Variance and Scale-Free Properties of Resting-State Blood Oxygenation Level-Dependent Signal After Fear Memory Acquisition and Extinction

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.

Decreased long‐range temporal correlations in the resting‐state functional magnetic resonance imaging blood‐oxygen‐level‐dependent signal reflect motor sequence learning up to 2 weeks following training

“…Similarly, Barnes et al ( 2009 ) observed lower LRTC during cognitive performance that was followed by recovery to baseline levels ~15 min after completing the task. These and similar studies have proposed that there are baseline levels of self‐similarity that are temporarily disturbed by active tasks /cognitive effort (Barnes et al, 2009 ; Churchill et al, 2016 ; Tetereva et al, 2020 ; Wenger et al, 2017 ). Other studies have reported that increased LRTC in resting state data is reflective of prior task performance (Mahjoory et al, 2019 ; Samek et al, 2016 ; Wink et al, 2006 ).…”

The Laplacian eigenmaps dimensionality reduction of fMRI data for discovering stimulus-induced changes in the resting-state brain activity

“…We analyzed resting-state fMRI data of 23 healthy right-handed volunteers (23.90 ± 3.93 years old, 8 females) who participated in the study of longitudinal changes in the brain RS functional connectivity such as RS after fear learning and fear memory extinction (RS_FE) in comparison with the initial RS data (RS_0). These data were already used in the previous projects 28 .…”

“…During the RS scanning, participants were asked to remain calm with their eyes closed and to try not to think purposefully. A full description of the experimental procedure can be found in our previous paper 28 . In the current study, we concentrated on analyzing RS1 and RS2 interleaved by FL and FE to separate two RS scan data acquired before and after exposure to emotionally meaningful stimuli.…”