Phase-locking of resting-state brain networks with the gastric basal electrical rhythm

Kimberly R Smith,Martin A Lindquist,Brian S Caffo,James J Pekar,Hamed Honari,Bohao Tang,Tyler Davis,Ann S Choe

doi:10.1371/journal.pone.0244756

Kimberly R Smith, Martin A Lindquist + Show 6 more

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https://doi.org/10.1371/journal.pone.0244756

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Journal: PLOS ONE	Publication Date: Jan 5, 2021
Citations: 15	License type: CC BY 4.0

Affiliation: Johns Hopkins University, Kennedy Krieger Institute

Abstract

A network of myenteric interstitial cells of Cajal in the corpus of the stomach serves as its “pacemaker”, continuously generating a ca 0.05 Hz electrical slow wave, which is transmitted to the brain chiefly by vagal afferents. A recent study combining resting-state functional MRI (rsfMRI) with concurrent surface electrogastrography (EGG), with cutaneous electrodes placed on the epigastrium, found 12 brain regions with activity that was significantly phase-locked with this gastric basal electrical rhythm. Therefore, we asked whether fluctuations in brain resting state networks (RSNs), estimated using a spatial independent component analysis (ICA) approach, might be synchronized with the stomach. In the present study, in order to determine whether any RSNs are phase-locked with the gastric rhythm, an individual participant underwent 22 scanning sessions; in each, two 15-minute runs of concurrent EGG and rsfMRI data were acquired. EGG data from three sessions had weak gastric signals and were excluded; the other 19 sessions yielded a total of 9.5 hours of data. The rsfMRI data were analyzed using group ICA; RSN time courses were estimated; for each run, the phase-locking value (PLV) was computed between each RSN and the gastric signal. To assess statistical significance, PLVs from all pairs of “mismatched” data (EGG and rsfMRI data acquired on different days) were used as surrogate data to generate a null distribution for each RSN. Of a total of 18 RSNs, three were found to be significantly phase-locked with the basal gastric rhythm, namely, a cerebellar network, a dorsal somatosensory-motor network, and a default mode network. Disruptions to the gut-brain axis, which sustains interoceptive feedback between the central nervous system and the viscera, are thought to be involved in various disorders; manifestation of the infra-slow rhythm of the stomach in brain rsfMRI data could be useful for studies in clinical populations.

Highlights

A network of myenteric interstitial cells of Cajal in the corpus of the stomach serve as its “pacemaker”, constantly and intrinsically generating a ca 0.05 Hz electrical slow wave, which governs gastric peristalsis when there is food or chyme in the stomach, and which is transmitted to the brain by vagal afferents [1,2,3,4]
A recent study [5] combining resting-state functional MRI with concurrent surface electrogastrography (EGG), in which signals are recorded from cutaneous electrodes on the epigastrium, reported that brain activity in 12 regions including somato-motor cortices, dorsal precuneus, and the extrastriate body area was significantly phase-locked to the basal gastric rhythm
Comparing the matched and mismatched phase-locking value (PLV) distributions, we found that three brain networks were significantly phaselocked to the basal gastric rhythm: a cerebellar network (FDR-adjusted p-value = 0.0022), a dorsal somatosensory-motor network, and a default mode network

Summary

Introduction

A network of myenteric interstitial cells of Cajal in the corpus of the stomach serve as its “pacemaker”, constantly and intrinsically generating a ca 0.05 Hz electrical slow wave, which governs gastric peristalsis when there is food or chyme in the stomach, and which is transmitted to the brain by vagal afferents [1,2,3,4]. A recent study [5] combining resting-state functional MRI (rsfMRI) with concurrent surface electrogastrography (EGG), in which signals are recorded from cutaneous electrodes on the epigastrium (abdominal skin over the stomach), reported that brain activity in 12 regions including somato-motor cortices, dorsal precuneus, and the extrastriate body area was significantly phase-locked to the basal gastric rhythm. This collection of 12 gastric-synchronized regions, or nodes, was dubbed the gastric network, and it was suggested that time lags of several seconds between nodes were responsible for this “delayed connectivity network” not having been previously detected.

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