Variability and task-responsiveness of electrophysiological dynamics: Scale-free stability and oscillatory flexibility.

Cortical oscillations and scale-free neural activity are thought to influence a variety of cognitive functions, but their differential relationships to neural stability and flexibility has never been investigated. Based on the existing literature, we hypothesize that scale-free and oscillatory processes in the brain exhibit different trade-offs between stability and flexibility; specifically, cortical oscillations may reflect variable, task-responsive aspects of brain activity, while scale-free activity is proposed to reflect a more stable and task-unresponsive aspect. We test this hypothesis using data from two large-scale MEG studies (HCP: n = 89; CamCAN: n = 195), operationalizing stability and flexibility by task-responsiveness and spontaneous intra-subject variability in resting state. We demonstrate that the power-law exponent of scale-free activity is a highly stable parameter, which responds little to external cognitive demands and shows minimal spontaneous fluctuations over time. In contrast, oscillatory power, particularly in the alpha range (8-13 Hz), responds strongly to tasks and exhibits comparatively large spontaneous fluctuations over time. In sum, our data support differential roles for oscillatory and scale-free activity in the brain with respect to neural stability and flexibility. This result carries implications for criticality-based theories of scale-free activity, state-trait models of variability, and homeostatic views of the brain with regulated variables vs. effectors.