Probing fMRI brain connectivity and activity changes during emotion regulation by EEG neurofeedback

Abstract

Despite the existence of several emotion regulation studies using neurofeedback, interactions among a small number of regions were evaluated, and therefore, further investigation is needed to understand the interactions of the brain regions involved in emotion regulation. We implemented electroencephalography (EEG) neurofeedback with simultaneous functional magnetic resonance imaging (fMRI) using a modified happiness-inducing task through autobiographical memories to upregulate positive emotion. Then, an explorative analysis of whole brain regions was done to understand the effect of neurofeedback on brain activity and the interaction of whole brain regions involved in emotion regulation. The participants in the control and experimental groups were asked to do emotion regulation while viewing positive images of autobiographical memories and getting sham or real (based on alpha asymmetry) EEG neurofeedback, respectively. The proposed multimodal approach quantified the effects of EEG neurofeedback in changing EEG alpha power, fMRI blood oxygenation level-dependent (BOLD) activity of prefrontal, occipital, parietal, and limbic regions (up to 1.9% increase), and functional connectivity in/between prefrontal, parietal, limbic system, and insula in the experimental group. New connectivity links were identified by comparing the brain functional connectivity between experimental conditions (Upregulation and View blocks) and also by comparing the brain connectivity of the experimental and control groups. Psychometric assessments confirmed significant changes in positive and negative mood states in the experimental group by neurofeedback. Based on the exploratory analysis of activity and connectivity among all brain regions involved in emotion regions, we found significant BOLD and functional connectivity increases due to EEG neurofeedback in the experimental group, but no learning effect was observed in the control group. The results reveal several new connections among brain regions as a result of EEG neurofeedback which can be justified according to emotion regulation models and the role of those regions in emotion regulation and recalling positive autobiographical memories.

Keywords: autobiographical memory; emotion regulation; frontal asymmetry; functional connectivity; neurofeedback; simultaneous recording of EEG and fMRI.

FIGURE 1

Neurofeedback bar and timing of the tasks used in the one run of neurofeedback protocol, which contains Rest, View, and Upregulation blocks.

FIGURE 2

(A) Scatter plot of frontal asymmetry in blocks of View and Upregulation versus Rest for the experimental group. (B) Boxplot of frontal asymmetry in blocks of Rest, View, and Upregulation for the experimental and control groups. (C) Boxplot of frontal asymmetry for Upregulation versus View and Rest in the experimental and control groups.

FIGURE 3

(A) Activation map for Upregulation versus View in the experimental group (p_corrected = 0.01), (B) activation map masked by amygdala.

FIGURE 4

Normalized fMRI BOLD signal in the Rest, View, and Upregulation blocks for contrast of Upregulation versus View and Rest for the experimental and experimental groups in panel (A) left amygdala and p-value _{Upregulation–View (Experimental group–Control group) for left amygdala} = 2.4 × 10^{– 3}; p-value _{Upregulation–Rest (Experimental group–Control group) for left amygdala} = 1.3 × 10^{– 4}, (B) left insula and p-value _{Upregulation–View (Experimental group–Control group) for left Insula} = 3.6 × 10^{– 5}; p-value _{Upregulation–Rest (Experimental group–Control group) for left Insula} = 5.9 × 10^{– 4}, and (C) left orbitofrontal cortex and p-value _{Upregulation–View (Experimental group–Control group) for left OFC} = 6.8 × 10^{– 3}; p-value _{Upregulation–Rest (Experimental group–Control group) for left OFC} = 1.5 × 10^{– 5} (*indicates p < 0.05 and n.s. indicates not significant).

FIGURE 5

Significant edges of differential connectivity networks which show network links with significant changes between the Upregulation and View blocks for panel (A) sagittal, (B) axial, and (C) coronal layout. L, left; R, right; Amyg, amygdala; ThaL, thalamus; Ins, insula; OFC, orbitofrontal cortex; VS, ventral striatum; DMPFC, dorsomedial prefrontal cortex; VLPFC, ventrolateral prefrontal cortex; PC, postcentral.

FIGURE 6

Functional connectivity distribution of Upregulation and View blocks for significant connections in the experimental group.