Elsevier

Biological Psychiatry

Volume 72, Issue 6, 15 September 2012, Pages 448-456
Biological Psychiatry

Priority Communication
Potentiated Amygdala Response to Repeated Emotional Pictures in Borderline Personality Disorder

https://doi.org/10.1016/j.biopsych.2012.03.027Get rights and content

Background

Borderline personality disorder (BPD) is characterized by an inability to regulate emotional responses. The amygdala is important in learning about the valence (goodness and badness) of stimuli and functions abnormally in BPD.

Methods

Event-related functional magnetic resonance imaging (MRI) was employed in three groups: unmedicated BPD (n = 33) and schizotypal personality disorder (n = 28) participants and healthy control subjects (n = 32) during a task involving an intermixed series of unpleasant, neutral, and pleasant pictures each presented twice within their respective trial block/run. The amygdala was hand-traced on each participant's structural MRI scan and co-registered to their MRI scan. Amygdala responses were examined with a mixed-model multivariate analysis of variance.

Results

Compared with both control groups, BPD patients showed greater amygdala activation, particularly to the repeated emotional but not neutral pictures, and a prolonged return to baseline for the overall blood oxygen level-dependent response averaged across all pictures. Despite amygdala overactivation, BPD patients showed blunted self-report ratings of emotional but not neutral pictures. Fewer dissociative symptoms in both patient groups were associated with greater amygdala activation to repeated unpleasant pictures.

Conclusions

The increased amygdala response to the repeated emotional pictures observed in BPD was not observed in schizotypal patients, suggesting diagnostic specificity. This BPD-related abnormality is consistent with the well-documented clinical feature of high sensitivity to emotional stimuli with unusually strong and long-lasting reactions. The finding of a mismatch between physiological and self-report measures of emotion reactivity in BPD patients suggests they may benefit from treatments targeting emotion recognition.

Section snippets

Participants

Thirty-three patients with BPD, 28 patients with SPD, and 32 HCs were included (Table 1; Table S1 in Supplement 1 for additional demographic/clinical/exclusionary criteria details). The groups did not significantly differ in age, gender, or education and all patients met DSM-IV criteria. All patients were unmedicated at the time of their fMRI scan (>6 weeks) and most were never previously medicated. Patients with a history of schizophrenia, psychotic disorder, bipolar (type I) affective

Functional and Structural MRI Acquisition

The MRI scan procedure was conducted on an Allegra head-dedicated 3T scanner (Siemens, Erlangen, Germany) and included a T2, echo planar image, and T1-weighted structural magnetization prepared rapid acquisition gradient-echo (MP-RAGE) scan. See Figure S1 in Supplement 1 for scan parameter details.

Amygdala Activation During Picture Processing

Following picture onset, the BPD patients exhibited an overall amygdala BOLD response curve (averaged across all repeated measures except time) with a much slower return to baseline compared with the HC and SPD groups (Figure 1, top). The HCs showed the smallest amygdala BOLD response peak, while the SPD group showed the greatest and the BPD patients were intermediate. The HCs also had the fastest peak latency; SPD patients showed the slowest; and BPD patients were intermediate, group × time

Discussion

Our study has two novel findings reflecting BPD-related abnormalities in amygdala function. First, BPD patients showed reduced overall habituation (time series) in terms of their BOLD response curve returning to baseline following picture onset. That is, averaged across the three picture conditions (unpleasant, neutral, and pleasant), BPD patients showed a prolonged amygdala response compared with the HC and SPD groups. The region of interest time series showed and the whole-brain analysis

References (75)

  • H.W. Koenigsberg et al.

    Neural correlates of emotion processing in borderline personality disorder

    Psychiatry Res

    (2009)
  • H.W. Koenigsberg et al.

    Neural correlates of the use of psychological distancing to regulate responses to negative social cues: A study of patients with borderline personality disorder

    Biol Psychiatry

    (2009)
  • L. Schulze et al.

    Neuronal correlates of cognitive reappraisal in borderline patients with affective instability

    Biol Psychiatry

    (2011)
  • J. LeDoux

    Emotional networks and motor control: A fearful view

    Prog Brain Res

    (1996)
  • E.A. Hazlett et al.

    Exaggerated affect-modulated startle during unpleasant stimuli in borderline personality disorder

    Biol Psychiatry

    (2007)
  • A. Limberg et al.

    Emotional vulnerability in borderline personality disorder is cue specific and modulated by traumatization

    Biol Psychiatry

    (2011)
  • S.M. Smith et al.

    Advances in functional and structural MR image analysis and implementation as FSL

    Neuroimage

    (2004)
  • R.J. Larsen et al.

    A multitrait-multimethod examination of affect structure: Hedonic level and emotional intensity

    Person Individ Diff

    (1985)
  • M.M. Bradley et al.

    Measuring emotion: The Self-Assessment Manikin and the Semantic Differential

    J Behav Ther Exp Psychiatry

    (1994)
  • M. Jenkinson et al.

    Improved optimization for the robust and accurate linear registration and motion correction of brain images

    Neuroimage

    (2002)
  • E.A. Hazlett et al.

    Frontal-striatal-thalamic mediodorsal nucleus dysfunction in schizophrenia-spectrum patients during sensorimotor gating

    Neuroimage

    (2008)
  • I. Dziobek et al.

    Neuronal correlates of altered empathy and social cognition in borderline personality disorder

    Neuroimage

    (2011)
  • U.W. Ebner-Priemer et al.

    Affective dysregulation and dissociative experience in female patients with borderline personality disorder: A startle response study

    J Psychiatr Res

    (2005)
  • J. Debiec et al.

    Disruption of reconsolidation but not consolidation of auditory fear conditioning by noradrenergic blockade in the amygdala

    Neuroscience

    (2004)
  • J.G. Gunderson et al.

    A current view of the interface between borderline personality disorder and depression

    Am J Psychiatry

    (1991)
  • M.M. Linehan

    Cognitive Behavioral Treatment of Borderline Personality Disorder

    (1993)
  • A.E. Skodol et al.

    Functional impairment in patients with schizotypal, borderline, avoidant, or obsessive-compulsive personality disorder

    Am J Psychiatry

    (2002)
  • J. Coid et al.

    Prevalence and correlates of personality disorder in Great Britain

    Br J Psychiatry

    (2006)
  • B.F. Grant et al.

    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

    (2008)
  • J.G. Gunderson et al.

    Pathogenesis in borderline personality

  • M.M. Linehan

    Understanding Borderline Personality Disorder

    (1995)
  • J.L. Andreassi

    Psychophysiology: Human Behavior and Physiological Response

    (1989)
  • R.M. Stern et al.

    Psychophysiological Recording

    (2001)
  • G.J. Siegle et al.

    Use of fMRI to predict recovery from unipolar depression with cognitive behavior therapy

    Am J Psychiatry

    (2006)
  • P.J. Whalen et al.

    Masked presentations of emotional facial expressions modulate amygdala activity without explicit knowledge

    J Neurosci

    (1998)
  • E.A. Phelps

    Emotion and cognition: Insights from studies of the human amygdala

    Annu Rev Psychol

    (2006)
  • M. Davis et al.

    The amygdala: Vigilance and emotion

    Mol Psychiatry

    (2001)
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