Low-frequency electrical waves in the stomach seem to be synchronised with the activity of a newly discovered resting-state network in the human brain

Aglioti, Salvatore Maria

Monti, Alessandro

Porciello, Giuseppina

eLife

English

Low-frequency electrical waves in the stomach seem to be synchronised with the activity of a newly discovered resting-state network in the human brain.</jats:p

Giuseppina Porciello

Alessandro Monti

Salvatore Maria Aglioti

Crossref

How the stomach and the brain work together at rest

Archivio della ricerca- Università di Roma La Sapienza

THE GASTRIC NETWORKHow the stomach and the brainwork together at restLow-frequency electrical waves in the stomach seem to be synchronisedwith the activity of a newly discovered resting-state network in thehuman brain.GIUSEPPINA PORCIELLO, ALESSANDRO MONTI AND SALVATORE MARIA AGLIOTIThe brain is always active – even when it isat rest, it receives a continuous stream ofinformation from other areas of thebody. From gut feelings to heartbeats, this infor-mation is constantly monitored to maintain astate of physiological equilibrium known ashomeostasis. Signals from the body, includingthe stomach, also influence a variety of mentalprocesses and complex human behaviours(Critchley and Harrison, 2013; Herbert andPollatos, 2012; Porciello et al., 2018).Although the anatomy of the homeostatic neuralpathway is relatively well known (Craig, 2003),its physiology is less well understood.During periods of wakeful rest, our brain gen-erates its own spontaneous and synchronisedactivity within different groups of brain regions(known as resting-state networks). On the otherhand, specialised cells in the stomach produce aslow, continuous pattern of electrical impulsesthat set the pace of stomach contractions duringdigestion. But the stomach also generates thesesignals when it is empty, which suggests thatthey may have another purpose. Now, in eLife,Ignacio Rebollo of the PSL Research Universityand co-workers – Anne-Dominique Devauchelle,Benoıˆt Be´ranger, and Catherine Tallon-Baudry –report how they have combined two techniques,functional magnetic resonance imaging andelectrogastrography, to shed new light on theinteractions between the brain and the stomach(Rebollo et al., 2018).Rebollo et al. placed electrodes on the abdo-men of volunteers as they lay inside a brain scan-ner and analysed the coupling between thesignals from the stomach and the brain using amethod called phase-locking value analysis. Theresearchers discovered a new resting-state net-work – the gastric network – which fired in syn-chrony with the rhythm of the stomach(Figure 1A). Furthermore, the various brainregions within this network showed a delayedfunctional connectivity between each other.Although the role of the gastric networkremains unknown, Rebollo et al. reasoned thatsome of the brain regions within the networkmap information about vision, touch and move-ment in bodily coordinates. Thus, they advancedthe tantalising hypothesis that this network coor-dinates different ‘body-centred maps’ in thebrain. According to this, a region in the brainknown as the insula should be strongly involvedin the gastric network: this region receives directinput from the internal organs (e.g. stomach,intestine), which is integrated to create a coher-ent representation of the whole body(Critchley and Harrison, 2013; Craig, 2009).However, Rebollo et al. found that the insulawas only marginally synchronised to the rhythmof the stomach.Copyright Porciello et al. Thisarticle is distributed under the termsof the Creative Commons AttributionLicense, which permits unrestricteduse and redistribution provided thatthe original author and source arecredited.Related research article Rebollo I, Devau-chelle AD, Be´ranger B, Tallon-Baudry C.2018. Stomach-brain synchrony reveals anovel, delayed-connectivity resting-statenetwork in humans. eLife 7:e33321. DOI:10.7554/eLife.33321Porciello et al. eLife 2018;7:e37009. DOI: https://doi.org/10.7554/eLife.37009 1 of 3INSIGHTThus, we suggest that the gastric networkmay rather act as a homeostatic regulator offood intake. Indeed, it neatly overlaps with areasprocessing information from the face, mouthand hands, and with three brain regions acti-vated by tongue- or hand-related actions(Amiez and Petrides, 2014). We speculate thatthe insula would play a bigger role in the net-work if at least one of the following applied: thefasting happened over a longer period; the par-ticipants had to complete tasks that made themfocus on their own gut feelings (interoceptivetasks); the participants attached a higher emo-tional value to food, either as a source of rewardor disgust, as happens in people with eating dis-orders such as anorexia or bulimia nervosa(Figure 1B).Due to the limitations of the phase-lockingmethod (Lachaux et al., 1999), it remainsunclear if the rhythmic interaction between thestomach and the brain is one-directional or two-directional. Clarifying this issue and measuringthe stomach-brain coupling during conditions inwhich the body is far from homeostasis, and dur-ing interoceptive or emotional tasks, may helpto shed light on the true functional role of thegastric network. We believe that the findings ofRebollo et al. not only open new avenues toimproving our understanding of the resting-stateactivity, but also fire up an exciting debate onhow signals from the enteric nervous system inthe gut could shape the brain.Giuseppina Porciello is in the Department ofPsychology, Sapienza University of Rome, Italy and theIRCCS Santa Lucia Foundation, Rome, Italyhttps://orcid.org/0000-0001-8374-5320Alessandro Monti is in the Department of Psychology,Sapienza University of Rome, Italy and the IRCCSSanta Lucia Foundation, Rome, Italyhttps://orcid.org/0000-0002-2818-0563Salvatore Maria Aglioti is in the Department ofPsychology, Sapienza University of Rome, Italy and theIRCCS Santa Lucia Foundation, Rome, Italysalvatoremaria.aglioti@uniroma1.ithttps://orcid.org/0000-0001-8175-7563Competing interests: The authors declare that nocompeting interests exist.Published 04 May 2018ReferencesAmiez C, Petrides M. 2014. Neuroimaging evidence ofthe anatomo-functional organization of the humancingulate motor areas. Cerebral Cortex 24:563–578.DOI: https://doi.org/10.1093/cercor/bhs329,PMID: 23131805Craig AD. 2003. Interoception: the sense of thephysiological condition of the body. Current Opinionin Neurobiology 13:500–505. DOI: https://doi.org/10.1016/S0959-4388(03)00090-4, PMID: 12965300Craig AD. 2009. How do you feel–now? The anteriorinsula and human awareness. Nature ReviewsNeuroscience 10:59–70. DOI: https://doi.org/10.1038/nrn2555, PMID: 19096369Critchley HD, Harrison NA. 2013. Visceral influenceson brain and behavior. Neuron 77:624–638.DOI: https://doi.org/10.1016/j.neuron.2013.02.008,PMID: 23439117Herbert BM, Pollatos O. 2012. The body in the mind:on the relationship between interoception andembodiment. Topics in Cognitive Science 4:692–704.Figure 1. Coupling between the activity of the brain and the stomach. (A) When the body is at rest, Rebollo et al.found that the blood flow in the brain (as measured by functional magnetic resonance imaging; blue wave) andthe electrical activity in the stomach (as measured by electrogastrography; red wave) are in delayed sync with eachother (Rebollo et al., 2018). (B) Rebollo et al. discovered that the insula (green) was only marginally coupled withthe stomach. We think that the activity of this region (green wave) will be more synchronous with that of thestomach when certain conditions are met (see main text).Porciello et al. eLife 2018;7:e37009. DOI: https://doi.org/10.7554/eLife.37009 2 of 3Insight The Gastric Network How the stomach and the brain work together at restDOI: https://doi.org/10.1111/j.1756-8765.2012.01189.x, PMID: 22389201Lachaux JP, Rodriguez E, Martinerie J, Varela FJ.1999. Measuring phase synchrony in brain signals.Human Brain Mapping 8:194–208. DOI: https://doi.org/10.1002/(SICI)1097-0193(1999)8:4<194::AID-HBM4>3.0.CO;2-C, PMID: 10619414Porciello G, Bufalari I, Minio-Paluello I, Di Pace E,Aglioti SM. 2018. The ’Enfacement’ illusion: a windowon the plasticity of the self. Cortex:S0010-9452(18)30020-0. DOI: https://doi.org/10.1016/j.cortex.2018.01.007, PMID: 29478669Rebollo I, Devauchelle AD, Be´ranger B, Tallon-BaudryC. 2018. Stomach-brain synchrony reveals a novel,delayed-connectivity resting-state network in humans.eLife 7:e33321. DOI: https://doi.org/10.7554/eLife.33321, PMID: 29561263Porciello et al. eLife 2018;7:e37009. DOI: https://doi.org/10.7554/eLife.37009 3 of 3Insight The Gastric Network How the stomach and the brain work together at rest

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How the stomach and the brain work together at rest

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