Progressive modulation of resting-state brain activity during neurofeedback of positive-social emotion regulation networks

Marina Krylova,Stavros Skouras,Andrew A Nicholson,Geraint Rees,Adeel Razi,Frank Scharnowski,David Steyrl,Olga Boukrina,Alexander Karner,Yury Koush

doi:10.1038/s41598-021-02079-4

Abstract

Neurofeedback allows for the self-regulation of brain circuits implicated in specific maladaptive behaviors, leading to persistent changes in brain activity and connectivity. Positive-social emotion regulation neurofeedback enhances emotion regulation capabilities, which is critical for reducing the severity of various psychiatric disorders. Training dorsomedial prefrontal cortex (dmPFC) to exert a top-down influence on bilateral amygdala during positive-social emotion regulation progressively (linearly) modulates connectivity within the trained network and induces positive mood. However, the processes during rest that interleave the neurofeedback training remain poorly understood. We hypothesized that short resting periods at the end of training sessions of positive-social emotion regulation neurofeedback would show alterations within emotion regulation and neurofeedback learning networks. We used complementary model-based and data-driven approaches to assess how resting-state connectivity relates to neurofeedback changes at the end of training sessions. In the experimental group, we found lower progressive dmPFC self-inhibition and an increase of connectivity in networks engaged in emotion regulation, neurofeedback learning, visuospatial processing, and memory. Our findings highlight a large-scale synergy between neurofeedback and resting-state brain activity and connectivity changes within the target network and beyond. This work contributes to our understanding of concomitant learning mechanisms post training and facilitates development of efficient neurofeedback training.

Highlights

Neurofeedback allows for the self-regulation of brain circuits implicated in specific maladaptive behaviors, leading to persistent changes in brain activity and connectivity
We first briefly describe neurofeedback task-related learning effects of the positive-social emotion regulation based on effective connectivity neurofeedback training, which were thoroughly reported and discussed in a previous publication[29]
The ANOVA on valence ratings revealed the main effect of group [Fig. 1D, F(1,12) = 4.80, p = 0.049], which was driven by an expected significant increase in valence ratings due to neurofeedback training in the experimental [one-tailed paired t-test, t(8) = 2.04, p = 0.038], but not in the control group [one-tailed paired t-test, t(5) = 1.33, p = 0.120]

Summary

Introduction

Neurofeedback allows for the self-regulation of brain circuits implicated in specific maladaptive behaviors, leading to persistent changes in brain activity and connectivity. Training dorsomedial prefrontal cortex (dmPFC) to exert a top-down influence on bilateral amygdala during positive-social emotion regulation progressively (linearly) modulates connectivity within the trained network and induces positive mood. Neurofeedback is associated with post-training resting-state functional connectivity (rs-FC) modulations in target brain areas and beyond them, as detected immediately after neurofeedback training[9,11,12], several days after training[13] or weeks/months after training[14,15,16]. According to emotion regulation models, successful regulation is achieved through the modulation of bottomup emotional responses in limbic areas by cognitive top-down processes originating in prefrontal cortices[22,23,24,25,26,27]. The role of rest in neurofeedback learning and concomitant resting-state neural modulations remains unexplored, where filling this knowledge gap could help understand learning mechanisms and improve design efficiency of neurofeedback training paradigms

Methods

Results

Conclusion