Whole brain functional connectivity: Insights from next generation neural mass modelling incorporating electrical synapses

Forrester, Michael; Petros, Sammy; Cattell, Oliver; Lai, Yi Ming; O’Dea, Reuben D.; Sotiropoulos, Stamatios; Coombes, Stephen

Abstract

The ready availability of brain connectome data has both inspired and facilitated the modelling of whole brain activity using networks of phenomenological neural mass models that can incorporate both interaction strength and tract length between brain regions. Recently, a new class of neural mass model has been developed from an exact mean field reduction of a network of spiking cortical cell models with a biophysically realistic model of the chemical synapse. Moreover, this new population dynamics model can naturally incorporate electrical synapses. Here we demonstrate the ability of this new modelling framework, when combined with data from the Human Connectome Project, to generate patterns of functional connectivity (FC) of the type observed in both magnetoencephalography and functional magnetic resonance neuroimaging. Some limited explanatory power is obtained via an eigenmode description of frequency-specific FC patterns, obtained via a linear stability analysis of the network steady state in the neigbourhood of a Hopf bifurcation. However, direct numerical simulations show that empirical data is more faithfully recapitulated in the nonlinear regime, and exposes a key role of gap junction coupling strength in generating empirically-observed neural activity, and associated FC patterns and their evolution. Thereby, we emphasise the importance of maintaining known links with biological reality when developing multi-scale models of brain dynamics. As a tool for the study of dynamic whole brain models of the type presented here we further provide a suite of C++ codes for the efficient, and user friendly, simulation of neural mass networks with multiple delayed interactions.

Citation

Forrester, M., Petros, S., Cattell, O., Lai, Y. M., O’Dea, R. D., Sotiropoulos, S., & Coombes, S. (2024). Whole brain functional connectivity: Insights from next generation neural mass modelling incorporating electrical synapses. PLoS Computational Biology, 20(12), Article e1012647. https://doi.org/10.1371/journal.pcbi.1012647

• Journal Article Type: Article
• Acceptance Date: Nov 18, 2024
• Online Publication Date: Dec 5, 2024
• Publication Date: Dec 5, 2024
• Deposit Date: Dec 9, 2024
• Journal: PLOS Computational Biology
• Print ISSN: 1553-734X
• Electronic ISSN: 1553-7358
• Publisher: Public Library of Science
• Peer Reviewed: Peer Reviewed
• Volume: 20
• Issue: 12
• Article Number: e1012647
• DOI: https://doi.org/10.1371/journal.pcbi.1012647
• Public URL: https://nottingham-repository.worktribe.com/output/42831605
• Publisher URL: https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1012647