Optimal Griffiths Phase in Heterogeneous Human Brain Networks: Brain Criticality Embracing Stability and Flexibility across Individuals

Abstract

A prominent hypothesis in neuroscience proposes that brains achieve optimal performance by operating near a critical point. However, this framework, which often assumes a universal critical point, fails to account for the extensive individual variability observed in neural dynamics and cognitive functions. These variabilities are not noise but rather an inherent manifestation of a fundamental systems-biology principle: the necessary trade-off between robustness and flexibility in human populations. Here, we propose that the Griffiths phase (GP), an extended critical regime synergically induced by two kinds of heterogeneities in brain network region and connectivity, offers a unified framework for brain criticality that better reconciles robustness and flexibility and accounts for individual variability. Using Human Connectome Project data and whole-brain modeling, we demonstrated that the synergic interplay between structural network modularity and regional heterogeneity in local excitability yields biologically viable GP featured with widely extended global excitability ranges, with an embedded optimal point that balances global/local information transmission. Crucially, an individua's position within the GP gives rise to unique global network dynamics, which in turn confer a distinctive cognitive profile via flexible configuration of functional connectivity for segregation, integration, and balance between them. These results establish GP as an evolved adaptive mechanism resolving the robustness-flexibility trade-off, fulfilling diverse cognitive demands through individualized criticality landscapes, providing a new framework of brain criticality.