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Phase-amplitude coupling at the organism level: The amplitude of spontaneous alpha rhythm fluctuations varies with the phase of the infra-slow gastric basal rhythm

Authors :
Craig G. Richter
Catherine Tallon-Baudry
Mariana Babo-Rebelo
Denis Schwartz
Laboratoire de Neurosciences Cognitives & Computationnelles (LNC2)
Département d'Etudes Cognitives - ENS Paris (DEC)
École normale supérieure - Paris (ENS Paris)
Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-École normale supérieure - Paris (ENS Paris)
Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-Institut National de la Santé et de la Recherche Médicale (INSERM)
Ernst Strüngmann Institute for Neuroscience in Cooperation (ESI)
Max-Planck-Gesellschaft
Institut du Cerveau et de la Moëlle Epinière = Brain and Spine Institute (ICM)
Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-Centre National de la Recherche Scientifique (CNRS)-CHU Pitié-Salpêtrière [AP-HP]
Sorbonne Université (SU)-Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Sorbonne Université (SU)-Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)
École normale supérieure - Paris (ENS-PSL)
Université Paris sciences et lettres (PSL)-Université Paris sciences et lettres (PSL)-École normale supérieure - Paris (ENS-PSL)
Université Pierre et Marie Curie - Paris 6 (UPMC)-Institut National de la Santé et de la Recherche Médicale (INSERM)-CHU Pitié-Salpêtrière [AP-HP]
Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Sorbonne Université (SU)-Assistance publique - Hôpitaux de Paris (AP-HP) (AP-HP)-Sorbonne Université (SU)-Centre National de la Recherche Scientifique (CNRS)
HAL-UPMC, Gestionnaire
Source :
Frontiers in Neuroscience, NeuroImage, NeuroImage, Elsevier, 2016, ⟨10.1016/j.neuroimage.2016.08.043⟩, Neuroimage, NeuroImage, 2016, ⟨10.1016/j.neuroimage.2016.08.043⟩, Europe PubMed Central
Publication Year :
2016

Abstract

A fundamental feature of the temporal organization of neural activity is phase-amplitude coupling between brain rhythms at different frequencies, where the amplitude of a higher frequency varies according to the phase of a lower frequency. Here, we show that this rule extends to brain-organ interactions. We measured both the infra-slow (~0.05 Hz) rhythm intrinsically generated by the stomach – the gastric basal rhythm – using electrogastrography, and spontaneous brain dynamics with magnetoencephalography during resting-state with eyes open. We found significant phase-amplitude coupling between the infra-slow gastric phase and the amplitude of the cortical alpha rhythm (10–11 Hz), with gastric phase accounting for 8% of the variance of alpha rhythm amplitude fluctuations. Gastric-alpha coupling was localized to the right anterior insula, and bilaterally to occipito-parietal regions. Transfer entropy, a measure of directionality of information transfer, indicates that gastric-alpha coupling is due to an ascending influence from the stomach to both the right anterior insula and occipito-parietal regions. Our results show that phase-amplitude coupling so far only observed within the brain extends to brain-viscera interactions. They further reveal that the temporal structure of spontaneous brain activity depends not only on neuron and network properties endogenous to the brain, but also on the slow electrical rhythm generated by the stomach.<br />Highlights • Spontaneous alpha rhythm fluctuations locked to gastric phase. • Gastric phase explains 8% of alpha variance. • Gastric-alpha coupling mostly to due to ascending influences from stomach to brain. • The stomach as an external oscillator constraining spontaneous brain activity.

Details

ISSN :
10959572 and 10538119
Volume :
146
Database :
OpenAIRE
Journal :
NeuroImage
Accession number :
edsair.doi.dedup.....35b2f337fa55b42adb15af6095808d3b
Full Text :
https://doi.org/10.1016/j.neuroimage.2016.08.043⟩