Role of criticality in the structure-function relationship in the human brain

Year: 2025

Authors: Angiolelli M., Scarpetta S., Sorrentino P., Lopez ET., Quarantelli M., Granata C., Sorrentino G., Palmieri V., Messuti G., Stefano M., Filippi S., Cherubini C., Loppini A., Chiodo L.

Autors Affiliation: Univ Campus Biomed Roma, Dept Engn, Via Alvaro del Portillo 21, I-00128 Rome, Italy; Univ Salerno, Dept Phys E R Caianiello, Via Giovanni Paolo 2 132, I-84084 Fisciano, Italy; INFN sez, Coll Salerno, Via Giovanni Paolo 2,132, I-84084 Fisciano, Italy; Aix Marseille Univ, Inst Neurosci Syst, INSERM, INS, 27 Blvd Jean Moulin, F-13005 Marseille, France; CNR, Natl Res Council INO, Natl Inst Opt, Largo Enr Fermi 6, I-50125 Florence, Italy; Univ Sassari, Dept Biomed Sci, Viale S Pietro 43c, I-07100 Sassari, Italy; Univ Naples Parthenope, Dept Med Motor & Wellness Sci, Via Amm F Acton 38, I-80133 Naples, Italy; Ist Clin Sci Maugeri Hermitage, Via Miano 69, I-80145 Naples, Italy; Intelligent Syst Natl Res Council, Inst Appl Sci, Via Campi Flegrei 34, I-80078 Pozzuoli, Italy; Natl Res Council DSFTM CNR, Dept Phys Sci & Technol Matter, I-00128 Rome, Italy; Univ Campus Biomed Roma, Dept Sci & Technol Sustainable Dev & Hlth 1, Via Alvaro Portillo 21, I-00128 Rome, Italy; ICRANet Int Ctr Relativist Astrophys Network, Piazza Repubbl 10, I-65122 Pescara, Italy; Univ Campus Biomed Roma, Dept Med & Surg, Via Alvaro Portillo 21, I-00128 Rome, Italy.

Abstract: A healthy brain exhibits a rich dynamical repertoire, with flexible spatiotemporal patterns replaying on both microscopic and macroscopic scales. We hypothesize that the observed relationship between empirical structure and functional patterns is best explained when the microscopic neuronal dynamics is close to a critical regime. Using a modular spiking neuronal network model based on empirical connectomes, we posit that multiple stored functional patterns can transiently reoccur when the system operates near a critical regime, generating realistic brain dynamics and structural-functional relationships. The connections in the model are chosen so as to force the network to learn and propagate suited modular spatiotemporal patterns. To test our hypothesis, we employ magnetoencephalography and tractography data from five healthy individuals. We show that the extended critical region of the model maximizes the structure-function correlation and generates realistic features, demonstrating the relevance of near-critical regimes for physiological brain activity.

Journal/Review: PHYSICAL REVIEW RESEARCH

Volume: 7 (4)      Pages from: 43153-1  to: 43153-21

More Information: This research has received funding from the Italian National Recovery and Resilience Plan (PNRR), M4C2, funded by the European Union-NextGenerationEU (Project IR0000011, CUP B51E22000150006, EBRAINS-Italy (European Brain ReseArch INfrastructureS-Italy). Helpful discussions with Antonio de Candia are gratefully acknowledged. M.A., S.F., C.C., A.L., and L.C. wish to acknowledge the Italian National Group for Mathematical Physics, GNFM-INdAM. S.F. wishes to acknowledge ICRANet. Cartoons in Figs. 1, 2, and 6 were created at [112]. The author contributions are as follows: M.A., S.S., P.S., C.C, A.L, L.C.: Conceptualization and Methodology; M.A., S.S., P.S.: Simulations and Data analysis; M.A., S.S., P.S., C.C, L.C.: Formal analysis; P.S., E.T.L., M.Q., C.G., G.S., S.S.: Resources; M.A., S.S., P.S., C.C, L.C.: Writing-Original Draft; M.A., S.S., P.S., E.T.L., M.Q., C.G., G.S., V.P., G.M., M.S., S.F., C.C., A.L., L.C.: Writing-Review-Editing; M.A., S.S., P.S., V.P., G.M., M.S., S.F., C.C, A.L., L.C.: Visualization; S.S., P.S., C.C., L.C.: Supervision and Project administration; S.S., P.S., G.S., S.F.: Funding acquisition. All authors read and approved the final manuscript. The authors declare no competing interests.
KeyWords: Neuronal Avalanches; Cortical Networks; Memory; Dynamics; Cortex; Range; State; Organization; Architecture; Information
DOI: 10.1103/PhysRevResearch.7.043153