró, S, Gomar, J, Vila, F, Martínez, A, Guerrero, A, Ortiz-Gil, J, Sans-Sansa, B, Capdevila, A, Cebamanos, JM and McKenna, PJ (2008) Failure to deactivate in the prefrontal cortex in schizophrenia: dysfunction of the default mode network? Psychological Medicine 38, 1185–1193.CrossRefGoogle ScholarPubMed
Pomarol-Clotet, E, Moro, N, Sarró, S, Goikolea, JM, Vieta, E, Amann, B, Fernandez-Corcuera, P, Sans-Sansa, B, Monté, GC, Capdevila, A, McKenna, PJ and Salvador, R (2012) Failure of de-activation in the medial frontal cortex in mania: evidence for default mode network dysfunction in the disorder. The World Federation of Societies of Biological Psychiatry 13, 616–626.CrossRefGoogle ScholarPubMed
Price, JL and Drevets, WC (2012) Neural circuits underlying the pathophysiology of mood disorders. Trends in Cognitive Sciences 16, 61–71.CrossRefGoogle ScholarPubMed
Rive, MM, van Rooijen, G, Veltman, DJ, Phillips, ML, Schene, AH and Ruhé, HG (2013) Neural correlates of dysfunctional emotion regulation in major depressive disorder. A systematic review of neuroimaging studies. Neuroscience and Biobehavioral Reviews 37, 2529–2553.CrossRefGoogle ScholarPubMed
Ruocco, AC (2005) The neuropsychology of borderline personality disorder: a meta-analysis and review. Psychiatry Research 137, 191–202.CrossRefGoogle ScholarPubMed
Ruocco, AC, Amirthavasagam, S and Zakzanis, KK (2012) Amygdala and hippocampal volume reductions as candidate endophenotypes for borderline personality disorder: a meta-analysis of magnetic resonance imaging studies. Psychiatry Research 201, 245–252.CrossRefGoogle ScholarPubMed
Salgado-Pineda, P, Fakra, E, Delaveau, P, McKenna, PJ, Pomarol-Clotet, E and Blin, O (2011) Correlated structural and functional brain abnormalities in the default mode network in schizophrenia patients. Schizophrenia Research 125, 101–109.CrossRefGoogle ScholarPubMed
Salvador, R, Vega, D, Pascual, JC, Marco, J, Canales-Rodríguez, EJ, Aguilar, S, Anguera, M, Soto, A, Ribas, J, Soler, J, Maristany, T, Rodríguez-Fornells, A and Pomarol-Clotet, E (2014) Converging medial frontal resting state and diffusion-based abnormalities in borderline personality disorder. Biological Psychiatry 79, 107–116.CrossRefGoogle ScholarPubMed
Schacter, DL, Addis, DR and Buckner, RL (2007) Remembering the past to imagine the future: the prospective brain. Nature Reviews Neuroscience 8, 657–661.CrossRefGoogle ScholarPubMed
Schneider, FC, Royer, A, Grosselin, A, Pellet, J, Barral, F-G, Laurent, B, Brouillet, D and Lang, F (2011) Modulation of the default mode network is task-dependant in chronic schizophrenia patients. Schizophrenia Research 125, 110–117.CrossRefGoogle ScholarPubMed
Schulze, L, Schmahl, C and Niedtfeld, I (2016) Neural correlates of disturbed emotion processing in borderline personality disorder: a multimodal meta-analysis. Biological Psychiatry 79, 97–106.CrossRefGoogle ScholarPubMed
Schurz, M, Radua, J, Aichhorn, M, Richlan, F and Perner, J (2014) Fractionating theory of mind: a meta-analysis of functional brain imaging studies. Neuroscience and Biobehavioral Reviews 42, 9–34.CrossRefGoogle ScholarPubMed
Sebastian, A, Jung, P, Krause-Utz, A, Lieb, K, Schmahl, C and 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.CrossRefGoogle ScholarPubMed
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 and Stern, E (2007) Failure of frontolimbic inhibitory function in the context of negative emotion in borderline personality disorder. American Journal of Psychiatry 164, 1832–1841.CrossRefGoogle ScholarPubMed
Slotema, CW, Daalman, K, Blom, JD, Diederen, KM, Hoek, HW and Sommer, IEC (2012) Auditory verbal hallucinations in patients with borderline personality disorder are similar to those in schizophrenia. Psychological Medicine 42, 1873–1878.CrossRefGoogle Scholar
Smits, ML, Feenstra, DJ, Bales, DL, de Vos, J, Lucas, Z, Verheul, R and Luyten, P (2017) Subtypes of borderline personality disorder patients: a cluster-analytic approach. Borderline Personality Disorder and Emotion Dysregulation 4, 16.CrossRefGoogle ScholarPubMed
Spencer, MD, Chura, LR, Holt, RJ, Suckling, J, Calder, AJ, Bullmore, ET and Baron-Cohen, S (2012) Failure to deactivate the default mode network indicates a possible endophenotype of autism. Molecular Autism 3, 15.CrossRefGoogle ScholarPubMed
Svoboda, E, McKinnon, MC and Levine, B (2006) The functional neuroanatomy of autobiographical memory: a meta-analysis. Neuropsychologia 44, 2189–2208.CrossRefGoogle ScholarPubMed
Villar García, M, Pérez Prieto, JF, Hernández Viadel, M, Renovell Farré, M, Leal Cercos, C and Gómez Beneyto, M (1995) Preparation of a SCID-II-based diagnostic tool for personality disorders. Spanish version. Translation and adaptation. Actas Luso-Españolas de Neurología, Psiquiatría y Ciencias Afines 23, 178–183.Google ScholarPubMed
Visintin, E, De Panfilis, C, Amore, M, Balestrieri, M, Wolf, RC and Sambataro, F (2016) Mapping the brain correlates of borderline personality disorder: a functional neuroimaging meta-analysis of resting state studies. Journal of Affective Disorders 204, 262–269.CrossRefGoogle ScholarPubMed
Whitfield-Gabrieli, S, Thermenos, HW, Milanovic, S, Tsuang, MT, Faraone, SV, McCarley, RW, Shenton, ME, Green, AI, Nieto-Castanon, A, LaViolette, P, Wojcik, J, Gabrieli, JDE and Seidman, LJ (2009) Hyperactivity and hyperconnectivity of the default network in schizophrenia and in first-degree relatives of persons with schizophrenia. Proceedings of the National Academy of Sciences 106, 1279–1284.CrossRefGoogle ScholarPubMed
Xu, T, Cullen, KR, Mueller, B, Schreiner, MW, Lim, KO, Schulz, SC and Parhi, KK (2016) Network analysis of functional brain connectivity in borderline personality disorder using resting-state fMRI. NeuroImage: Clinical 11, 302–315.CrossRefGoogle ScholarPubMed
Yee, L, Korner, AJ, McSwiggan, S, Meares, RA and Stevenson, J (2005) Persistent hallucinosis in borderline personality disorder. Comprehensive Psychiatry 46, 147–154.CrossRefGoogle ScholarPubMed
Zanarini, MC, Frankenburg, FR, Dubo, ED, Sickel, AE, Trikha, A, Levin, A and Reynolds, V (1998) Axis I comorbidity of borderline personality disorder. American Journal of Psychiatry 155, 1733–1739.CrossRefGoogle ScholarPubMed
Zanarini, MC, Frankenburg, FR, Wedig, MM and Fitzmaurice, GM (2013) Cognitive experiences reported by patients with borderline personality disorder and axis II comparison subjects: a 16-year prospective follow-up study. American Journal of Psychiatry 170, 671–679.CrossRefGoogle ScholarPubMed
Zimmerman, M and Morgan, TA (2013) The relationship between borderline personality disorder and bipolar disorder. Dialogues in Clinical Neuroscience 15, 155–169.Google ScholarPubMed
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