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
Open accessAbstract
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 (~0.05Hz) 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 (10-11Hz), 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.
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In humans, part of the coupling observed corresponds to information flowing from stomach to brain.
“but in humans part of the coupling observed corresponds information flowing from stomach to brain 183 .”
From Interoceptive rhythms in the brain (2023) · cites this paper as [183]
Interoceptive mechanisms influence adaptive and maladaptive motivational decisions and have implications for preventing and managing clinical disorders.
“Detailed understanding of these mechanisms is important given their influence on adaptive [16] and maladaptive [51 ] motivational decisions and their implications for preventing and managing clinical disorders [19 ,20 ,21 ,34,41, 42,46,50 ].”
From Interoception and emotion. (2017) · cites this paper as [16]
The Results section (‘Directionality of interactions between stomach and brain’) reports information transfer from gastric rhythm to brain activity, but does not address motivational decisions. Searches for adaptive or maladaptive decisions and for prevention or management of clinical disorders found no passage making those claims in our copy. (LLM, conf=0.76)
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Nonparametric statistical testing of EEG- and MEG-data
Maris, E., & Oostenveld, R. (2007) · Journal of Neuroscience Methods · doi:10.1016/j.jneumeth.2007.03.024 · Cited by 8,496 · see citing works
Visceral influences on brain and behavior
Critchley, H. D., & Harrison, N. A. (2013) · Neuron · doi:10.1016/j.neuron.2013.02.008 · Cited by 1,177 · cited 5× · see citing works
“Contents lists available at ScienceDirect NeuroImage http://d 1053-81 n Corr E-m catherin journal homepage: www.elsevier.com/locate/neuroimage 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 Craig G. Ric…”
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The Embodiment of Emotional Feelings in the Brain
Harrison, N. A., Gray, M. A., Gianaros, P. J., & Critchley, H. D. (2010) · The Journal of Neuroscience · doi:10.1523/jneurosci.1725-10.2010 · Cited by 250 · see citing works
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Babo-Rebelo, M., Richter, C. G., & Tallon-Baudry, C. (2016) · The Journal of Neuroscience · doi:10.1523/jneurosci.0262-16.2016 · Cited by 207 · see citing works
Self-citationFlorin, E., & Baillet, S. (2015) · NeuroImage · doi:10.1016/j.neuroimage.2015.01.054 · Cited by 184 · see citing works
Roux, F., Wibral, M., Singer, W., Aru, J., & Uhlhaas, P. J. (2013) · The Journal of Neuroscience · doi:10.1523/jneurosci.5778-12.2013 · Cited by 169 · see citing works
THE ACTION POTENTIALS OF THE STOMACH
Bozler, E. (1945) · American Journal of Physiology-Legacy Content · doi:10.1152/ajplegacy.1945.144.5.693 · Cited by 88 · see citing works
Flagged first, then by citations
Research works printed but not linked: 52
- Babo-Rebelo M., Wolpert N., Adam C., Hasboun D., Tallon-Baudry C., 2016. Is the cardiac monitoring function related to the self in both the default-network and right anterior insula? Phil. Trans. Roy. Soc. B. (in press). PMC5062094 28080963
- Bahramisharif A. van Gerven M.A. Aarnoutse E.J. Mercier M.R. Schwartz T.H. Foxe J.J. Ramsey N.F. Jensen O. Propagating neocortical gamma bursts are coordinated by traveling alpha waves J. Neurosci. 33 2013 18849 18854 24285891 PMC4262700
- Birren J.E. Phillips S.L. Cardon P.V. Reaction time as a function of cardiac cycle in young adults Science 140 1963 195 196 13971178
- Birn R.M. Diamond J.B. Smith M.A. Bandettini P.A. Separating respiratory-variation-related fluctuations from neuronal-activity-related fluctuations in fMRI Neuroimage 31 2006 1536 1548 16632379
- Bragin A. Jando G. Nadasdy Z. Hetke J. Wise K. Buzsaki G. Gamma (40–100 Hz) oscillation in the Hippocampus of the behaving Rat J. Neurosci. 15 1995 47 60 7823151 PMC6578273
- Buzsaki G. Neural syntax: cell assemblies, synapsembles, and readers Neuron 68 2010 362 385 21040841 PMC3005627
- Buzsaki G. Draguhn A. Neuronal oscillations in cortical networks Science 304 2004 1926 1929 15218136
- Canolty R.T. Edwards E. Dalal S.S. Soltani M. Nagarajan S.S. Kirsch H.E. Berger M.S. Barbaro N.M. Knight R.T. High gamma power is phase-locked to theta oscillations in human neocortex Science 313 2006 1626 1628 16973878 PMC2628289
- Chen J.D. Zou X. Lin X. Ouyang S. Liang J. Detection of gastric slow wave propagation from the cutaneous electrogastrogram Am J Physiol 277 1999 424 430 10444457
- Deco G. Jirsa V. McIntosh A.R. Sporns O. Kotter R. Key role of coupling, delay, and noise in resting brain fluctuations Proc. Natl. Acad. Sci. USA 106 2009 10302 10307 19497858 PMC2690605
- Dirlich G. Vogl L. Plaschke M. Strian F. Cardiac field effects on the EEG Electroencephalogr. Clin. Neurophysiol. 102 1997 307 315 9146492
- Elliott R. Graf V. Visual sensitivity as a function of phase of cardiac cycle Psychophysiology 9 1972 357 361 5034123
- Furness J.B. Rivera L.R. Cho H.J. Bravo D.M. Callaghan B. The gut as a sensory organ Nat. Rev. Gastroenterol. Hepatol. 10 2013 729 740 24061204
- Glover G.H. Li T.Q. Ress D. Image-based method for retrospective correction of physiological motion effects in fMRI: RETROICOR Magn. Reson. Med. 44 2000 162 167 10893535
- Gray M.A. Rylander K. Harrison N.A. Wallin B.G. Critchley H.D. Following one's heart: cardiac rhythms gate central initiation of sympathetic reflexes J. Neurosci. 29 2009 1817 1825 19211888 PMC2869038
- Haegens S. Nacher V. Luna R. Romo R. Jensen O. alpha-Oscillations in the monkey sensorimotor network influence discrimination performance by rhythmical inhibition of neuronal spiking Proc. Natl. Acad. Sci. USA 108 2011 19377 19382 22084106 PMC3228466
- Hyafil A. Giraud A.L. Fontolan L. Gutkin B. Neural cross-frequency coupling: connecting architectures, mechanisms, and functions Trends Neurosci. 38 2015 725 740 26549886
- Ito S. Visceral region in the rat primary somatosensory cortex identified by vagal evoked potential J. Comp. Neurol. 444 2002 10 24 11835179
- Jensen O. Mazaheri A. Shaping functional architecture by oscillatory alpha activity: gating by inhibition Front. Hum. Neurosci. 4 2010 186 21119777 PMC2990626
- Kern M. Aertsen A. Schulze-Bonhage A. Ball T. Heart cycle-related effects on event-related potentials, spectral power changes, and connectivity patterns in the human ECoG Neuroimage 81C 2013 178 190 23684883
- Klimesch W. alpha-band oscillations, attention, and controlled access to stored information Trends Cogn. Sci. 16 2012 606 617 23141428 PMC3507158
- Koch K.L. Stern R.M. Handbook of Electrogastrography 2004 Oxford University Press Oxford
- Lindner M. Vicente R. Priesemann V. Wibral M. TRENTOOL: a Matlab open source toolbox to analyse information flow in time series data with transfer entropy BMC Neurosci. 12 2011 119 22098775 PMC3287134
- Mayer E.A. Gut feelings: the emerging biology of gut-brain communication Nat. Rev. Neurosci. 12 2011 453 466 21750565 PMC3845678
- Mayer E.A. Aziz Q. Coen S. Kern M. Labus J.S. Lane R. Kuo B. Naliboff B. Tracey I. Brain imaging approaches to the study of functional GI disorders: a Rome working team report Neurogastroenterol. Motil 21 2009 579 596 19646070 PMC3829384
- Monto S. Palva S. Voipio J. Palva J.M. Very slow EEG fluctuations predict the dynamics of stimulus detection and oscillation amplitudes in humans J. Neurosci. 28 2008 8268 8272 18701689 PMC6670577
- Murphy K. Birn R.M. Bandettini P.A. Resting-state fMRI confounds and cleanup Neuroimage 80 2013 349 359 23571418 PMC3720818
- Oostenveld R. Fries P. Maris E. Schoffelen J.M. FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data Comput. Intell. Neurosci. 2011 2011 156869 21253357 PMC3021840
- Osipova D. Hermes D. Jensen O. Gamma power is phase-locked to posterior alpha activity PLoS One 3 2008 e3990 19098986 PMC2602598
- Palva J.M. Palva S. Kaila K. Phase synchrony among neuronal oscillations in the human cortex J. Neurosci. 25 2005 3962 3972 15829648 PMC6724920
- Palva S. Palva J.M. New vistas for alpha-frequency band oscillations Trends Neurosci. 30 2007 150 158 17307258
- Park H.D. Correia S. Ducorps A. Tallon-Baudry C. Spontaneous fluctuations in neural responses to heartbeats predict visual detection Nat. Neurosci. 17 2014 612 618 24609466
- Petersen C.C. Sporns O. Brain networks and cognitive architectures Neuron 88 2015 207 219 26447582 PMC4598639
- Pigarev I. Almirall H. Pigareva M.L. Bautista V. Sanchez-Bahillo A. Barcia C. Herrero M.T. Visceral signals reach visual cortex during slow wave sleep: study in monkeys Acta Neurobiol. Exp. 66 2006 69 73 16617678
- Pigarev I.N. Neurons of visual cortex respond to visceral stimulation during slow wave sleep Neuroscience 62 1994 1237 1243 7845596
- Ponce-Alvarez A. Deco G. Hagmann P. Romani G.L. Mantini D. Corbetta M. Resting-state temporal synchronization networks emerge from connectivity topology and heterogeneity PLoS Comput. Biol. 11 2015 e1004100 25692996 PMC4333573
- Powley T.L. Phillips R.J. Vagal intramuscular array afferents form complexes with interstitial cells of Cajal in gastrointestinal smooth muscle: analogues of muscle spindle organs? Neuroscience 186 2011 188 200 21530617 PMC3110524
- Ragwitz M. Kantz H. Markov models from data by simple nonlinear time series predictors in delay embedding spaces Phys. Rev. E Stat. Nonlin. Soft Matter Phys. 65 2002 056201 12059674
- Riezzo G. Russo F. Indrio F. Electrogastrography in adults and children: the strength, pitfalls, and clinical significance of the cutaneous recording of the gastric electrical activity Biomed. Res. Int. 2013 2013 282757 23762836 PMC3677658
- Salmelin R. Hari R. Characterization of spontaneous MEG rhythms in healthy adults Electroencephalogr. Clin. Neurophysiol. 91 1994 237 248 7523073
- Sanders K.M. Koh S.D. Ward S.M. Interstitial cells of Cajal as pacemakers in the gastrointestinal tract Annu. Rev. Physiol. 68 2006 307 343 16460275
- Sanders K.M. Ward S.M. Koh S.D. Interstitial cells: regulators of smooth muscle function Physiol. Rev. 94 2014 859 907 24987007 PMC4152167
- Schandry R. Montoya P. Event-related brain potentials and the processing of cardiac activity Biol. Psychol. 42 1996 75 85 8770371
- Schroeder C.E. Lakatos P. Low-frequency neuronal oscillations as instruments of sensory selection Trends Neurosci. 32 2009 9 18 19012975 PMC2990947
- Shmueli K. van Gelderen P. de Zwart J.A. Horovitz S.G. Fukunaga M. Jansma J.M. Duyn J.H. Low-frequency fluctuations in the cardiac rate as a source of variance in the resting-state fMRI BOLD signal Neuroimage 38 2007 306 320 17869543 PMC2128785
- Suzuki N. Prosser C.L. Dahms V. Boundary cells between longitudinal and circular layers - essential for electrical slow waves in cat intestine Am. J. Physiol. 250 1986 G287 G294 3953815
- Tort A.B. Komorowski R. Eichenbaum H. Kopell N. Measuring phase-amplitude coupling between neuronal oscillations of different frequencies J. Neurophysiol. 104 2010 1195 1210 20463205 PMC2941206
- Tzourio-Mazoyer N. Landeau B. Papathanassiou D. Crivello F. Etard O. Delcroix N. Mazoyer B. Joliot M. Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain Neuroimage 15 2002 273 289 11771995
- van Oudenhove L. Vandenberghe J. Dupont P. Geeraerts B. Vos R. Bormans G. van Laere K. Fischler B. Demyttenaere K. Janssens J. Tack J. Cortical deactivations during gastric fundus distension in health: visceral pain-specific response or attenuation of 'default mode' brain function? A H2 15O-PET study Neurogastroenterol. Motil. 21 2009 259 271 19019011
- Vicente R. Wibral M. Lindner M. Pipa G. Transfer entropy--a model-free measure of effective connectivity for the neurosciences J. Comput. Neurosci. 30 2011 45 67 20706781 PMC3040354
- Vinck M. van Wingerden M. Womelsdorf T. Fries P. Pennartz C.M. The pairwise phase consistency: a bias-free measure of rhythmic neuronal synchronization Neuroimage 51 2010 112 122 20114076
- Weaver K.E. Wander J.D. Ko A.L. Casimo K. Grabowski T.J. Ojemann J.G. Darvas F. Directional patterns of cross frequency phase and amplitude coupling within the resting state mimic patterns of fMRI functional connectivity Neuroimage 128 2016 238 251 26747745 PMC4762762
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- Authors
- Richter, C. G., Babo-Rebelo, M., Schwartz, D., & Tallon-Baudry, C.
- Affiliations
- Max Planck Society (DE)
- Inserm (FR)
- Centre National de la Recherche Scientifique (FR)
- Corresponding author
- Richter, Craig G.
- Venue
- NeuroImage
- Publisher
- Elsevier BV
- Published
- 2017-02
- Volume
- 146
- Pages
- 951-958
- ISSN
- 1053-8119 (ISSN-L)
- PMC
- PMC5312779
- OpenAlex
- W2517088698
- Cited by
- 151
- References
- 8
- Citations by year
- 2026: 16 · 2025: 15 · 2024: 17 · 2023: 14 · 2022: 24 · 2021: 16 · 2020: 10 · 2019: 15 · 2018: 13 · 2017: 11
- FWCI
- 8.27
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- NeuroImage (publishedVersion, cc-by-nc-nd)
- PubMed Central (publishedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- HAL (submittedVersion, cc-by-nc-nd)
- UCL Discovery (University College London) (submittedVersion)
- Max Planck Digital Library (submittedVersion)
- MPG.PuRe (Max Planck Society) (submittedVersion)
- Funders
- Agence Nationale de la Recherche (ANR-10-IDEX-0001-02 PSL, ANR-BLAN-BSH2-0002-01)
- European Research Council
- Topics
- Life Sciences › Neuroscience › Cognitive Neuroscience › Neural dynamics and brain function
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Heart Rate Variability and Autonomic Control
- Life Sciences › Neuroscience › Cognitive Neuroscience › Functional Brain Connectivity Studies
- Keywords
- phase-amplitude coupling, alpha rhythm, electrogastrography, anterior insula, parieto-occipital cortex, transfer entropy, spontaneous brain activity, resting state
- MeSH terms
- Adult, Alpha Rhythm, Brain, Female, Humans, Male, Neural Pathways, Stomach, Magnetoencephalography, Young Adult
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