Abstract
Higher-order interactions have long figured both at the microscopic and macroscopic level in neuronal and whole-brain descriptions, with the aim to capture structural, functional, and ultimately cognitive aspects. They are systematizing the paradigm shift that graph theory introduced by moving from studying neural and brain activation to co-activation patterns. Recently, topology has emerged as a central tool in this context due to its natural capacity to describe relations beyond pairwise interactions, and to recent advances in its computational applications. In this chapter, we summarize fundamental concepts and results of the application of higher-order descriptions to neuroscience. We start from the microscopic scale, describing how higher-order interactions have been introduced and measured in the context of neuronal populations activation patterns and in neural coding theory. We then move to the macroscopic scale, discussing recent applications of topological data analysis to whole-brain data, and finally highlight the challenges related to extracting higher-order signals from low-order ones.
Access this chapter
Tax calculation will be finalised at checkout
Purchases are for personal use only
References
A. Babichev, D. Morozov, Y. Dabaghian, R. spatial memory maps encoded by networks with transient connections. PLOS Comput. Biol. 14(9), e1006433 (2018)
A. Babichev, D. Morozov, Y. Dabaghian, Replays of spatial memories suppress topological fluctuations in cognitive map. Network Neurosc. (Cambridge, Mass.), 3(3):707–724, 2019
A. Babichev, D. Morozov, Y. Dabaghian, Replays of spatial memories suppress topological fluctuations in cognitive map. Netw. Neurosci. 3(3), 707–724 (2019)
H.C. Barron, R.B. Mars, D. Dupret, J.P. Lerch, Cassandra sampaio-baptista. Cross-species neuroscience: closing the explanatory gap. Philosoph. Trans. of the Royal Society B, 376(1815), 20190633 (2021)
J.M. Beggs, D. Plenz, Neuronal avalanches in neocortical circuits. J. Neurosci. Official J. Soc. Neurosc. 23(35), 11167–11177 (2003)
J. Billings, M. Saggar, J. Hlinka, S. Keilholz, G. Petri, Simplicial and topological descriptions of human brain dynamics. Network Neurosci. 5(2), 549–568 (2021)
N.A. Cayco-Gajic, J. Zylberberg, E. Shea-Brown, Triplet correlations among similarly tuned cells impact population coding. Front. Comput. Neurosci. 9, 57 (2015)
K.K.A. Cho, R. Hoch, A.T. Lee, T. Patel, J.L.R. Rubenstein, V.S. Sohal, Gamma rhythms link prefrontal interneuron dysfunction with cognitive inflexibility in Dlx5/6+/- Mice. Neuron. 85(6), 1332–1343 (2015)
A. Choudhary, A. Saha, S. Krueger, C. Finke, Phys. Rev., (A curious case of weak interactions (Weak-winner phase synchronization, Physical Review Research, 2021), p. 2021
M.K. Chung, H. Lee, A. DiChristofano, H. Ombao, V. Solo, Exact topological inference of the resting-state brain networks in twins. Netw. Neurosci. 3(3), 674–694 (2019)
M.K. Chung, V. Villalta-Gil, H. Lee, P.J. Rathouz, B.B. Lahey, D.H. Zald, Exact topological inference for paired brain networks via persistent homology. in International Conference on Information Processing in Medical Imaging (Springer, 2017), pp. 299–310
C. Curto, V. Itskov, Cell groups reveal structure of stimulus space. PLoS Comput. Biol. 4(10), e1000205 (2008)
Y. Dabaghian, V.L. Brandt, L.M. Frank, Reconceiving the hippocampal map as a topological template. Elife 3, e03476 (2014)
Y. Dabaghian, F. Mémoli, L. Frank, G. Carlsson, A topological paradigm for hippocampal spatial map formation using persistent homology. PLOS Comput. Biol. 8(8), e1002581 (2012)
F. de Vico Fallani, J. Richiardi, M. Chavez, S. Achard, Graph analysis of functional brain networks: practical issues in translational neuroscience. Philosoph. Trans. Royal Soc. B: Biolog. Sciences, 369(1653), 20130521 (2014)
P. Expert, L.-D. Lord, M.L. Kringelbach, G. Petri, Editorial: topological neuroscience. Netw. Neurosci. 3(3), 653–655 (2019)
T. Ezaki, T. Watanabe, M. Ohzeki, N. Masuda, Energy landscape analysis of neuroimaging data. Philosoph. Trans. Royal Soc. A: Mathe. Phys. Eng. Sci. 375(2096), 20160287 (2017)
J. Faskowitz, F.Z. Esfahlani, Y. Jo, O. Sporns, R.F. Betzel, Edge-centric functional network representations of human cerebral cortex reveal overlapping system-level architecture. Nat. Neurosc. 23(12), 1644–1654 (2020)
E. Ganmor, R. Segev, E. Schneidman, Sparse low-order interaction network underlies a highly correlated and learnable neural population code. Proc. Natl. Acad. Sci. U.S.A. 108(23), 9679–9684 (2011)
M. Gatica, R. Cofré, P.A.M. Mediano, F.E. Rosas, P. Orio, I. Diez, S.P. Swinnen, J.M. Cortes (High-order interdependencies in the aging brain, Brain connectivity, 2021)
R. Ghrist, Barcodes: the persistent topology of data. Bull. Am. Math. Soc. 45(1), 61–75 (2008)
C. Giusti, E. Pastalkova, C. Curto, V. Itskov, Clique topology reveals intrinsic geometric structure in neural correlations. Proc. Natl. Acad. Sci. U.S.A. 112(44), 13455–13460 (2015)
M.S. Granovetter, The strength of weak ties. Am. J. Sociol. 1–22 (1973)
T. Hafting, M. Fyhn, S. Molden, M.-B. Moser, E.I. Moser, Microstructure of a spatial map in the entorhinal cortex. Nature 436(7052), 801–806 (2005)
X. Huang, X. Kaibin, C. Chu, T. Jiang, Y. Shan, Weak higher-order interactions in macroscopic functional networks of the resting brain. J. Neurosci. 37(43), 10481–10497 (2017)
E. Ibáñez-Marcelo, L. Campioni, D. Manzoni, E.L. Santarcangelo, G. Petri, Spectral and topological analyses of the cortical representation of the head position: does hypnotizability matter? Brain Behav. 9(6), e01277 (2019)
E. Ibáñez-Marcelo, L. Campioni, A. Phinyomark, G. Petri, E.L. Santarcangelo, Topology highlights mesoscopic functional equivalence between imagery and perception: the case of hypnotizability. NeuroImage 200, 437–449 (2019)
V. Itskov, C. Curto, E. Pastalkova, G. Buzsáki, Cell assembly sequences arising from spike threshold adaptation keep track of time in the hippocampus. J. Neurosc?: Official J. Soc. Neurosci. 31(8), 2828–2834 (2011)
L. Kanari, S. Ramaswamy, Y. Shi, S. Morand, J. Meystre, R. Perin, M. Abdellah, Y. Wang, K. Hess, H. Markram, Objective morphological classification of neocortical pyramidal cells. Cerebral Cortex (New York, N.Y. 1991), 29(4), 1719–1735 (2019)
P.S. Katz, Neural mechanisms underlying the evolvability of behaviour. Philosoph. Trans. Royal Soc. B: Biolog. Sci. 366(1574), 2086–2099 (2011)
U. Köster, J. Sohl-Dickstein, C.M. Gray, B.A. Olshausen, Modeling higher-order correlations within cortical microcolumns. PLOS Comput. Biol. 10(7), e1003684 (2014)
B. Kralemann, A. Pikovsky, M. Rosenblum, Reconstructing effective phase connectivity of oscillator networks from observations. New J. Phys. 16(8), 085013 (2014)
H. Lee, M.K. Chung, H. Choi, H. Kang, S. Ha, Y.K. Kim, D.S. Lee, Harmonic holes as the submodules of brain network and network dissimilarity, in International Workshop on Computational Topology in Image Context (Springer, 2019), pp. 110–122
H. Lee, M.K. Chung, H. Kang, B.-N. Kim, D.S. Lee. Discriminative persistent homology of brain networks, in 2011 IEEE International Symposium on Biomedical Imaging: From Nano to Macro (IEEE, 2011), , pp. 841–844
H. Lee, M.K. Chung, H. Kang, D.S. Lee, Hole detection in metabolic connectivity of Alzheimer’s disease using k- Laplacian, in International Conference on Medical Image Computing and Computer-Assisted Intervention (Springer, 2014), pp. 297–304
H. Lee, H. Kang, M.K. Chung, B.-N. Kim, D.S. Lee, Persistent brain network homology from the perspective of dendrogram. IEEE Trans. Med. Imaging 31(12), 2267–2277 (2012)
H. Lee, H. Kang, M.K. Chung, S. Lim, B.-N. Kim, D.S. Lee, Integrated multimodal network approach to PET and MRI based on multidimensional persistent homology. Hum. Brain Mapp. 38(3), 1387–1402 (2017)
L.-D. Lord, P. Expert, H.M. Fernandes, G. Petri, T.J. Van Hartevelt, F. Vaccarino, G. Deco, F. Turkheimer, M.L. Kringelbach, Insights into brain architectures from the homological scaffolds of functional connectivity networks. Front. Syst. Neurosci. 10, 85 (2016)
A. Montalto, L. Faes, D. Marinazzo, Mute: a matlab toolbox to compare established and novel estimators of the multivariate transfer entropy. PloS one 9(10), e109462 (2014)
M.E.J. Newman, Modularity and community structure in networks. Proc. Natl. Acad. Sci. U.S.A. 103(23), 8577–8582 (2006)
J. O’Keefe, J. Dostrovsky, The hippocampus as a spatial map. Preliminary evidence from unit activity in the freely-moving rat. Brain Res. 34(1), 171–175 (1971)
F. Orhan, H. Fatouros-Bergman, M. Goiny, A. Malmqvist, F. Piehl, K. Schizophrenia Project (KaSP) Consortium, S. Cervenka, K. Collste, P. Victorsson, C.M. Sellgren, L. Flyckt, S. Erhardt, G. Engberg CSF GABA is reduced in first-episode psychosis and associates to symptom severity. Mol. Psych. 23(5), 1244–1250 (2018)
A. Patania, P. Selvaggi, M. Veronese, O. Dipasquale, P. Expert, G. Petri, Topological gene expression networks recapitulate brain anatomy and function. Netw. Neurosci. (Cambridge, Mass.) 3(3), 744–762 (2019)
G. Petri, P. Expert, F. Turkheimer, R. Carhart-Harris, D. Nutt, P.J. Hellyer, F. Vaccarino, Homological scaffolds of brain functional networks. J. R. Soc. Interface 11(101), 20140873 (2014)
G. Petri, S. Musslick, B. Dey, K. Özcimder, D. Turner, N.K. Ahmed, T.L. Willke, J.D. Cohen, Topological limits to the parallel processing capability of network architectures. Nat. Phys. 17(5), 646–651 (2021)
G. Petri, M. Scolamiero, I. Donato, F. Vaccarino. Topological strata of weighted complex networks. PLOS ONE, 8(6) (2013)
A. Phinyomark, E. Ibanez-Marcelo, G. Petri, Resting-state fMRI functional connectivity: big data preprocessing pipelines and topological data analysis. IEEE Trans. Big Data 3(4), 415–428 (2017)
S.M. Plis, J. Sui, T. Lane, S. Roy, V.P. Clark, V.K. Potluru, R.J. Huster, A. Michael, S.R. Sponheim, M.P Weisend et al. High-order interactions observed in multi-task intrinsic networks are dominant indicators of aberrant brain function in schizophrenia. Neuroimage 102, 35–48 (2014)
B. Rasch, J. Born, About sleep’s role in memory. Physiolog. Rev. 93(2), 681–766 (2013)
M.W. Reimann, M. Nolte, M. Scolamiero, K. Turner, R. Perin, G. Chindemi, P. Dłotko, R. Levi, K. Hess, H. Markram, Cliques of neurons bound into cavities provide a missing link between structure and function. Front. Comput. Neurosci. 11, 48 (2017)
J. Richiardi, A. Altmann, A.-C. Milazzo, C. Chang, M.M. Chakravarty, T. Banaschewski, G.J. Barker, A.L.W. Bokde, U. Bromberg, C. Büchel, P. Conrod, M. Fauth-Bühler, H. Flor, V. Frouin, J. Gallinat, H. Garavan, P. Gowland, A. Heinz, H. Lemaître, K.F. Mann, J.-L. Martinot, F. Nees, T. Paus, Z. Pausova, M. Rietschel, T.W. Robbins, M.N. Smolka, R. Spanagel, A. Ströhle, G. Schumann, M. Hawrylycz, M.D. Greicius, IMAGEN consortium, L. Albrecht, C. Andrew, M. Arroyo, E. Artiges, S. Aydin, C. Bach, T. Banaschewski, A. Barbot, G. Barker, N. Boddaert, A. Bokde, Z. Bricaud, U. Bromberg, R. Bruehl, C. Büchel, A. Cachia, A. Cattrell, P. Conrod, P. Constant, J. Dalley, B. Decideur, S. Desrivieres, T. Fadai, H.Flor, J. Gallinat, H. Garavan, F.G. Briand, P. Gowland, B. Heinrichs, A. Heinz, N. Heym, T. Hübner, J. Ireland, B. Ittermann, T. Jia, M. Lathrop, D. Lanzerath, C. Lawrence, H. Lemaitre, K. Lüdemann, C. Macare, C. Mallik, J.-F. Mangin, K. Mann, J.-L. Martinot, E. Mennigen, F.M. de Carvahlo, X. Mignon, R. Miranda, K. Müller, F. Nees, C. Nymberg, M.-L. Paillere, Z. Pausova, J.-B. Poline, L. Poustka, M. Rapp, G. Robert, J. Reuter, M. Rietschel, S. Ripke, T. Robbins, S. Rodehacke, J. Rogers, A. Romanowski, B. Ruggeri, C. Schmäl, D. Schmidt, S. Schneider, M. Schumann, F. Schubert, Y. Schwartz, M. Smolka, W. Sommer, R. Spanagel, C. Speiser, T. Spranger, A. Stedman, S. Steiner, D. Stephens, N. Strache, A. Ströhle, M. Struve, N. Subramaniam, L. Topper, R. Whelan, S. Williams, J. Yacubian, M. Zilbovicius, C.P. Wong, S. Lubbe, L. Martinez-Medina, A. Fernandes, A. Tahmasebi, Correlated gene expression supports synchronous activity in brain networks. Science 348(6240), 1241–1244 (2015)
B. Rieck, T. Yates, C. Bock, K. Borgwardt, G. Wolf, N. Turk-Browne, S. Krishnaswamy, Uncovering the topology of time-varying fmri data using cubical persistence (2020). ArXiv preprint arXiv:2006.07882
F.E. Rosas, P.A.M. Mediano, M. Gastpar, H.J. Jensen, Quantifying high-order interdependencies via multivariate extensions of the mutual information. Phys. Rev. E. 100(3), 032305 (2019)
Y. Roudi, J. Tyrcha, J. Hertz, Ising model for neural data: model quality and approximate methods for extracting functional connectivity. Phys. Rev. E 79(5), 051915–12 (2009)
E. Rybakken, N. Baas, B. Dunn, Decoding of neural data using cohomological feature extraction. Neural Comput. 31(1), 68–93 (2019)
M. Saggar, O. Sporns, J. Gonzalez-Castillo, P.A. Bandettini, G. Carlsson, G. Glover, A.L. Reiss, Towards a new approach to reveal dynamical organization of the brain using topological data analysis. Nat. Commun. 9(1), 1–14 (2018)
F.A.N. Santos, E.P. Raposo, M.D. Coutinho-Filho, M. Copelli, C.J. Stam, L. Douw, Topological phase transitions in functional brain networks. Phys. Rev. E 100(3), 032414 (2019)
E. Schneidman, M.J. Berry II., R. Segev, W. Bialek, Weak pairwise correlations imply strongly correlated network states in a neural population. Nature 440(7087), 1007 (2006)
W.L. Shew, H. Yang, S. Yu, R. Roy, D. Plenz, Information capacity and transmission are maximized in balanced cortical networks with neuronal avalanches 31(1), 55–63 (2011)
H. Shimazaki, S. Amari, E.N. Brown, S. Grün, State-space analysis of time-varying higher-order spike correlation for multiple neural spike train data. PLOS Comput. Biol. 8(3), e1002385 (2012)
H. Shimazaki, K. Sadeghi, T. Ishikawa, Y. Ikegaya, T. Toyoizumi, Simultaneous silence organizes structured higher-order interactions in neural populations. Sci. Rep. 5, 9821 (2015)
A.E. Sizemore, C. Giusti, A. Kahn, J.M. Vettel, R.F. Betzel, D.S. Bassett, Cliques and cavities in the human connectome. J. Comput. Neurosci. 44(1), 115–145 (2018)
T.H. Sun, Linear dependence structure of the entropy space. Inf. Control. 29(4), 337–68 (1975)
E. Tagliazucchi, P. Balenzuela, D. Fraiman, D.R. Chialvo, Criticality in large-scale brain fMRI dynamics unveiled by a novel point process analysis. Front. Phys. 1–12 (2013)
F.E. Turkheimer, R. Leech, P. Expert, L.-D. Lord, A.C. Vernon, The brain’s code and its canonical computational motifs. From sensory cortex to the default mode network: a multi-scale model of brain function in health and disease. Neurosc. Biobehav. Rev. 55, 211–222 (2015)
F.E. Turkheimer, F.E. Rosas, O. Dipasquale, D. Martins, E.D. Fagerholm, P. Expert, F. Váša, L.-D. Lord, R. Leech, A Complex systems perspective on neuroimaging studies of behavior and its disorders. The Neuroscientist: a Rev J. Bring. Neurob. Neurol. Psychiatry pp. 1073858421994784 (2021)
S. Watanabe, Information theoretical analysis of multivariate correlation. IBM J. Res. Dev. 4(1), 66–82 (1960)
T. Watanabe, S. Hirose, H. Wada, Y. Imai, T. Machida, I. Shirouzu, S. Konishi, Y. Miyashita, N. Masuda, Energy landscapes of resting-state brain networks. Front. Neuroinformatics 8, 12 (2014)
T. Watanabe, N. Masuda, F. Megumi, R. Kanai, G. Rees, Energy landscape and dynamics of brain activity during human bistable perception. Nature 5, 4765 (2014)
S. Yu, H. Yang, H. Nakahara, G.S. Santos, D. Nikolić, D. Plenz, Higher-order interactions characterized in cortical activity. J. Neurosci. 31(48), 17514–17526 (2011)
H. Zhang, X. Chen, F. Shi, G. Li, M. Kim, P. Giannakopoulos, S. Haller, D. Shen, Topographical information-based high-order functional connectivity and its application in abnormality detection for mild cognitive impairment. J. Alzheimers Dis. 54(3), 1095–1112 (2016)
H. Zhang, Y. Xiaobo Chen, Zhang, D. Shen, Test-retest reliability of “high-order” functional connectivity in young healthy adults. Front. Neurosci. 11, 439 (2017)
Author information
Authors and Affiliations
Corresponding author
Editor information
Editors and Affiliations
Rights and permissions
Copyright information
© 2022 The Author(s), under exclusive license to Springer Nature Switzerland AG
About this chapter
Cite this chapter
Expert, P., Petri, G. (2022). Higher-Order Description of Brain Function. In: Battiston, F., Petri, G. (eds) Higher-Order Systems. Understanding Complex Systems. Springer, Cham. https://doi.org/10.1007/978-3-030-91374-8_17
Download citation
DOI: https://doi.org/10.1007/978-3-030-91374-8_17
Published:
Publisher Name: Springer, Cham
Print ISBN: 978-3-030-91373-1
Online ISBN: 978-3-030-91374-8
eBook Packages: Physics and AstronomyPhysics and Astronomy (R0)