Spike avalanches exhibit universal dynamics across the sleep-wake cycle.


BACKGROUND: Scale-invariant neuronal avalanches have been observed in cell cultures and slices as well as anesthetized and awake brains, suggesting that the brain operates near criticality, i.e. within a narrow margin between avalanche propagation and extinction. In theory, criticality provides many desirable features for the behaving brain, optimizing computational capabilities, information transmission, sensitivity to sensory stimuli and size of memory repertoires. However, a thorough characterization of neuronal avalanches in freely-behaving (FB) animals is still missing, thus raising doubts about their relevance for brain function. METHODOLOGY/PRINCIPAL FINDINGS: To address this issue, we employed chronically implanted multielectrode arrays (MEA) to record avalanches of action potentials (spikes) from the cerebral cortex and hippocampus of 14 rats, as they spontaneously traversed the wake-sleep cycle, explored novel objects or were subjected to anesthesia (AN). We then modeled spike avalanches to evaluate the impact of sparse MEA sampling on their statistics. We found that the size distribution of spike avalanches are well fit by lognormal distributions in FB animals, and by truncated power laws in the AN group. FB data surrogation markedly decreases the tail of the distribution, i.e. spike shuffling destroys the largest avalanches. The FB data are also characterized by multiple key features compatible with criticality in the temporal domain, such as 1/f spectra and long-term correlations as measured by detrended fluctuation analysis. These signatures are very stable across waking, slow-wave sleep and rapid-eye-movement sleep, but collapse during anesthesia. Likewise, waiting time distributions obey a single scaling function during all natural behavioral states, but not during anesthesia. Results are equivalent for neuronal ensembles recorded from visual and tactile areas of the cerebral cortex, as well as the hippocampus. CONCLUSIONS/SIGNIFICANCE: Altogether, the data provide a comprehensive link between behavior and brain criticality, revealing a unique scale-invariant regime of spike avalanches across all major behaviors.





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Publication Info

Ribeiro, Tiago L, Mauro Copelli, Fábio Caixeta, Hindiael Belchior, Dante R Chialvo, Miguel AL Nicolelis and Sidarta Ribeiro (2010). Spike avalanches exhibit universal dynamics across the sleep-wake cycle. PLoS One, 5(11). p. e14129. 10.1371/journal.pone.0014129 Retrieved from https://hdl.handle.net/10161/4584.

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Miguel Angelo L. Nicolelis

Professor Emeritus of Neurobiology

Miguel Nicolelis, M.D., Ph.D., is the Duke School of Medicine Distinguished Professor of Neuroscience, Duke University Professor of Neurobiology, Biomedical Engineering and Psychology and Neuroscience, and founder of Duke's Center for Neuroengineering. He is the founder and Scientific Director of the Edmond and Lily Safra International Institute for Neuroscience of Natal.  Dr. Nicolelis is also founder of the Walk Again Project, an international consortium of scientists and engineers, dedicated to the development of an exoskeleton device to assist severely paralyzed patients in regaining full body mobility.

Dr. Nicolelis has dedicated his career to investigate how the brains of freely behaving animals encode sensory and motor information. As a result of his studies, Dr. Nicolelis was first to propose and demonstrate that animals and human subjects can utilize their electrical brain activity to directly control neuroprosthetic devices via brain-machine interfaces (BMI).

Over the past 25 years, Dr. Nicolelis pioneered and perfected the development of a new neurophysiological method, known today as chronic, multi-site, multi-electrode recordings. Using this approach in a variety of animal species, as well as in intra-operative procedures in human patients, Dr. Nicolelis launched a new field of investigation, which aims at measuring the concurrent activity and interactions of large populations of single neurons throughout the brain. Through his work, Dr. Nicolelis has discovered a series of key physiological principles that govern the operation of mammalian brain circuits.

Dr. Nicolelis pioneering BMI studies have become extremely influential since they offer new potential therapies for patients suffering from severe levels of paralysis, Parkinson’s disease, and epilepsy. Today, numerous neuroscience laboratories in the US, Europe, Asia, and Latin America have incorporated Dr. Nicolelis' experimental paradigm to study a variety of mammalian neuronal systems. His research has influenced basic and applied research in computer science, robotics, and biomedical engineering. 

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