Amplitude and phase coupling optimize information transfer between brain networks that function at criticality

Abstract

Brain function depends on segregation and integration of information processing in brain networks often separated by long-range anatomical connections. Neuronal oscillations orchestrate such distributed processing through transient amplitude and phase coupling, yet surprisingly little is known about local network properties facilitating these functional connections. Here, we test whether criticality--a dynamical state characterized by scale-free oscillations--optimizes the capacity of neuronal networks to couple through amplitude or phase, and transfer information. We coupled in silico networks with varying excitatory and inhibitory connectivity, and found that phase coupling emerges at criticality, and that amplitude coupling, as well as information transfer, are maximal when networks are critical. Importantly, regulating criticality through neuromodulation of synaptic strength showed that critical dynamics--as opposed to a static ratio of excitatory and inhibitory connections--optimize network coupling and information transfer. Our data support the idea that criticality is important for local and global information processing and may help explain why brain disorders characterized by local alterations in criticality also exhibit impaired long-range synchrony, even prior to degeneration of axonal connections.