Skip to main content
Top
Published in: European Archives of Psychiatry and Clinical Neuroscience 4/2018

Open Access 01-06-2018 | Original Paper

Reduced amygdala reactivity and impaired working memory during dissociation in borderline personality disorder

Authors: Annegret Krause-Utz, Dorina Winter, Friederike Schriner, Chui-De Chiu, Stefanie Lis, Philip Spinhoven, Martin Bohus, Christian Schmahl, Bernet M. Elzinga

Published in: European Archives of Psychiatry and Clinical Neuroscience | Issue 4/2018

Login to get access

Abstract

Affective hyper-reactivity and impaired cognitive control of emotional material are core features of borderline personality disorder (BPD). A high percentage of individuals with BPD experience stress-related dissociation, including emotional numbing and memory disruptions. So far little is known about how dissociation influences the neural processing of emotional material in the context of a working memory task in BPD. We aimed to investigate whole-brain activity and amygdala functional connectivity (FC) during an Emotional Working Memory Task (EWMT) after dissociation induction in un-medicated BPD patients compared to healthy controls (HC). Using script-driven imagery, dissociation was induced in 17 patients (‘BPD_D’), while 12 patients (‘BPD_N’) and 18 HC were exposed to neutral scripts during fMRI. Afterwards, participants performed the EWMT with neutral vs. negative IAPS pictures vs. no distractors. Main outcome measures were behavioral performance (reaction times, errors) and whole-brain activity during the EWMT. Psychophysiological interaction analysis was used to examine amygdala connectivity during emotional distraction. BPD patients after dissociation induction showed overall WM impairments, a deactivation in bilateral amygdala, and lower activity in left cuneus, lingual gyrus, and posterior cingulate than BPD_N, along with stronger left inferior frontal gyrus activity than HC. Furthermore, reduced amygdala FC with fusiform gyrus and stronger amygdala FC with right middle/superior temporal gyrus and left inferior parietal lobule was observed in BPD_D. Findings suggest that dissociation affects reactivity to emotionally salient material and WM. Altered activity in areas associated with emotion processing, memory, and self-referential processes may contribute to dissociative states in BPD.
Appendix
Available only for authorised users
Literature
2.
go back to reference Schmahl C, Herpertz SC, Bertsch K et al (2014) Mechanisms of disturbed emotion processing and social interaction in borderline personality disorder: state of the art and research agenda of the German Clinical Research Unit. Borderline Personal Disord Emot Dysregulation 1:12. doi:10.1186/2051-6673-1-12 CrossRef Schmahl C, Herpertz SC, Bertsch K et al (2014) Mechanisms of disturbed emotion processing and social interaction in borderline personality disorder: state of the art and research agenda of the German Clinical Research Unit. Borderline Personal Disord Emot Dysregulation 1:12. doi:10.​1186/​2051-6673-1-12 CrossRef
6.
go back to reference Krause-Utz A, Frost R, Winter D, Elzinga BM (2017) Dissociation and alterations in brain function and structure: implications for borderline personality disorder. Curr Psychiatry Rep 19(1):1–22. doi:10.1007/s11920-017-0757-y CrossRef Krause-Utz A, Frost R, Winter D, Elzinga BM (2017) Dissociation and alterations in brain function and structure: implications for borderline personality disorder. Curr Psychiatry Rep 19(1):1–22. doi:10.​1007/​s11920-017-0757-y CrossRef
11.
go back to reference Phillips ML, Sierra M (2003) Depersonalization disorder: a functional neuroanatomical perspective. Stress 6(3):157–165CrossRefPubMed Phillips ML, Sierra M (2003) Depersonalization disorder: a functional neuroanatomical perspective. Stress 6(3):157–165CrossRefPubMed
13.
go back to reference Ebner-Priemer UW, Mauchnik J, Kleindienst N et al (2009) Emotional learning during dissociative states in borderline personality disorder. J Psychiatry Neurosci 34(3):214–222PubMedPubMedCentral Ebner-Priemer UW, Mauchnik J, Kleindienst N et al (2009) Emotional learning during dissociative states in borderline personality disorder. J Psychiatry Neurosci 34(3):214–222PubMedPubMedCentral
19.
go back to reference Arntz A, Stupar-Rutenfrans S, Bloo J, van Dyck R, Spinhoven P (2015) Prediction of treatment discontinuation and recovery from borderline personality disorder: results from an RCT comparing schema therapy and transference focused psychotherapy. Behav Res Ther 74:60–71. doi:10.1016/j.brat.2015.09.002 CrossRefPubMed Arntz A, Stupar-Rutenfrans S, Bloo J, van Dyck R, Spinhoven P (2015) Prediction of treatment discontinuation and recovery from borderline personality disorder: results from an RCT comparing schema therapy and transference focused psychotherapy. Behav Res Ther 74:60–71. doi:10.​1016/​j.​brat.​2015.​09.​002 CrossRefPubMed
21.
go back to reference Ludaescher P, Valerius G, Stiglmayr C et al (2010) Pain sensitivity and neural processing during dissociative states in patients with borderline personality disorder with and without comorbid posttraumatic stress disorder: a pilot study. J Psychiatry Neurosci 35(3):177–184. doi:10.1503/jpn.090022 CrossRef Ludaescher P, Valerius G, Stiglmayr C et al (2010) Pain sensitivity and neural processing during dissociative states in patients with borderline personality disorder with and without comorbid posttraumatic stress disorder: a pilot study. J Psychiatry Neurosci 35(3):177–184. doi:10.​1503/​jpn.​090022 CrossRef
30.
go back to reference Lang PJ, Bradley MM, Cuthbert BN (2005) International Affective Picture System (IAPS): digitized photographs, instruction manual and affective ratings (Technical Report A, 6th Edn). University of Florida, Gainesville Lang PJ, Bradley MM, Cuthbert BN (2005) International Affective Picture System (IAPS): digitized photographs, instruction manual and affective ratings (Technical Report A, 6th Edn). University of Florida, Gainesville
31.
go back to reference Stiglmayr C, Schmahl C, Bremner JD, Bohus M, Ebner-Priemer U (2009) Development and psychometric characteristics of the DSS-4 as a short instrument to assess dissociative experience during neuropsychological experiments. Psychopathology 42(6):370–374. doi:10.1159/000236908 CrossRefPubMed Stiglmayr C, Schmahl C, Bremner JD, Bohus M, Ebner-Priemer U (2009) Development and psychometric characteristics of the DSS-4 as a short instrument to assess dissociative experience during neuropsychological experiments. Psychopathology 42(6):370–374. doi:10.​1159/​000236908 CrossRefPubMed
32.
go back to reference First MB, Spitzer RL, Gibbon M, Williams JB (1997) Structured Clinical Interview for DSM-IV Axis I Disorders—Clinical Version (SCID-CV). American Psychiatric Press, Washington, DC First MB, Spitzer RL, Gibbon M, Williams JB (1997) Structured Clinical Interview for DSM-IV Axis I Disorders—Clinical Version (SCID-CV). American Psychiatric Press, Washington, DC
33.
go back to reference Loranger AW (1999) International Personality Disorder Examination (IPDE): DSM-IV and ICD-10 modules. Psychological Assessment Resources, Odessa Loranger AW (1999) International Personality Disorder Examination (IPDE): DSM-IV and ICD-10 modules. Psychological Assessment Resources, Odessa
34.
go back to reference Bohus M, Kleindienst N, Limberger MF et al (2009) The short version of the Borderline Symptom List (BSL-23): development and initial data on psychometric properties. Psychopathology 42(1):32–39. doi:10.1159/000173701 CrossRefPubMed Bohus M, Kleindienst N, Limberger MF et al (2009) The short version of the Borderline Symptom List (BSL-23): development and initial data on psychometric properties. Psychopathology 42(1):32–39. doi:10.​1159/​000173701 CrossRefPubMed
37.
go back to reference Beck AT, Steer RA, Brown GK (1996) Manual for the Beck depression inventory–II. Psychological Corporation, San Antonio Beck AT, Steer RA, Brown GK (1996) Manual for the Beck depression inventory–II. Psychological Corporation, San Antonio
38.
go back to reference Spielberger CD, Gorsuch RL, Lushene RE (1970) Manual for the state-trait anxiety inventory. Consulting Psychologists Press, Palo Alto Spielberger CD, Gorsuch RL, Lushene RE (1970) Manual for the state-trait anxiety inventory. Consulting Psychologists Press, Palo Alto
39.
40.
go back to reference Roesler M, Retz-Junginger P, Retz W, Stieglitz RD (2008) [Homburger ADHS-Skalen für Erwachsene (HASE)]. Manual [in German]. Hogrefe, Göttingen Roesler M, Retz-Junginger P, Retz W, Stieglitz RD (2008) [Homburger ADHS-Skalen für Erwachsene (HASE)]. Manual [in German]. Hogrefe, Göttingen
43.
go back to reference Oei NY, Veer IM, Wolf OT, Spinhoven P, Rombouts SA, Elzinga BM (2012) Stress shifts brain activation towards ventral “affective” areas during emotional distraction. Soc Cogn Affect Neurosci 7(4):403–412. doi:10.1093/scan/nsr024 CrossRefPubMed Oei NY, Veer IM, Wolf OT, Spinhoven P, Rombouts SA, Elzinga BM (2012) Stress shifts brain activation towards ventral “affective” areas during emotional distraction. Soc Cogn Affect Neurosci 7(4):403–412. doi:10.​1093/​scan/​nsr024 CrossRefPubMed
45.
go back to reference Tzourio-Mazoyer N, Landeau B, Papathanassiou D et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15(1):273–289. doi:10.1006/nimg.2001.0978 CrossRefPubMed Tzourio-Mazoyer N, Landeau B, Papathanassiou D et al (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. NeuroImage 15(1):273–289. doi:10.​1006/​nimg.​2001.​0978 CrossRefPubMed
56.
go back to reference Ochsner KN, Gross JJ (2007) The neural architecture of emotion regulation. In: Gross JJ, Buck R (eds) The Handbook of emotion regulation. Guilford Press, New York, pp 87–109 Ochsner KN, Gross JJ (2007) The neural architecture of emotion regulation. In: Gross JJ, Buck R (eds) The Handbook of emotion regulation. Guilford Press, New York, pp 87–109
62.
63.
65.
go back to reference Kamphausen S, Schroder P, Maier S et al (2013) Medial prefrontal dysfunction and prolonged amygdala response during instructed fear processing in borderline personality disorder. World J Biol Psychiatry 14(4):307–318, S1–4. doi:10.3109/15622975.2012.665174 Kamphausen S, Schroder P, Maier S et al (2013) Medial prefrontal dysfunction and prolonged amygdala response during instructed fear processing in borderline personality disorder. World J Biol Psychiatry 14(4):307–318, S1–4. doi:10.​3109/​15622975.​2012.​665174
68.
go back to reference Krause-Utz A, Veer IM, Rombouts SARB, Bohus M, Schmahl C, Elzinga BM (2014) Amygdala and anterior cingulate resting-state functional connectivity in borderline personality disorder patients with a history of interpersonal trauma. Psychol Med 44(13):2889–2901. doi:10.1017/S0033291714000324 CrossRefPubMed Krause-Utz A, Veer IM, Rombouts SARB, Bohus M, Schmahl C, Elzinga BM (2014) Amygdala and anterior cingulate resting-state functional connectivity in borderline personality disorder patients with a history of interpersonal trauma. Psychol Med 44(13):2889–2901. doi:10.​1017/​S003329171400032​4 CrossRefPubMed
70.
go back to reference Kruschwitz JD, Meyer-Lindenberg A, Veer IM et al (2015) Segregation of face sensitive areas within the fusiform gyrus using global signal regression? A study on amygdala resting-state functional connectivity. Hum Brain Mapp 36(10):4089–40103. doi:10.1002/hbm.22900 CrossRefPubMed Kruschwitz JD, Meyer-Lindenberg A, Veer IM et al (2015) Segregation of face sensitive areas within the fusiform gyrus using global signal regression? A study on amygdala resting-state functional connectivity. Hum Brain Mapp 36(10):4089–40103. doi:10.​1002/​hbm.​22900 CrossRefPubMed
74.
go back to reference Nicholson AA, Densmore M, Frewen PA et al (2015) The dissociative subtype of posttraumatic stress disorder: unique resting-state functional connectivity of basolateral and centromedial amygdala complexes. Neuropsychopharmacology 40(10):2317–2326. doi:10.1038/npp.2015.79 CrossRefPubMedPubMedCentral Nicholson AA, Densmore M, Frewen PA et al (2015) The dissociative subtype of posttraumatic stress disorder: unique resting-state functional connectivity of basolateral and centromedial amygdala complexes. Neuropsychopharmacology 40(10):2317–2326. doi:10.​1038/​npp.​2015.​79 CrossRefPubMedPubMedCentral
76.
go back to reference Bremner JD, Vermetten E, Southwick SM, Krystal JH, Charney DS (1998) Trauma, memory, and dissociation: an integrative formulation. American Psychiatric Association Press, Washington, DC, pp 365–402 Bremner JD, Vermetten E, Southwick SM, Krystal JH, Charney DS (1998) Trauma, memory, and dissociation: an integrative formulation. American Psychiatric Association Press, Washington, DC, pp 365–402
79.
go back to reference Fanselow MS, Lester LS (1988) A functional behavioristic approach to aversively motivated behavior: predatory imminence as a determinant of the topography of the defensive behavior. In: Bolles RC, Breecher MD (eds) Evolution and learning. Erlbaum, Hilsdale, pp 185–212 Fanselow MS, Lester LS (1988) A functional behavioristic approach to aversively motivated behavior: predatory imminence as a determinant of the topography of the defensive behavior. In: Bolles RC, Breecher MD (eds) Evolution and learning. Erlbaum, Hilsdale, pp 185–212
83.
go back to reference Cannon WB (1929) Bodily changes in pain, hunger, fear, and range. Appleton-Century-Crofts, New York Cannon WB (1929) Bodily changes in pain, hunger, fear, and range. Appleton-Century-Crofts, New York
Metadata
Title
Reduced amygdala reactivity and impaired working memory during dissociation in borderline personality disorder
Authors
Annegret Krause-Utz
Dorina Winter
Friederike Schriner
Chui-De Chiu
Stefanie Lis
Philip Spinhoven
Martin Bohus
Christian Schmahl
Bernet M. Elzinga
Publication date
01-06-2018
Publisher
Springer Berlin Heidelberg
Published in
European Archives of Psychiatry and Clinical Neuroscience / Issue 4/2018
Print ISSN: 0940-1334
Electronic ISSN: 1433-8491
DOI
https://doi.org/10.1007/s00406-017-0806-x

Other articles of this Issue 4/2018

European Archives of Psychiatry and Clinical Neuroscience 4/2018 Go to the issue