Abstract

Recently, the dynamic properties of brain activity rather than its stationary values have attracted more interest in clinical applications. It has been shown that brain signals exhibit scale-free dynamics or long-range temporal correlations (LRTC) that differ between rest and cognitive tasks in healthy controls and clinical groups. Little is known about how fear-inducing tasks may influence dispersion and the LRTC of subsequent resting-state brain activity. In this study, we aimed to explore the changes in the variance and scale-free properties of the brain’s blood oxygenation level-dependent (BOLD) signal during the resting-state sessions before and after fear learning and fear memory extinction. During a 1-h break between magnetic resonance imaging (MRI) scanning, 23 healthy, right-handed volunteers experienced a fear extinction procedure, followed by Pavlovian fear conditioning that included partial reinforcement using mild electrical stimulation. We extracted the average time course of the BOLD signal from 245 regions of interest (ROIs) taken from the resting-state functional atlas. The variance of the BOLD signal and the Hurst exponent (H), which reflects the scale-free dynamic, were compared in the resting states before and after fear learning and fear memory extinction. After fear extinction, six ROIs showed a difference in H at the uncorrected level of significance, including areas associated with fear processing. H decreased during fear extinction but then became higher than before fear learning, specifically in areas related to the fear extinction network (FEN). However, activity in the other ROIs restored the H to its initial level. The variance of the BOLD signal in six ROIs demonstrated a significant increase from initial rest to the post-task rest. A limited number of ROIs showed changes in both H and variance. Our results imply that the variability and scale-free properties of the BOLD signal might serve as additional indicators of changes in spontaneous brain activity related to recent experience.

Highlights

  • In recent years, research on the human brain demonstrates an increasing interest to the dispersion and dynamic properties of brain activity than to its stationary values

  • During variance analysis of the signal, we found 91 areas that had a difference between the RS1 and RS2, but the changes passed false discovery rate (FDR) correction in only 7 regions of interest (ROIs) (Table 1 and Figure 2)

  • We assume that significant long-range temporal correlations (LRTC) changes in the fear extinction network (FEN) and task-related contrast (TRC) ROIs might have been missing due to that our study focused on the resting-state data and the corresponding preprocessing pipelines, while masks of the FEN and TRC ROIs were obtained in the task-based functional magnetic resonance imaging (fMRI) designs and preprocessing based more on the task-induced neural activity rather than neural efficiency

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Summary

Introduction

Research on the human brain demonstrates an increasing interest to the dispersion and dynamic properties of brain activity than to its stationary values. The variability of brain dynamics can be most described through the variance (σ2) of the blood oxygenation level-dependent (BOLD) signal. This variance provides additional information about the signal change in comparison to conventional measures as the averaged activity. Several works have shown strong associations of the BOLD signal variance with age (Garrett et al, 2011, 2013; Nomi et al, 2017), task performance (He, 2011; Garrett et al, 2012), and performance efficiency (Burzynska et al, 2015). The variance differs with mental diseases, including autism (Di Martino et al, 2014), Alzheimer’s disease (Zhao et al, 2015), and schizophrenia (Yu et al, 2014)

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