Metastable dynamics emerge from local excitatory–inhibitory homeostasis in the cortex at rest

Abstract

The dynamics of the human cortex are highly metastable, driving the spontaneous exploration of network states. This metastability depends on circuit-level edge-of-bifurcation dynamics, which emerge from firing-rate control through multiple mechanisms of excitatory–inhibitory (E–I) homeostasis. However, it is unclear how these contribute to the metastability of cortical networks. We propose that individual mechanisms of the E–I homeostasis contribute uniquely to the emergence of resting-state dynamics and test this hypothesis in a large-scale model of the human cortex. We show that empirical connectivity and dynamics can only be reproduced when accounting for multiple mechanisms of the E–I homeostasis. More specifically, while the homeostasis of excitation and inhibition enhances metastability, the regulation of intrinsic excitability ensures moderate synchrony, maximizing functional complexity. Furthermore, the modulation bifurcation modulation by the homeostasis of excitation and intrinsic excitability compensates for strong input fluctuations in connector hubs. Importantly, this only occurs in models accounting for local gamma oscillations, suggesting a relationship between E–I balance, gamma rhythms, and metastable dynamics. Altogether, our results show that cortical networks self-organize toward maximal metastability through the multifactor homeostasis of E–I balance. Therefore, the benefits of combining multiple homeostatic mechanisms transcend the circuit level, supporting the metastable dynamics of large-scale cortical networks.