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Physical pain recruits the nucleus accumbens during social distress in borderline personality disorder.

ABSTRACT: Patients with borderline personality disorder (BPD) often engage in dangerous self-injurious behaviors (SIBs) as a maladaptive technique to decrease heightened feelings of distress (e.g. negative feelings caused by social exclusion). The reward system has recently been proposed as a plausible neural substrate, which may influence the interaction between social distress and physical pain processing in patients that engage in SIBs. Using functional magnetic resonance imaging (fMRI) in 20 adult BPD patients with a history of SIBs and 23 healthy controls (HCs), we found a hyper-activation of the nucleus accumbens (NAcc) and amygdala when painful stimuli were presented to BPD patients (but not HCs) in a state of heightened distress, induced via social exclusion. This differential NAcc activity was mediated by anxious attachment style, which is a key developmental feature of the disorder. Altogether, these results suggest a neural mechanism underlying the pathophysiology of SIBs in these patients, which is likely reinforced via the reward system.

SUBMITTER: Olie E

PROVIDER: S-EPMC6204482 | biostudies-literature | 2018 Oct

REPOSITORIES: biostudies-literature

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Physical pain recruits the nucleus accumbens during social distress in borderline personality disorder.

Olié Emilie E Doell Kimberly C KC Corradi-Dell'Acqua Corrado C Courtet Philippe P Perroud Nader N Schwartz Sophie S

Social cognitive and affective neuroscience 20181001 10

Patients with borderline personality disorder (BPD) often engage in dangerous self-injurious behaviors (SIBs) as a maladaptive technique to decrease heightened feelings of distress (e.g. negative feelings caused by social exclusion). The reward system has recently been proposed as a plausible neural substrate, which may influence the interaction between social distress and physical pain processing in patients that engage in SIBs. Using functional magnetic resonance imaging (fMRI) in 20 adult BPD ...[more]

PMID: 30204911

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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:BackgroundInterpersonal impairments in borderline personality disorder (BPD) are characterised by a lack in the sense of belonging and the fear of being excluded. One feature of interactions that can promote a sense of social belonging is interpersonal touch. While some studies suggest that individuals with BPD experience social touch as less pleasurable than healthy individuals (HCs), there are no studies that investigated whether this difference is associated with feeling less socially connected. This question is particularly important during the COVID-19 pandemic, since one central behavioural recommendation is "social distancing". An increase in loneliness has been discussed as a consequence and it has been suggested that individuals with BPD may be particularly burdened. However, the primary goal of "social distancing" is not preventing social contacts, but physical proximity. In our study we investigated the interplay between feeling close to others, contact frequency and the appraisal of social touch in BPD. We were additionally interested in whether these factors contribute to the burden through "physical distancing".MethodsWe assessed subjective and objective social isolation, the need, importance, and liking of social touch, as well as the burden through "physical distancing" policies in 130 women (61 BPD and 69 HCs).ResultsParticipants of the BPD group reported higher loneliness, less social contacts and a lower need for, importance and liking of social touch compared to HCs. Larger social networks, higher frequency of in-person contacts and higher liking and importance of social touch were associated with lower levels of loneliness. Both groups did not differ regarding their burden through "physical distancing". A higher need for and lower importance of social touch predicted a higher burden through "physical distancing".ConclusionsA positive appraisal of social touch was associated with less loneliness, independently of an individual's objective social isolation. In BPD, impairments of this fundamental facet of social interaction might hamper forming and strengthening of social bonds and contribute to the patients' interpersonal dysfunction. Changing the attitude towards social touch and in consequence its liking and importance in social interaction might provide one avenue to improve the sense of social connectedness in these patients.

Dataset Information

Physical pain recruits the nucleus accumbens during social distress in borderline personality disorder.

Publications

Physical pain recruits the nucleus accumbens during social distress in borderline personality disorder.

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