Synergistic information in a dynamical model implemented on the human structural connectome reveals spatially distinct associations with age.

Davide Nuzzi,Sebastiano Stramaglia,Daniele Marinazzo,Leonardo Angelini,Mario Pellicoro

doi:10.1162/netn_a_00146

Davide Nuzzi, Sebastiano Stramaglia + Show 3 more

Open Access

https://doi.org/10.1162/netn_a_00146

Copy DOI

Abstract

We implement the dynamical Ising model on the large-scale architecture of white matter connections of healthy subjects in the age range 4–85 years, and analyze the dynamics in terms of the synergy, a quantity measuring the extent to which the joint state of pairs of variables is projected onto the dynamics of a target one. We find that the amount of synergy in explaining the dynamics of the hubs of the structural connectivity (in terms of degree strength) peaks before the critical temperature, and can thus be considered as a precursor of a critical transition. Conversely, the greatest amount of synergy goes into explaining the dynamics of more central nodes. We also find that the aging of structural connectivity is associated with significant changes in the simulated dynamics: There are brain regions whose synergy decreases with age, in particular the frontal pole, the subcallosal area, and the supplementary motor area; these areas could then be more likely to show a decline in terms of the capability to perform higher order computation (if structural connectivity was the sole variable). On the other hand, several regions in the temporal cortex show a positive correlation with age in the first 30 years of life, that is, during brain maturation.

Highlights

Recent advances in diffusion imaging and tractography methods allow noninvasive in vivo mapping of white matter cortico-cortical projections at relatively high spatial resolution, providing a connection matrix of interregional structural connectivity (SC) representing the geometry of the brain (Sporns, 2010)
In a previous study implementing the Ising model on a 2D lattice, we showed that the joint synergistic information shared by two variables on a target one peaks before the transition to an ordered state
- Does the synergy still peak before the critical point in a nonuniform network? - Are the hubs of structural connectivity hubs of synergy? - Is there association with age?

Summary

Introduction

Recent advances in diffusion imaging and tractography methods allow noninvasive in vivo mapping of white matter cortico-cortical projections at relatively high spatial resolution, providing a connection matrix of interregional structural connectivity (SC) representing the geometry of the brain (Sporns, 2010). Dynamical models implemented on the large-scale architecture of the human brain may shed light on how function is constrained by the underlying structure. This is the case of the so-called neural mass or mean-field models that describe the collective activity of cell populations (Deco & Jirsa, 2012), or phase coupling models (Finger et al, 2016), down to abstract models such as the Ising model (Deco, Senden, & Jirsa, 2012; Haimovici, Tagliazucchi, Balenzuela, & Chialvo, 2013; Marinazzo et al, 2014; Stramaglia et al, 2017). The possible origin and role of criticality in living adaptive and evolutionary systems has recently been ascribed to adaptive and evolutionary functional advantages (Hidalgo et al, 2014)

Objectives

Methods

Results

Discussion

Conclusion