The critical roaming hypothesis: arousal-driven transitions across critical lines reproduce human functional connectivity dynamics

Abstract

Ongoing brain activity displays rich temporal variability associated with efficient cognition, with functional connectivity (FC) continually reconfiguring over time. The resulting functional connectivity dynamics (FCD) specifically show complex, fat-tailed statistics that alternate between persistent epochs and faster reconfiguration transients. While nonlinear whole-brain models tuned nearby a critical point have reproduced some aspects of FCD, they fall short of capturing its full temporal complexity. We propose that slow fluctuations in arousal offer a biologically plausible mechanism for exploring critical regimes in large-scale brain dynamics and thus enrich FCD. Using a connectome-based model of coupled cortical populations, we identified phase boundaries where system dynamics transition between regimes of faster or slower FCD. We then phenomenologically incorporated arousal changes, modeling them as stochastic fluctuations in key parameters such as cortical excitability, input gain, and noise amplitude. This non-autonomous formulation enables the system to roam dynamically across regime boundaries, flexibly tuning its distance from critical transition lines and producing intermittent transitions that mirror the stochastic evolution observed in empirical FCD. Fitting these models to human resting-state fMRI and performing model comparison, we find that arousal-driven models more accurately reproduce the distinctive quantitative features of FCD with the greatest improvements coming from the previously poorly accounted fat-tailed portions of the distributions. Together, these results suggest that arousal fluctuations -likely mediated by changes in neuromodulatory tone - shape the brains attractor landscape over time, expanding the repertoire of accessible functional network states and providing a mechanistic basis for the complexity of spontaneous functional dynamics.