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

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

NeuroImage. Clinical 20191219

<h4>Background-</h4>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.<h4>Methods-</h4>We acquired functional MRI data from 21 BPD women and 24 matched healthy controls (HCs) whi ...[more]

PMID: 31884223

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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.

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

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

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