Variability and task-responsiveness of electrophysiological dynamics: Scale-free stability and oscillatory flexibility
Soren Wainio-Theberge,
Annemarie Wolff,
Javier Gomez-Pilar,
Jianfeng Zhang,
Georg Northoff
Affiliations
Soren Wainio-Theberge
Mind, Brain Imaging, and Neuroethics Unit, Institute of Mental Health Research, Royal Ottawa Mental Health Centre, University of Ottawa, 1145 Carling Avenue, Rm. 6435, Ottawa, ON K1Z 7K4, Canada; Integrated Program in Neuroscience, McGill University, Montréal, QC, Canada; Corresponding authors at: Mind, Brain Imaging, and Neuroethics Unit, Institute of Mental Health Research, Royal Ottawa Mental Health Centre, University of Ottawa, 1145 Carling Avenue, Rm. 6435, Ottawa, ON K1Z 7K4, Canada.
Annemarie Wolff
Mind, Brain Imaging, and Neuroethics Unit, Institute of Mental Health Research, Royal Ottawa Mental Health Centre, University of Ottawa, 1145 Carling Avenue, Rm. 6435, Ottawa, ON K1Z 7K4, Canada
Javier Gomez-Pilar
Biomedical Engineering Group, University of Valladolid, Paseo de Belén, 15, Valladolid 47011, Spain; Centro de Investigación Biomédica en Red en Bioingeniería, Biomateriales y Nanomedicina, (CIBER-BBN), Valladolid, Spain
Jianfeng Zhang
Mental Health Centre/7th Hospital, Zhejiang University School of Medicine, Tianmu Road 305, Hangzhou, Zhejiang 310013, China; College of Biomedical Engineering and Instrument Sciences, Zhejiang University, Hangzhou, China
Georg Northoff
Mind, Brain Imaging, and Neuroethics Unit, Institute of Mental Health Research, Royal Ottawa Mental Health Centre, University of Ottawa, 1145 Carling Avenue, Rm. 6435, Ottawa, ON K1Z 7K4, Canada; Mental Health Centre/7th Hospital, Zhejiang University School of Medicine, Tianmu Road 305, Hangzhou, Zhejiang 310013, China; Centre for Cognition and Brain Disorders, Hangzhou Normal University, Hangzhou, Zhejiang 311121, China; Corresponding authors at: Mind, Brain Imaging, and Neuroethics Unit, Institute of Mental Health Research, Royal Ottawa Mental Health Centre, University of Ottawa, 1145 Carling Avenue, Rm. 6435, Ottawa, ON K1Z 7K4, Canada.
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.
