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Atypical processing of social anticipation and feedback in borderline personality disorder.

ABSTRACT: BACKGROUND-:Borderline personality disorder (BPD) is characterized by maladaptive social functioning, and widespread negativity biases. The neural underpinnings of these impairments remain elusive. We thus tested whether BPD patients show atypical neural activity when processing social (compared to non-social) anticipation, feedback, and particularly, how they relate to each other. METHODS-:We acquired functional MRI data from 21 BPD women and 24 matched healthy controls (HCs) while they performed a task in which cues and feedbacks were either social (neutral faces for cues; happy or angry faces for positive and negative feedbacks, respectively) or non-social (dollar sign; winning or losing money for positive and negative feedbacks, respectively). This task allowed for the analysis of social anticipatory cues, performance-based feedback, and their interaction. RESULTS-:Compared to HCs, BPD patients expressed increased activation in the superior temporal sulcus during the processing of social cues, consistent with elevated salience associated with an upcoming social event. BPD patients also showed reduced activation in the amygdala while processing evaluative social feedback. Importantly, perigenual anterior cingulate cortex (pgACC) activity during the presentation of the social cue correlated with reduced amygdala activity during the presentation of the negative social feedback in the BPD patients. CONCLUSIONS-:These neuroimaging results clarify how BPD patients express altered responses to different types of social stimuli (i.e. social anticipatory cues and evaluative feedback) and uncover an atypical relationship between frontolimbic regions (pgACC-amygdala) over the time span of a social interaction. These findings may help to explain why BPD patients suffer from pervasive difficulties adapting their behavior in the context of interpersonal relationships and should be considered while designing better-targeted interventions.

SUBMITTER: Doell KC

PROVIDER: S-EPMC6938803 | biostudies-literature | 2020

REPOSITORIES: biostudies-literature

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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.

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.

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Atypical processing of social anticipation and feedback in borderline personality disorder.

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