Algebraic Topology of Multi-Brain Connectivity Networks Reveals Dissimilarity in Functional Patterns during Spoken Communications

Human behaviour in various circumstances mirrors the corresponding brain connectivity patterns, which are suitably represented by functional brain networks. While the objective analysis of these networks by graph theory tools deepened our understanding of brain functions, the multi-brain structures and connections underlying human social behaviour remain largely unexplored. In this study, we analyse the aggregate graph that maps coordination of EEG signals previously recorded during spoken communications in two groups of six listeners and two speakers. Applying an innovative approach based on the algebraic topology of graphs, we analyse higher-order topological complexes consisting of mutually interwoven cliques of a high order to which the identified functional connections organise. Our results reveal that the topological quantifiers provide new suitable measures for differences in the brain activity patterns and inter-brain synchronisation between speakers and listeners. Moreover, the higher topological complexity correlates with the listener’s concentration to the story, confirmed by self-rating, and closeness to the speaker’s brain activity pattern, which is measured by network-to-network distance. The connectivity structures of the frontal and parietal lobe consistently constitute distinct clusters, which extend across the listener’s group. Formally, the topology quantifiers of the multi-brain communities exceed the sum of those of the participating individuals and also reflect the listener’s rated attributes of the speaker and the narrated subject. In the broader context, the presented study exposes the relevance of higher topological structures (besides standard graph measures) for characterising functional brain networks under different stimuli.

[1]  Anil Bollimunta,et al.  Attention as an effect not a cause , 2014, Trends in Cognitive Sciences.

[2]  C. Bron,et al.  Algorithm 457: finding all cliques of an undirected graph , 1973 .

[3]  P. Gould,et al.  Q-Analysis, or a Language of Structure: An Introduction for Social Scientists, Geographers and Planners , 1980, Int. J. Man Mach. Stud..

[4]  Xuelong Li,et al.  A survey of graph edit distance , 2010, Pattern Analysis and Applications.

[5]  E. C. Padovani Characterization of the Community Structure of Large Scale Functional Brain Networks During Ketamine-Medetomidine Anesthetic Induction , 2016, 1606.04719.

[6]  M. Goldberg,et al.  Attention, intention, and priority in the parietal lobe. , 2010, Annual review of neuroscience.

[7]  D. Hu,et al.  Identifying major depression using whole-brain functional connectivity: a multivariate pattern analysis. , 2012, Brain : a journal of neurology.

[8]  Sergey N. Dorogovtsev,et al.  Lectures on Complex Networks , 2010 .

[9]  Vaskar Saha,et al.  Outcome of Central Nervous System Relapses In Childhood Acute Lymphoblastic Leukaemia – Prospective Open Cohort Analyses of the ALLR3 Trial , 2014, PloS one.

[10]  J Martinerie,et al.  Functional modularity of background activities in normal and epileptic brain networks. , 2008, Physical review letters.

[11]  Edward T. Bullmore,et al.  Whole-brain anatomical networks: Does the choice of nodes matter? , 2010, NeuroImage.

[12]  Bosiljka Tadic,et al.  Hierarchical sequencing of online social graphs , 2014, ArXiv.

[13]  Chaozhe Zhu,et al.  Neural Synchronization during Face-to-Face Communication , 2012, The Journal of Neuroscience.

[14]  Rosario N. Mantegna,et al.  Book Review: An Introduction to Econophysics, Correlations, and Complexity in Finance, N. Rosario, H. Mantegna, and H. E. Stanley, Cambridge University Press, Cambridge, 2000. , 2000 .

[15]  Klaus Lehnertz,et al.  Time-dependent degree-degree correlations in epileptic brain networks: from assortative to dissortative mixing , 2015, Front. Hum. Neurosci..

[16]  N. Kriegeskorte,et al.  Neural correlates of trust , 2007, Proceedings of the National Academy of Sciences.

[17]  Georgios A. Keliris,et al.  Introduction to Research Topic – Binocular Rivalry: A Gateway to Studying Consciousness , 2012, Front. Hum. Neurosci..

[18]  A. Barabasi,et al.  Uncovering disease-disease relationships through the incomplete interactome , 2015, Science.

[19]  Olaf Sporns,et al.  Communication Efficiency and Congestion of Signal Traffic in Large-Scale Brain Networks , 2014, PLoS Comput. Biol..

[20]  J. Verhoeven,et al.  Developmental Foreign Accent Syndrome: Report of a New Case , 2016, Front. Hum. Neurosci..

[21]  Jonas Richiardi,et al.  Graph analysis of functional brain networks: practical issues in translational neuroscience , 2014, Philosophical Transactions of the Royal Society B: Biological Sciences.

[22]  Line Garnero,et al.  Inter-Brain Synchronization during Social Interaction , 2010, PloS one.

[23]  Mahmoud Hassan,et al.  EEG Source Connectivity Analysis: From Dense Array Recordings to Brain Networks , 2014, PloS one.

[24]  O. Sporns,et al.  Network hubs in the human brain , 2013, Trends in Cognitive Sciences.

[25]  Mason A. Porter,et al.  Robust Detection of Dynamic Community Structure in Networks , 2012, Chaos.

[26]  Asaf Madi,et al.  Genome Holography: Deciphering Function-Form Motifs from Gene Expression Data , 2008, PloS one.

[27]  Dmitry N. Kozlov,et al.  Combinatorial Algebraic Topology , 2007, Algorithms and computation in mathematics.

[28]  Laura Astolfi,et al.  Defecting or Not Defecting: How to “Read” Human Behavior during Cooperative Games by EEG Measurements , 2010, PloS one.

[29]  Eshel Ben-Jacob,et al.  Functional holography of recorded neuronal networks activity , 2007, Neuroinformatics.

[30]  Dezhong Yao,et al.  Large-Scale Functional Networks Identified from Resting-State EEG Using Spatial ICA , 2016, PloS one.

[31]  Holly N. Phillips,et al.  Hierarchical Organization of Frontotemporal Networks for the Prediction of Stimuli across Multiple Dimensions , 2015, The Journal of Neuroscience.

[32]  Chong Wu,et al.  A new network node similarity measure method and its applications , 2014, ArXiv.

[33]  J. Clulow,et al.  We Made Your Bed, Why Won’t You Lie in It? Food Availability and Disease May Affect Reproductive Output of Reintroduced Frogs , 2016, PloS one.

[34]  M. Mitrovic,et al.  Spectral and dynamical properties in classes of sparse networks with mesoscopic inhomogeneities. , 2008, Physical review. E, Statistical, nonlinear, and soft matter physics.

[35]  Xenophon Papademetris,et al.  Graph-theory based parcellation of functional subunits in the brain from resting-state fMRI data , 2010, NeuroImage.

[36]  R. H. Atkin,et al.  An Algebra for Patterns on a Complex, I , 1974, Int. J. Man Mach. Stud..

[37]  Jingyuan E. Chen,et al.  NIRS-Based Hyperscanning Reveals Inter-brain Neural Synchronization during Cooperative Jenga Game with Face-to-Face Communication , 2016, Front. Hum. Neurosci..

[38]  G. Ding,et al.  Leader emergence through interpersonal neural synchronization , 2015, Proceedings of the National Academy of Sciences.

[39]  T. Womelsdorf,et al.  Long-Range Attention Networks: Circuit Motifs Underlying Endogenously Controlled Stimulus Selection , 2015, Trends in Neurosciences.

[40]  Julien Cohen-Adad,et al.  The Human Connectome Project and beyond: Initial applications of 300mT/m gradients , 2013, NeuroImage.

[41]  R. Adolphs,et al.  The social brain: neural basis of social knowledge. , 2009, Annual review of psychology.

[42]  Jari Saramäki,et al.  Characterizing the Community Structure of Complex Networks , 2010, PloS one.

[43]  Jean M. Vettel,et al.  Controllability of structural brain networks , 2014, Nature Communications.

[44]  Viktor Müller,et al.  Intra- and Inter-Brain Synchronization during Musical Improvisation on the Guitar , 2013, PloS one.

[45]  John-Dylan Haynes,et al.  Content-specific coordination of listeners' to speakers' EEG during communication , 2012, Front. Hum. Neurosci..

[46]  José Manuel Pastor,et al.  Application of Entropy-Based Metrics to Identify Emotional Distress from Electroencephalographic Recordings , 2016, Entropy.

[47]  M. Grigutsch,et al.  Music and emotion: electrophysiological correlates of the processing of pleasant and unpleasant music. , 2007, Psychophysiology.

[48]  S. Shimojo,et al.  Interpersonal body and neural synchronization as a marker of implicit social interaction , 2012, Scientific Reports.

[49]  Edward T. Bullmore,et al.  Modular and Hierarchically Modular Organization of Brain Networks , 2010, Front. Neurosci..

[50]  Alex Arenas,et al.  Synchronization reveals topological scales in complex networks. , 2006, Physical review letters.

[51]  Béla Bollobás,et al.  Modern Graph Theory , 2002, Graduate Texts in Mathematics.

[52]  J. Jonsson Simplicial complexes of graphs , 2007 .

[53]  Scott T. Grafton,et al.  Dynamic reconfiguration of human brain networks during learning , 2010, Proceedings of the National Academy of Sciences.

[54]  M. Jorge Cardoso,et al.  Consensus between Pipelines in Structural Brain Networks , 2014, PloS one.

[55]  Olaf Sporns,et al.  Complex network measures of brain connectivity: Uses and interpretations , 2010, NeuroImage.

[56]  O. Sporns,et al.  Complex brain networks: graph theoretical analysis of structural and functional systems , 2009, Nature Reviews Neuroscience.

[57]  F. Babiloni,et al.  Estimation of the cortical functional connectivity with the multimodal integration of high-resolution EEG and fMRI data by directed transfer function , 2005, NeuroImage.

[58]  C. Frith,et al.  Meeting of minds: the medial frontal cortex and social cognition , 2006, Nature Reviews Neuroscience.

[59]  Thomas Wolbers,et al.  Space, time, and numbers in the right posterior parietal cortex: Differences between response code associations and congruency effects , 2016, NeuroImage.

[60]  Marija Mitrovic,et al.  Correlation Patterns in Gene Expressions along the Cell Cycle of Yeast , 2009, CompleNet.

[61]  Santo Fortunato,et al.  Community detection in graphs , 2009, ArXiv.

[62]  R. Ho Algebraic Topology , 2022 .

[63]  Joaquín Goñi,et al.  A Network Convergence Zone in the Hippocampus , 2014, PLoS Comput. Biol..

[64]  Franco Bagnoli,et al.  Mapping cortical functions with a local community detection algorithm , 2014, J. Complex Networks.

[65]  M. Iacoboni,et al.  The self and social cognition: the role of cortical midline structures and mirror neurons , 2007, Trends in Cognitive Sciences.

[66]  B. Tadić,et al.  Jamming and correlation patterns in traffic of information on sparse modular networks , 2009, 0904.1082.

[67]  Xiang Xiao,et al.  Cluster imaging of multi-brain networks (CIMBN): a general framework for hyperscanning and modeling a group of interacting brains , 2015, Front. Neurosci..

[68]  Chaozhe Zhu,et al.  Cross-Brain Neurofeedback: Scientific Concept and Experimental Platform , 2013, PloS one.

[69]  A. Roepstorff,et al.  The two-brain approach: how can mutually interacting brains teach us something about social interaction? , 2012, Front. Hum. Neurosci..

[70]  L. Freeman Q-analysis and the structure of friendship networks , 1980 .

[71]  G. Tononi,et al.  Rethinking segregation and integration: contributions of whole-brain modelling , 2015, Nature Reviews Neuroscience.

[72]  Fan Cao,et al.  How does language distance between L1 and L2 affect the L2 brain network? An fMRI study of Korean–Chinese–English trilinguals , 2016, NeuroImage.

[73]  Bosiljka Tadić,et al.  Hidden geometry of traffic jamming. , 2015, Physical review. E, Statistical, nonlinear, and soft matter physics.