Transient networks of spatio-temporal connectivity map communication pathways in brain functional systems

• Published in: NeuroImage (Orlando, Fla.) Vol. 155; pp. 490 - 502
• Main Authors: Griffa, Alessandra, Ricaud, Benjamin, Benzi, Kirell, Bresson, Xavier, Daducci, Alessandro, Vandergheynst, Pierre, Thiran, Jean-Philippe, Hagmann, Patric
• Format: Journal Article
• Language: English
• Published: United States Elsevier Inc 15.07.2017; Elsevier Limited
• Subjects: Adult; Attention; Brain; Brain - anatomy & histology; Brain - diagnostic imaging; Brain - physiology; Brain connectivity; Brain dynamics; Brain mapping; Communication; Communication-through-coherence; Connectome - methods; Diffusion Magnetic Resonance Imaging - methods; Diffusion MRI; Female; Functional anatomy; Functional magnetic resonance imaging; Humans; Information processing; Male; Multilayer network; Nerve Net - anatomy & histology; Nerve Net - diagnostic imaging; Nerve Net - physiology; Neural networks; NMR; Nuclear magnetic resonance; Oscillations; Point-process; Propagation; Resting-state fMRI; Spatio-temporal connectome; Structure-function relationships; Studies; Temporal network; Time series; Young Adult; Communication-through-coherence; Spatio-temporal connectome; Brain connectivity; Temporal network; Resting-state fMRI; Brain dynamics; Diffusion MRI; Point-process; Multilayer network
• ISSN: 1053-8119; 1095-9572; 1095-9572
• DOI: 10.1016/j.neuroimage.2017.04.015

The study of brain dynamics enables us to characterize the time-varying functional connectivity among distinct neural groups. However, current methods suffer from the absence of structural connectivity information. We propose to integrate infra-slow neural oscillations and anatomical-connectivity maps, as derived from functional and diffusion MRI, in a multilayer-graph framework that captures transient networks of spatio-temporal connectivity. These networks group anatomically wired and temporary synchronized brain regions and encode the propagation of functional activity on the structural connectome. In a group of 71 healthy subjects, we find that these transient networks demonstrate power-law spatial and temporal size, globally organize into well-known functional systems and describe wave-like trajectories of activation across anatomically connected regions. Within the transient networks, activity propagates through polysynaptic paths that include selective ensembles of structural connections and differ from the structural shortest paths. In the light of the communication-through-coherence principle, the identified spatio-temporal networks could encode communication channels' selection and neural assemblies, which deserves further attention. This work contributes to the understanding of brain structure-function relationships by considering the time-varying nature of resting-state interactions on the axonal scaffold, and it offers a convenient framework to study large-scale communication mechanisms and functional dynamics. •Functional dynamics and structural connectivity are represented as multilayer graphs.•The graph components represent transient networks of spatio-temporal connectivity.•The transient networks embed viable polysynaptic pathways for communication.•Known functional systems are mapped by complex wave-like propagation patterns.