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The Journal of Neuroscience, July 1, 2009, 29(26):8512-8524; doi:10.1523/JNEUROSCI.0754-09.2009

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Behavioral/Systems/Cognitive
Bistability and Non-Gaussian Fluctuations in Spontaneous Cortical Activity

Frank Freyer,^1,2 Kevin Aquino,^4,6 Peter A. Robinson,^4,5,7 Petra Ritter,^1,2,3 and Michael Breakspear^6,8

¹Berlin Neuroimaging Center and Department of Neurology, Charité Universitaetsmedizin, and ²Bernstein Center for Computational Neuroscience, and ³Graduate School of Mind and Brain and Mind and Brain Institute, Faculty of Philosophy, Humboldt University, 10117 Berlin, Germany, ⁴School of Physics and ⁵Faculty of Medicine, University of Sydney, Sydney, New South Wales 2006, Australia, ⁶School of Psychiatry, University of New South Wales and The Black Dog Institute, Sydney, New South Wales 2031, Australia, ⁷Brain Dynamics Center, Westmead Millennium Institute, Westmead Hospital and University of Sydney, Westmead, New South Wales 2145, Australia, and ⁸Queensland Institute of Medical Research and the Royal Brisbane and Woman's Hospital, Brisbane, Queensland 4006, Australia

Correspondence should be addressed to Michael Breakspear, Queensland Institute for Medical Research, Herston, QLD 4006, Australia. Email: Michael.Breakspear{at}qimr.edu.au

The brain is widely assumed to be a paradigmatic example of a complex, self-organizing system. As such, it should exhibit the classic hallmarks of nonlinearity, multistability, and "nondiffusivity" (large coherent fluctuations). Surprisingly, at least at the very large scale of neocortical dynamics, there is little empirical evidence to support this, and hence most computational and methodological frameworks for healthy brain activity have proceeded very reasonably from a purely linear and diffusive perspective. By studying the temporal fluctuations of power in human resting-state electroencephalograms, we show that, although these simple properties may hold true at some temporal scales, there is strong evidence for bistability and nondiffusivity in key brain rhythms. Bistability is manifest as nonclassic bursting between high- and low-amplitude modes in the alpha rhythm. Nondiffusivity is expressed through the irregular appearance of high amplitude "extremal" events in beta rhythm power fluctuations. The statistical robustness of these observations was confirmed through comparison with Gaussian-rendered phase-randomized surrogate data. Although there is a good conceptual framework for understanding bistability in cortical dynamics, the implications of the extremal events challenge existing frameworks for understanding large-scale brain systems.

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Received Jan. 29, 2009; revised May 26, 2009; accepted May 27, 2009.

Correspondence should be addressed to Michael Breakspear, Queensland Institute for Medical Research, Herston, QLD 4006, Australia. Email: Michael.Breakspear{at}qimr.edu.au

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