Top

Published in:

01-05-2019 | Borderline Personality Disorder | Original Paper

Altered Oscillatory Responses to Feedback in Borderline Personality Disorder are Linked to Symptom Severity

Authors: Paul Alexander Schauer, Jonas Rauh, Gregor Leicht, Christina Andreou, Christoph Mulert

Published in: Brain Topography | Issue 3/2019

Abstract

Several studies using electroencephalography (EEG) demonstrate that the processing of feedback in patients suffering from borderline personality disorder (BPD) is altered in comparison to healthy controls. Differences occur in the theta (ca. 5 Hz) and high-beta frequency-ranges (ca. 20 Hz) of oscillations in response to negative and positive feedback, respectively. However, alpha (ca. 10 Hz) and low-beta (ca. 15 Hz) oscillations have also been shown to be involved in feedback processing. We hypothesized that additional alterations might occur in these frequency ranges in BPD. Eighteen patients with BPD and twenty-two healthy controls performed a gambling task while 64-channel-EEG was recorded. Induced oscillatory responses to positive (i.e. gain) and negative (i.e. loss) feedback in the alpha and low-beta frequency range were investigated. No significant differences were found in the alpha frequency range. Regarding the low-beta frequency range a significant Group (i.e. BPD vs. healthy controls) × Valence (i.e. gain vs. loss) interaction in the time frame between 600 and 700 milliseconds after feedback was found. This effect showed a significant correlation with symptom severity (assessed with the BSL-23). The results indicate that feedback processing in BPD could be more heavily altered than previously expected, with more severe symptomatology being linked to stronger alterations in oscillatory responses to feedback in the low-beta range.

Andreou C, Kleinert J, Steinmann S, Fuger U, Leicht G, Mulert C (2015) Oscillatory responses to reward processing in borderline personality disorder. World J Biol Psychiatry 16:575–586. https://doi.org/10.3109/15622975.2015.1054880 CrossRefPubMed

Andreou C et al (2017) Theta and high-beta networks for feedback processing: a simultaneous EEG-fMRI study in healthy male subjects. Transl Psychiatry 7:e1016. https://doi.org/10.1038/tp.2016.287 CrossRefPubMedPubMedCentral

Ball JS, Links PS (2009) Borderline personality disorder and childhood trauma: evidence for a causal relationship. Curr Psychiatry Rep 11:63–68CrossRefPubMed

Bandelow B, Schmahl C, Falkai P, Wedekind D (2010) Borderline personality disorder: a dysregulation of the endogenous opioid system? Psychol Rev 117:623–636. https://doi.org/10.1037/a0018095 CrossRefPubMed

Bluschke A, Roessner V, Beste C (2016) Editorial perspective: how to optimise frequency band neurofeedback for ADHD. J Child Psychol Psychiatry 57:457–461. https://doi.org/10.1111/jcpp.12521 CrossRefPubMed

Bohus M, Limberger MF, Frank U, Chapman AL, Kuhler T, Stieglitz RD (2007) Psychometric properties of the borderline symptom list (BSL). Psychopathology 40:126–132. https://doi.org/10.1159/000098493 CrossRefPubMed

Bohus M et al (2009) The short version of the borderline symptom list (BSL-23): development and initial data on psychometric properties. Psychopathology 42:32–39CrossRefPubMed

Cross CP, Cyrenne DL, Brown GR (2013) Sex differences in sensation-seeking: a meta-analysis. Sci Rep 3:2486. https://doi.org/10.1038/srep02486 CrossRefPubMedPubMedCentral

Delgado MR, Nystrom LE, Fissell C, Noll DC, Fiez JA (2000) Tracking the hemodynamic responses to reward and punishment in the striatum. J Neurophysiol 84:3072–3077. https://doi.org/10.1152/jn.2000.84.6.3072 CrossRefPubMed

Fuchs M, Kastner J, Wagner M, Hawes S, Ebersole JS (2002) A standardized boundary element method volume conductor model. Clin Neurophysiol 113:702–712CrossRefPubMed

Gehring WJ, Willoughby AR (2002) The medial frontal cortex and the rapid processing of monetary gains and losses. Science 295:2279–2282. https://doi.org/10.1126/science.1066893 CrossRefPubMed

Grant BF et al (2008) Prevalence, correlates, disability, and comorbidity of DSM-IV borderline personality disorder: results from the wave 2 National Epidemiologic Survey on alcohol and related conditions. J Clin Psychiatry 69:533–545CrossRefPubMedPubMedCentral

Hajihosseini A, Holroyd CB (2013) Frontal midline theta and N200 amplitude reflect complementary information about expectancy and outcome evaluation. Psychophysiology 50:550–562. https://doi.org/10.1111/psyp.12040 CrossRefPubMed

HajiHosseini A, Rodriguez-Fornells A, Marco-Pallares J (2012) The role of beta-gamma oscillations in unexpected rewards processing. Neuroimage 60:1678–1685. https://doi.org/10.1016/j.neuroimage.2012.01.125 CrossRefPubMed

Hauser TU, Hunt LT, Iannaccone R, Walitza S, Brandeis D, Brem S, Dolan RJ (2015) Temporally dissociable contributions of human medial prefrontal subregions to reward-guided. Learn J Neurosci 35:11209–11220. https://doi.org/10.1523/JNEUROSCI.0560-15.2015 CrossRefPubMed

Heinrich H, Busch K, Studer P, Erbe K, Moll GH, Kratz O (2014) EEG spectral analysis of attention in ADHD: implications for neurofeedback training? Front Hum Neurosci 8:611. https://doi.org/10.3389/fnhum.2014.00611 CrossRefPubMedPubMedCentral

Herman JL, Perry C, Van der Kolk BA (1989) Childhood trauma in borderline personality disorder. Am J Psychiatry 146:490CrossRefPubMed

Holroyd CB, Coles MGH (2002) The neural basis of human error processing: reinforcement learning, dopamine, and the error-related negativity. Psychol Rev 109:679–709. https://doi.org/10.1037/0033-295X.109.4.679 CrossRefPubMed

Kjaer J, Biskin R, Vestergaard C, Munk-Jørgensen P (2015) A nationwide study of mortality in patients with borderline personality disorder. Eur Psychiatry 30:202CrossRef

Knutson B, Adams CM, Fong GW, Hommer D (2001) Anticipation of increasing monetary reward selectively recruits nucleus accumbens. J Neurosci 21:RC159CrossRefPubMed

Lancaster JL et al (2000) Automated Talairach atlas labels for functional brain mapping. Hum Brain Mapp 10:120–131CrossRefPubMed

Lee SH, Park Y, Jin MJ, Lee YJ, Hahn SW (2017) Childhood trauma associated with enhanced high frequency band powers and induced subjective inattention of adults. Front Behav Neurosci 11:148. https://doi.org/10.3389/fnbeh.2017.00148 CrossRefPubMedPubMedCentral

Leicht G, Troschutz S, Andreou C, Karamatskos E, Ertl M, Naber D, Mulert C (2013) Relationship between oscillatory neuronal activity during reward processing and trait impulsivity and sensation seeking. PLoS ONE 8:e83414. https://doi.org/10.1371/journal.pone.0083414 CrossRefPubMedPubMedCentral

Lenzenweger MF, Lane MC, Loranger AW, Kessler RC (2007) DSM-IV personality disorders in the National Comorbidity Survey. Replication Biol Psychiatry 62:553–564. https://doi.org/10.1016/j.biopsych.2006.09.019 CrossRefPubMed

Marco-Pallares J, Cucurell D, Cunillera T, Garcia R, Andres-Pueyo A, Munte TF, Rodriguez-Fornells A (2008) Human oscillatory activity associated to reward processing in a gambling task. Neuropsychologia 46:241–248. https://doi.org/10.1016/j.neuropsychologia.2007.07.016 CrossRefPubMed

Marin RS (1991) Apathy: a neuropsychiatric syndrome. J Neuropsychiatry Clin Neurosci 3:243–254. https://doi.org/10.1176/jnp.3.3.243 CrossRefPubMed

Mazziotta J et al (2001) A probabilistic atlas and reference system for the human brain: International Consortium for Brain Mapping (ICBM). Philos Trans R Soc Lond B Biol Sci 356:1293–1322. https://doi.org/10.1098/rstb.2001.0915 CrossRefPubMedPubMedCentral

Mobascher A et al (2009) Fluctuations in electrodermal activity reveal variations in single trial brain responses to painful laser stimuli–a fMRI/. EEG Study Neuroimage 44:1081–1092. https://doi.org/10.1016/j.neuroimage.2008.09.004 CrossRefPubMed

Montgomery SA, Åsberg M (1979) A new depression scale designed to be sensitive to change. Br J Psychiatry 134:382–389CrossRef

Morey RD (2008) Confidence intervals from normalized data: a correction to Cousineau (2005). Reason 4:61–64

Mulert C et al (2004) Integration of fMRI and simultaneous EEG: towards a comprehensive understanding of localization and time-course of brain activity in target detection. Neuroimage 22:83–94. https://doi.org/10.1016/j.neuroimage.2003.10.051 CrossRefPubMed

Nieuwenhuis S, Slagter HA, von Geusau NJ, Heslenfeld DJ, Holroyd CB (2005) Knowing good from bad: differential activation of human cortical areas by positive and negative outcomes. Eur J Neurosci 21:3161–3168. https://doi.org/10.1111/j.1460-9568.2005.04152.x CrossRefPubMed

Olbrich S, Mulert C, Karch S, Trenner M, Leicht G, Pogarell O, Hegerl U (2009) EEG-vigilance and BOLD effect during simultaneous EEG/fMRI measurement. Neuroimage 45:319–332. https://doi.org/10.1016/j.neuroimage.2008.11.014 CrossRefPubMed

Paret C, Hoesterey S, Kleindienst N, Schmahl C (2016) Associations of emotional arousal, dissociation and symptom severity with operant conditioning in borderline personality disorder. Psychiatry Res 244:194–201. https://doi.org/10.1016/j.psychres.2016.07.054 CrossRefPubMed

Pascual-Marqui RD (2002) Standardized low-resolution brain electromagnetic tomography (sLORETA): technical details. Methods Find Exp Clin Pharmacol 24 Suppl D:5–12PubMed

Peters JR, Upton BT, Baer RA (2013) Brief report: relationships between facets of impulsivity and borderline personality features. J Pers Disord 27:547–552. https://doi.org/10.1521/pedi_2012_26_044 CrossRefPubMed

Philipsen A et al (2009) Borderline typical symptoms in adult patients with attention deficit/hyperactivity disorder. Atten Defic Hyperact Disord 1:11–18. https://doi.org/10.1007/s12402-009-0001-7 CrossRefPubMed

Pornpattananangkul N, Nusslock R (2016) Willing to wait: elevated reward-processing EEG activity associated with a greater preference for larger-but-delayed rewards. Neuropsychologia 91:141–162. https://doi.org/10.1016/j.neuropsychologia.2016.07.037 CrossRefPubMedPubMedCentral

Schuermann B, Kathmann N, Stiglmayr C, Renneberg B, Endrass T (2011) Impaired decision making and feedback evaluation in borderline personality disorder. Psychol Med 41:1917–1927. https://doi.org/10.1017/S003329171000262X CrossRefPubMed

Schultz W (2006) Behavioral theories and the neurophysiology of reward. Annu Rev Psychol 57:87–115. https://doi.org/10.1146/annurev.psych.56.091103.070229 CrossRefPubMed

Sheehan D et al (1998) The Mini-International Neuropsychiatric Interview (MINI): the development and validation of a structured diagnostic psychiatric interview for DSM-IV and ICD-10. J Clin Psychiatry 59:22PubMed

Stiglmayr CE, Shapiro DA, Stieglitz RD, Limberger MF, Bohus M (2001) Experience of aversive tension and dissociation in female patients with borderline personality disorder—a controlled study. J Psychiatr Res 35:111–118CrossRefPubMed

Taber KH, Black DN, Porrino LJ, Hurley RA (2012) Neuroanatomy of dopamine: reward and addiction. J Neuropsychiatry Clin Neurosci 24:1–4. https://doi.org/10.1176/appi.neuropsych.24.1.1 CrossRefPubMed

Threadgill AH, Gable PA (2018) Resting beta activation and trait motivation: neurophysiological markers of motivated motor-action preparation. Int J Psychophysiol 127:46–51. https://doi.org/10.1016/j.ijpsycho.2018.03.002 CrossRefPubMed

van Asselt AD, Dirksen CD, Arntz A, Severens JL (2007) The cost of borderline personality disorder: societal cost of illness in BPD-patients. Eur Psychiatry 22:354–361. https://doi.org/10.1016/j.eurpsy.2007.04.001 CrossRefPubMed

Vega D, Soto A, Amengual JL, Ribas J, Torrubia R, Rodriguez-Fornells A, Marco-Pallares J (2013) Negative reward expectations in borderline personality disorder patients: neurophysiological evidence. Biol Psychol 94:388–396. https://doi.org/10.1016/j.biopsycho.2013.08.002 CrossRefPubMed

Volkow ND, Wang GJ, Fowler JS, Tomasi D, Telang F (2011) Addiction: beyond dopamine reward circuitry. Proc Natl Acad Sci USA 108:15037–15042. https://doi.org/10.1073/pnas.1010654108 CrossRefPubMed

Wittchen H, Zaudig M, Fydrich T (1997) Structured clinical interview for DSM-IV. Hogrefe, Göttingen

Yaple Z, Martinez-Saito M, Novikov NA, Altukhov D, Shestakova A, Klucharev V (2018) Power of feedback-induced beta oscillations reflect omission of rewards: evidence from an EEG gambling study. Front Neurosci 12:776CrossRefPubMedPubMedCentral

Title: Altered Oscillatory Responses to Feedback in Borderline Personality Disorder are Linked to Symptom Severity
Authors: Paul Alexander Schauer
Jonas Rauh
Gregor Leicht
Christina Andreou
Christoph Mulert
Publication date: 01-05-2019
Publisher: Springer US
Keywords: Borderline Personality Disorder
Electroencephalography
Published in: Brain Topography / Issue 3/2019
Print ISSN: 0896-0267
Electronic ISSN: 1573-6792
DOI: https://doi.org/10.1007/s10548-019-00700-4

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Altered Oscillatory Responses to Feedback in Borderline Personality Disorder are Linked to Symptom Severity

Abstract

Keynote webinar | Spotlight on medication adherence

Springer Medicine

Abstract

Please log in to get access to this content

Other articles of this Issue 3/2019

Slow Theta tACS of the Right Parietal Cortex Enhances Contralateral Visual Working Memory Capacity

Characterization of Autism Spectrum Disorder across the Age Span by Intrinsic Network Patterns

MEG Assessment of Expressive Language in Children Evaluated for Epilepsy Surgery

Altered Dynamic Functional Network Connectivity in Frontal Lobe Epilepsy

Change-Driven M100 Component in the Bilateral Secondary Somatosensory Cortex: A Magnetoencephalographic Study

Effects of Acoustic Paired Associative Stimulation on Late Auditory Evoked Potentials