Self-organized criticality and stochastic resonance in the human brain

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Doctoral thesis (article-based)
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40, [49]
The human brain spontaneously generates neuronal network oscillations at around 10 and 20 Hz with a large variability in amplitude, duration, and recurrence. Despite more than 70 years of research, the complex dynamics and functional significance of these oscillations have remained poorly understood. This Thesis concerns the dynamic character and functional significance of noninvasively recorded 10- and 20-Hz oscillations in the human brain. The hypotheses, experimental paradigms, data analyses, and interpretations of the results are inspired by recent insights from physics - most notable the theory of self-organized criticality and the phenomenon of stochastic resonance whose applicability to large-scale neuronal networks is explained. We show that amplitude fluctuations of 10- and 20-Hz oscillations during wakeful rest are correlated over thousands of oscillation cycles and that the decay of temporal correlations exhibits power-law scaling behavior. However, when these ongoing oscillations are perturbed with sensory stimuli, the amplitude attenuates quickly, reliably, and transiently, and the long-range temporal dynamics is affected as evidenced by changes in scaling exponents compared to rest. In addition to the rich temporal dynamics in local areas of the cortex, ongoing oscillations tend to synchronize their phases and exhibit correlated amplitude fluctuations across the two hemispheres, as shown for oscillations in homologous areas of the sensorimotor cortices. Finally, it is revealed that intermediate amplitude levels of ongoing oscillations provide the optimal oscillatory state of the sensorimotor cortex for reliable and quick conscious detection of weak somatosensory stimuli. We propose that the long-range temporal correlations, the power-law scaling behavior, the high susceptibility to stimulus perturbations, and the large amplitude variability of ongoing oscillations may find a unifying explanation within the theory of self-organized criticality. This theory offers a general mechanism for the ubiquitous emergence of complex dynamics with power-law decay of spatiotemporal correlations in non-linear self-organizing stochastic systems consisting of many units. The optimal ability to detect consciously and respond behaviorally to weak somatosensory stimuli at intermediate levels of ongoing sensorimotor oscillations is attributed to stochastic resonance - the intuitively paradoxical phenomenon that the signal-to-noise ratio of detecting or transmitting a signal in a non-linear system can be enhanced by noise. Based on the above results, we conjecture that a mechanism of intrinsic stochastic resonance between self-organized critical and stimulus-induced activities may be a general organizing principle of great importance for central nervous system function and account for some of the variability in the way we perceive and react to the outside world.
neuroscience, complexity physics, neuronal population dynamics, avalanche dynamics, spontaneous or ongoing oscillations, self-organization, variability, criticality, brain states, stochastic resonance, correlations, scaling behavior
Other note
  • Linkenkaer-Hansen K, Nikouline VV, Palva JM, Ilmoniemi RJ. Long-range temporal correlations and scaling behavior in human brain oscillations. The Journal of Neuroscience, 21:1370-1377, 2001.
  • Nikouline VV, Wikström H, Linkenkaer-Hansen K, Kesäniemi M, Ilmoniemi RJ, Huttunen J. Somatosensory evoked magnetic fields: relation to pre-stimulus mu rhythm. Clinical Neurophysiology 111:1227-1233, 2000.
  • Nikouline VV, Linkenkaer-Hansen K, Wikström H, Kesäniemi M, Antonova EV, Ilmoniemi RJ, Huttunen J. Dynamics of mu-rhythm suppression caused by median nerve stimulation: a magnetoencephalographic study in human subjects. Neuroscience Letters 294:163-166, 2000.
  • Nikouline VV, Linkenkaer-Hansen K, Huttunen J, Ilmoniemi RJ. Interhemispheric phase synchrony and amplitude correlation of spontaneous beta oscillations in human subjects: a magnetoencephalographic study. NeuroReport 12:2487-2491, 2001.
  • Linkenkaer-Hansen K, Nikulin VV, Palva JM, Kaila K, Ilmoniemi RJ. Stimulus-induced change in long-range temporal correlations and scaling behavior of sensorimotor oscillations. TKK-F-A815 (2002). ISSN: 1456-3320. ISBN: 951-22-6176-6.
  • Linkenkaer-Hansen K, Nikulin VV, Palva S, Ilmoniemi RJ, Palva JM. Intrinsic stochastic resonance of sensorimotor processing mediated by ongoing neuronal oscillations. TKK-F-A816 (2002). ISSN: 1456-3320. ISBN: 951-22-6177-4.
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