Graph neural fields: A framework for spatiotemporal dynamical models on the human connectome.

Marco Aqil, Selen Atasoy, Morten L Kringelbach, Rikkert Hindriks
Author Information
  1. Marco Aqil: Department of Mathematics, Vrije Universiteit, Amsterdam, The Netherlands. ORCID
  2. Selen Atasoy: Centre for Eudaimonia and Human Flourishing, University of Oxford, Oxford, United Kingdom. ORCID
  3. Morten L Kringelbach: Centre for Eudaimonia and Human Flourishing, University of Oxford, Oxford, United Kingdom.
  4. Rikkert Hindriks: Department of Mathematics, Vrije Universiteit, Amsterdam, The Netherlands. ORCID

Abstract

Tools from the field of graph signal processing, in particular the graph Laplacian operator, have recently been successfully applied to the investigation of structure-function relationships in the human brain. The eigenvectors of the human connectome graph Laplacian, dubbed "connectome harmonics", have been shown to relate to the functionally relevant resting-state networks. Whole-brain modelling of brain activity combines structural connectivity with local dynamical models to provide insight into the large-scale functional organization of the human brain. In this study, we employ the graph Laplacian and its properties to define and implement a large class of neural activity models directly on the human connectome. These models, consisting of systems of stochastic integrodifferential equations on graphs, are dubbed graph neural fields, in analogy with the well-established continuous neural fields. We obtain analytic predictions for harmonic and temporal power spectra, as well as functional connectivity and coherence matrices, of graph neural fields, with a technique dubbed CHAOSS (shorthand for Connectome-Harmonic Analysis Of Spatiotemporal Spectra). Combining graph neural fields with appropriate observation models allows for estimating model parameters from experimental data as obtained from electroencephalography (EEG), magnetoencephalography (MEG), or functional magnetic resonance imaging (fMRI). As an example application, we study a stochastic Wilson-Cowan graph neural field model on a high-resolution connectome graph constructed from diffusion tensor imaging (DTI) and structural MRI data. We show that the model equilibrium fluctuations can reproduce the empirically observed harmonic power spectrum of resting-state fMRI data, and predict its functional connectivity, with a high level of detail. Graph neural fields natively allow the inclusion of important features of cortical anatomy and fast computations of observable quantities for comparison with multimodal empirical data. They thus appear particularly suitable for modelling whole-brain activity at mesoscopic scales, and opening new potential avenues for connectome-graph-based investigations of structure-function relationships.

References

  1. Nat Commun. 2019 Mar 5;10(1):1056 [PMID: 30837462]
  2. Biol Cybern. 2005 Aug;93(2):91-108 [PMID: 16059785]
  3. Neuroimage. 2019 Feb 1;186:211-220 [PMID: 30399418]
  4. Proc Natl Acad Sci U S A. 2009 Jun 23;106(25):10302-7 [PMID: 19497858]
  5. Front Neuroinform. 2013 Jun 11;7:10 [PMID: 23781198]
  6. Neuroimage. 2020 Aug 1;216:116805 [PMID: 32335264]
  7. Theory Biosci. 2024 Mar 9;: [PMID: 38460025]
  8. Philos Trans A Math Phys Eng Sci. 2011 Oct 13;369(1952):3785-801 [PMID: 21893528]
  9. Prog Neurobiol. 2005 Sep-Oct;77(1-2):1-37 [PMID: 16289760]
  10. Nat Rev Neurosci. 2011 Jan;12(1):43-56 [PMID: 21170073]
  11. PLoS Comput Biol. 2017 Jun 22;13(6):e1005550 [PMID: 28640803]
  12. Neuroimage. 2020 Nov 1;221:117137 [PMID: 32652217]
  13. J Math Neurosci. 2015 Apr 08;5:9 [PMID: 25859420]
  14. J Math Neurosci. 2018 Feb 5;8(1):3 [PMID: 29399710]
  15. Nat Commun. 2019 Oct 18;10(1):4747 [PMID: 31628329]
  16. Neuroimage. 2016 Nov 15;142:135-149 [PMID: 27480624]
  17. Hum Brain Mapp. 2020 Aug 1;41(11):2980-2998 [PMID: 32202027]
  18. Neuroscientist. 2018 Jun;24(3):277-293 [PMID: 28863720]
  19. Neuroimage. 2015 May 1;111:385-430 [PMID: 25592995]
  20. J Neurophysiol. 2020 Feb 1;123(2):726-742 [PMID: 31774370]
  21. Brain Topogr. 2010 Jun;23(2):139-49 [PMID: 20364434]
  22. Trends Cogn Sci. 2018 Dec;22(12):1073-1075 [PMID: 30236490]
  23. Elife. 2019 May 07;8: [PMID: 31063127]
  24. Front Neurosci. 2020 Nov 10;14:577574 [PMID: 33240037]
  25. Sci Rep. 2017 Dec 15;7(1):17661 [PMID: 29247209]
  26. Network. 2002 Feb;13(1):67-113 [PMID: 11878285]
  27. ACS Chem Neurosci. 2018 Oct 17;9(10):2331-2343 [PMID: 29461039]
  28. Nat Commun. 2016 Jan 21;7:10340 [PMID: 26792267]
  29. PLoS Comput Biol. 2008 Aug 29;4(8):e1000092 [PMID: 18769680]
  30. Neuroimage. 2008 Jan 15;39(2):647-60 [PMID: 17977024]
  31. Curr Biol. 2018 Oct 8;28(19):3065-3074.e6 [PMID: 30270185]
  32. IEEE Trans Med Imaging. 2013 Oct;32(10):1952-63 [PMID: 23807436]
  33. Kybernetik. 1973 Sep;13(2):55-80 [PMID: 4767470]
  34. Neuroimage. 2013 Dec;83:704-25 [PMID: 23774395]
  35. Proc Natl Acad Sci U S A. 2006 Sep 12;103(37):13848-53 [PMID: 16945915]
  36. Neuroimage. 2011 Jun 1;56(3):1043-58 [PMID: 21329758]
  37. Neuropsychopharmacology. 2017 Oct;42(11):2114-2127 [PMID: 28447622]
  38. Nat Neurosci. 2017 Feb 23;20(3):340-352 [PMID: 28230845]
  39. Sci Rep. 2020 Oct 20;10(1):17725 [PMID: 33082424]
  40. Proc Natl Acad Sci U S A. 2020 Apr 28;117(17):9566-9576 [PMID: 32284420]
  41. Physica D. 2017 Jun 15;349:27-45 [PMID: 28626276]
  42. Neuroimage. 2010 Sep;52(3):731-9 [PMID: 20096791]
  43. Nat Rev Neurosci. 2020 Nov;21(11):611-624 [PMID: 32929261]
  44. J Physiol. 1952 Aug;117(4):500-44 [PMID: 12991237]
  45. Sci Rep. 2019 Feb 27;9(1):2885 [PMID: 30814615]
  46. Nat Rev Neurosci. 2018 May;19(5):255-268 [PMID: 29563572]
  47. J Math Neurosci. 2016 Dec;6(1):1 [PMID: 26728012]
  48. Netw Neurosci. 2019 Jul 01;3(3):807-826 [PMID: 31410381]

MeSH Term

Brain
Computational Biology
Connectome
Electroencephalography
Humans
Magnetic Resonance Imaging
Magnetoencephalography
Models, Neurological
Nerve Net

Word Cloud

Created with Highcharts 10.0.0graphneuralhumanmodelsfieldsconnectomefunctionaldataLaplacianbraindubbedactivityconnectivitymodelfieldstructure-functionrelationshipsresting-statemodellingstructuraldynamicalstudystochasticharmonicpowerimagingfMRIGraphToolssignalprocessingparticularoperatorrecentlysuccessfullyappliedinvestigationeigenvectors"connectomeharmonics"shownrelatefunctionallyrelevantnetworksWhole-braincombineslocalprovideinsightlarge-scaleorganizationemploypropertiesdefineimplementlargeclassdirectlyconsistingsystemsintegrodifferentialequationsgraphsanalogywell-establishedcontinuousobtainanalyticpredictionstemporalspectrawellcoherencematricestechniqueCHAOSSshorthandConnectome-HarmonicAnalysisSpatiotemporalSpectraCombiningappropriateobservationallowsestimatingparametersexperimentalobtainedelectroencephalographyEEGmagnetoencephalographyMEGmagneticresonanceexampleapplicationWilson-Cowanhigh-resolutionconstructeddiffusiontensorDTIMRIshowequilibriumfluctuationscanreproduceempiricallyobservedspectrumpredicthighleveldetailnativelyallowinclusionimportantfeaturescorticalanatomyfastcomputationsobservablequantitiescomparisonmultimodalempiricalthusappearparticularlysuitablewhole-brainmesoscopicscalesopeningnewpotentialavenuesconnectome-graph-basedinvestigationsfields:frameworkspatiotemporal

Similar Articles

Cited By