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Cerebral processing of social rejection in patients with borderline personality disorder.

ABSTRACT: An intense fear of abandonment or rejection is a central feature of social relationships for individuals with borderline personality disorder (BPD). A total of 20 unmedicated BPD patients and 20 healthy participants (HC, matched for age and education) played a virtual ball-tossing game including the three conditions: exclusion, inclusion and a control condition with predefined game rules, whereas cerebral activity was assessed using functional magnetic resonance imaging. Subjective experiences of exclusion were assessed after each blocked condition. Both groups felt similarly excluded during the exclusion condition; however, BPD subjects felt more excluded than HC during the inclusion and control conditions. In all three conditions, BPD patients showed a stronger engagement of the dorsal anterior cingulate and medial prefrontal cortex. For HC, activation in several cerebral regions such as the insula and the precuneus differed depending on the interaction situation, whereas for BPD subjects activation in these regions was not modulated by experimental conditions. Subjects with BPD differed from HC in both their subjective reactions to and their neural processing of social interaction situations. Our data suggest that individuals with BPD have difficulty in discriminating between social situations, and tend to hypermentalize during social encounters that are not determined by the intentions of others.

SUBMITTER: Domsalla M

PROVIDER: S-EPMC4221221 | biostudies-literature | 2014 Nov

REPOSITORIES: biostudies-literature

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Cerebral processing of social rejection in patients with borderline personality disorder.

Domsalla Melanie M Koppe Georgia G Niedtfeld Inga I Vollstädt-Klein Sabine S Schmahl Christian C Bohus Martin M Lis Stefanie S

Social cognitive and affective neuroscience 20131121 11

An intense fear of abandonment or rejection is a central feature of social relationships for individuals with borderline personality disorder (BPD). A total of 20 unmedicated BPD patients and 20 healthy participants (HC, matched for age and education) played a virtual ball-tossing game including the three conditions: exclusion, inclusion and a control condition with predefined game rules, whereas cerebral activity was assessed using functional magnetic resonance imaging. Subjective experiences o ...[more]

PMID: 24273076

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Project description:ObjectiveThere is a general agreement that physical pain serves as an alarm signal for the prevention of and reaction to physical harm. It has recently been hypothesized that "social pain," as induced by social rejection or abandonment, may rely on comparable, phylogenetically old brain structures. As plausible as this theory may sound, scientific evidence for this idea is sparse. This study therefore attempts to link both types of pain directly. We studied patients with borderline personality disorder (BPD) because BPD is characterized by opposing alterations in physical and social pain; hyposensitivity to physical pain is associated with hypersensitivity to social pain, as indicated by an enhanced rejection sensitivity.MethodTwenty unmedicated female BPD patients and 20 healthy participants (HC, matched for age and education) played a virtual ball-tossing game (cyberball), with the conditions for exclusion, inclusion, and a control condition with predefined game rules. Each cyberball block was followed by a temperature stimulus (with a subjective pain intensity of 60% in half the cases). The cerebral responses were measured by functional magnetic resonance imaging. The Adult Rejection Sensitivity Questionnaire was used to assess rejection sensitivity.ResultsHigher temperature heat stimuli had to be applied to BPD patients relative to HCs to reach a comparable subjective experience of painfulness in both groups, which suggested a general hyposensitivity to pain in BPD patients. Social exclusion led to a subjectively reported hypersensitivity to physical pain in both groups that was accompanied by an enhanced activation in the anterior insula and the thalamus. In BPD, physical pain processing after exclusion was additionally linked to enhanced posterior insula activation. After inclusion, BPD patients showed reduced amygdala activation during pain in comparison with HC. In BPD patients, higher rejection sensitivity was associated with lower activation differences during pain processing following social exclusion and inclusion in the insula and in the amygdala.DiscussionDespite the similar behavioral effects in both groups, BPD patients differed from HC in their neural processing of physical pain depending on the preceding social situation. Rejection sensitivity further modulated the impact of social exclusion on neural pain processing in BPD, but not in healthy controls.

Project description:Humans engage in social interactions and have a fundamental need and motivation to establish and maintain social connections. Neuroimaging studies particularly focused on the neural substrates of social exclusion in healthy subjects (HC), borderline personality disorder (BPD), and major depression (MD). However, there is evidence regarding neural alterations also during social inclusion in BPD that we intended to elucidate in our study. Considering that patients with BPD often have comorbid MD, we investigated patients with BPD, and comorbid MD, patients with MD without BPD, and a sample of HC. By investigating these two clinical samples within one study design, we attempted to disentangle potential confounds arising by psychiatric disorder or medication and to relate neural alterations under social inclusion specifically to BPD. We investigated 48 females (15 BPD and MD, 16 MD, and 17 HC) aged between 18 and 40 years by fMRI (3T), using the established cyberball paradigm with social exclusion, inclusion, and passive watching conditions. Significant group-by-condition interaction effects (p < 0.05, FWE-corrected on cluster level) were observed within the dorsolateral (dlPFC) and dorsomedial prefrontal cortex (dmPFC), the temporo-parietal junction (TPJ), the posterior cingulate cortex (PCC), and the precuneus. Comparisons of estimated neural activations revealed that significant interaction effects were related to a relative increase in neural activations during social inclusion in BPD. In detail, we observed a significant increase in differential (social inclusion vs. passive watching) neural activation within the dmPFC and the PCC in BPD compared to both, MD and HC. However, significant interaction effects within the dlPFC and the TPJ could not specifically be linked to BPD considering that they did not differ significantly between the two clinical groups in post-hoc comparisons. Our study supports previous results on effects of social and inclusion in BPD, and provides further evidence regarding disorder specific neural alterations in BPD for brain regions associated with self-referential and mentalizing processes during social inclusion.

Project description:Recent neuroimaging studies have associated activity in the default mode network (DMN) with self-referential and pain processing, both of which are altered in borderline personality disorder (BPD). In patients with BPD, antinociception has been linked to altered activity in brain regions involved in the cognitive and affective evaluation of pain. Findings in healthy subjects indicate that painful stimulation leads to blood oxygenation level-dependent signal decreases and changes in the functional architecture of the DMN.To connect the previously separate research areas of DMN connectivity and altered pain perception in BPD and to explore DMN connectivity during pain processing in patients with BPD.Case-control study.University hospital.Twenty-five women with BPD, including 23 (92%) with a history of self-harm, and 22 age-matched control subjects.Psychophysical assessment and functional magnetic resonance imaging during painful heat vs neutral temperature stimulation.Connectivity of DMN as assessed via independent component analysis and psychophysiological interaction analysis.Compared with control subjects, patients with BPD showed less integration of the left retrosplenial cortex and left superior frontal gyrus into the DMN. Higher BPD symptom severity and trait dissociation were associated with an attenuated signal decrease of the DMN in response to painful stimulation. During pain vs neutral, patients with BPD exhibited less posterior cingulate cortex seed region connectivity with the left dorsolateral prefrontal cortex.Patients with BPD showed significant alterations in DMN connectivity, with differences in spatial integrity and temporal characteristics. These alterations may reflect a different cognitive and affective appraisal of pain as less self-relevant and aversive as well as a deficiency in the switching between baseline and task-related processing. This deficiency may be related to everyday difficulties of patients with BPD in regulating their emotions, focusing mindfully on 1 task at a time, and efficiently shifting their attention from one task to another.

Dataset Information

Cerebral processing of social rejection in patients with borderline personality disorder.

Publications

Cerebral processing of social rejection in patients with borderline personality disorder.

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