Abstract

Emotion dysregulation is central to the development and maintenance of psychopathology, and is common across many psychiatric disorders. Neurobiological models of emotion dysregulation involve the fronto-limbic brain network, including in particular the amygdala and prefrontal cortex (PFC). Neural variability has recently been suggested as an index of cognitive flexibility. We hypothesized that within-subject neural variability in the fronto-limbic network would be related to inter-individual variation in emotion dysregulation in the context of low affective control. In a multi-site cohort (N = 166, 93 females) of healthy individuals and individuals with emotional dysregulation (attention deficit/hyperactivity disorder (ADHD), bipolar disorder (BD), and borderline personality disorder (BPD)), we applied partial least squares (PLS), a multivariate data-driven technique, to derive latent components yielding maximal covariance between blood-oxygen level-dependent (BOLD) signal variability at rest and emotion dysregulation, as expressed by affective lability, depression and mania scores. PLS revealed one significant latent component (r = 0.62, p = 0.044), whereby greater emotion dysregulation was associated with increased neural variability in the amygdala, hippocampus, ventromedial, dorsomedial and dorsolateral PFC, insula and motor cortex, and decreased neural variability in occipital regions. This spatial pattern bears a striking resemblance to the fronto-limbic network, which is thought to subserve emotion regulation, and is impaired in individuals with ADHD, BD, and BPD. Our work supports emotion dysregulation as a transdiagnostic dimension with neurobiological underpinnings that transcend diagnostic boundaries, and adds evidence to neural variability being a relevant proxy of neural efficiency.

Highlights

  • Emotion regulation allows individuals to modulate, manage or organize emotions in order to help them meet the demands of the environment and achieve their goals [1,2,3], implicating various processes and systems

  • All posthoc analyses were corrected for multiple comparisons at a false discovery rate (FDR) of q < 0.05

  • We found that emotion dysregulation was associated with a pattern of increased blood-oxygen level-dependent (BOLD) signal variability in the ventromedial prefrontal cortex (PFC), dorsomedial and dorsolateral PFC, amygdala, hippocampus, insula and motor cortex, and decreased BOLD signal variability in Control analyses A number of control analyses were computed to assess the robustness of our results

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Summary

Introduction

Emotion regulation allows individuals to modulate, manage or organize emotions in order to help them meet the demands of the environment and achieve their goals [1,2,3], implicating various processes and systems (e.g., cognitive, behavioral, social, biological). Emotion regulation is thought to rely on a fronto-limbic network, whereby the prefrontal cortex (PFC) exerts cognitive control over the amygdala, a subcortical structure that is central to emotion processing and salience perception [10,11,12]. Alterations in this network are central to the pathophysiology of bipolar disorder (BD), borderline personality disorder (BPD), and attention deficit/hyperactivity disorder (ADHD), which are all characterized by emotion dysregulation [13,14,15,16,17,18]. This suggests that emotion dysregulation might have underlying neurobiological mechanisms that are shared across these disorders

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