Critical-like bistable dynamics in the resting-state human brain

Abstract

Brain activity exhibits scale-free avalanche dynamics and power-law long-range temporal correlations (LRTCs) across the nervous system. This has been thought to reflect “brain criticality”, i.e., brains operating near a critical phase transition between disorder and excessive order. Neuronal activity is, however, metabolically costly and may be constrained by activity-limiting mechanisms and resource depletion, which could make the phase transition discontinuous and bistable. Observations of bistability in awake human brain activity have nonetheless remained scarce and its functional significance unclear. First, using computational modelling where bistable synchronization dynamics emerged through local positive feedback, we found bistability to occur exclusively in a regime of critical-like dynamics. We then assessed bistability in vivo with resting-state magnetoencephalography and stereo-encephalography. Bistability was a robust characteristic of cortical oscillations throughout frequency bands from δ (3-7 Hz) to high-γ (100-225 Hz). As predicted by modelling, bistability and LRTCs were positively correlated. Importantly, while moderate levels of bistability were positively correlated with executive functioning, excessive bistability was associated with epileptic pathophysiology and predictive of local epileptogenicity. Critical bistability is thus a salient feature of spontaneous human brain dynamics in awake resting-state and is both functionally and clinically significant. These findings expand the framework of brain criticality and show that critical-like neuronal dynamics in vivo involves both continuous and discontinuous phase transitions in a frequency-, neuroanatomy-, and state-dependent manner.