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Comparative Study
, 72 (6), 448-56

Potentiated Amygdala Response to Repeated Emotional Pictures in Borderline Personality Disorder

Affiliations
Comparative Study

Potentiated Amygdala Response to Repeated Emotional Pictures in Borderline Personality Disorder

Erin A Hazlett et al. Biol Psychiatry.

Abstract

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.

Figures

Figure 1
Figure 1
Top: The amygdala BOLD response curve is shown for each of the three groups averaged across all repeated measures (picture type, repetition, startle/no startle, and hemisphere) except for Time (3, 6, 9…33 sec following picture onset). The amygdala was hand traced on each individual study participant’s structural MRI (MP-RAGE) and co-registered to their EPI scan. The borderline personality disorder (BPD) patients showed an amygdala response curve which peaked later than the healthy controls and took longer to return to baseline compared with both healthy controls and schizotypal personality disorder (SPD) patients. This BPD-related pattern of a protracted amygdala response is consistent with the concept that BPD patients have long-lasting responses to emotional stimuli. The SPD patients showed the longest peak latency and highest peak response in the amygdala while the controls showed the shortest peak response and lower overall BOLD activation in the amygdala. As shown, this Group × Time interaction was significant. For both graphs, the significant post-hoc Fisher’s LSD tests, p<0.05 are noted and the standard error bars are provided. Bottom: The BPD group showed a greater overall BOLD response in the amygdala during the repeated pictures compared with both the healthy controls and the SPD patients. In contrast, the SPD group showed a higher peak during the novel pictures. As shown, this Group × Picture repetition (novel, repeated) × Time interaction was significant.
Figure 2
Figure 2
Top: Overall, the BPD group showed greater amygdala activation during the repeated pictures compared with the healthy control and SPD groups. In contrast, the SPD group showed greater amygdala activation during the novel picture presentation. As shown, this Group × Picture repetition (novel, repeat) interaction was significant. Significant post-hoc Fisher’s LSD tests, p<0.05 and standard error bars are shown for both graphs. Bottom: For each of the groups, the mean amygdala BOLD response is shown during the novel and repeated picture presentations for each of the three picture types. Compared with healthy controls and schizotypal personality disorder (SPD) patients, the borderline personality disorder (BPD) patients showed an increase in their mean amygdala response from the novel to the repeated emotional (both the unpleasant and pleasant pictures) pictures. This Group × Picture type (unpleasant, neutral, pleasant) × Picture repetition (novel, repeat) interaction was significant.
Figure 3
Figure 3
Statistical probability maps from FSL(4.1)(39) for the between-group effects in response to unpleasant pictures are shown. The maps are thresholded at Z>2.0 (or p<0.05, corrected) and the color bar shows p<0.05 (corrected). See Table-S2 for the size and location of the clusters. A1–2. These SPM results demonstrate increased amygdala activity in SPD patients compared with HCs (A1) and in the SPD patients compared with BPD patients (A2) in response to the novel or first (i.e. Time 1) presentation of the unpleasant pictures. B1–2. With the repeated presentation of unpleasant pictures, the whole-brain analysis showed increased activity in the right amygdala (region inside the green circle) and left fusiform gyrus (BA37) in the BPD patients compared with the HCs (B1) and in regions including the bilateral amygdala and right dorsolateral prefrontal cortex (DLPFC; BA10) in the SPD patients compared with the HCs (B2). C1–2. Between-group effects for (Time 2 (repeated) – Time 1 (novel)) differences. C1. Activity was increased in brain areas including the right fusiform gyrus (BA37), anterior cingulate (BA24), and inferior frontal gyrus (BA44) in BPD patients compared with HCs. C2. Activity was also increased in BPD compared with SPD patients in regions including left and right (green circle) amygdala and right DLPFC (BA10). Standard whole-brain GLM analysis. GLM analysis was first carried out on the preprocessed fMRI data for each single subject with FILM (FMRIB’s Improved Linear Model) with six contrasts set for unpleasant, neutral, and pleasant pictures at novel presentation (Time-1) and repeated presentation (Time-2). Next, single-subject statistics were fed into second-level multi-session, multi-subject analysis. The between-group t-test analysis was performed on the three separate groups with FLAME (FMRIB’s Local Analysis of Mixed Effects).
Figure 4
Figure 4
Group means for the self-report ratings of picture valence are shown for the pictures viewed in the magnet (Top graph) and following the fMRI session (Bottom graph using the Self-Assessment Manikin (SAM) scale (47)). There were no between-group differences for the neutral picture ratings. Both Group × Picture type interactions are significant as shown. Top: During the fMRI session, both the borderline personality disorder (BPD) and schizotypal personality disorder (SPD) groups showed blunted (i.e. rated unpleasant and pleasant as more neutral) self-report ratings of the emotional pictures compared with healthy controls. Asterisks denote significant differences from the healthy controls (follow-up Fisher’s LSD tests), all p-values<0.007. Bottom: Similarly, the post-fMRI session self-report ratings show that compared with the healthy control group, both the BPD and SPD groups exhibited a blunted response pattern to the unpleasant pictures. BPD patients also showed a blunted response for the pleasant pictures compared with healthy controls and SPD patients. Asterisks denote significant differences from the healthy controls (Fisher’s LSD tests, all p-values<0.007). The “a” represents BPD>SPD, p=0.0002.

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