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

Ribeiro, Tiago L

Copelli, Mauro

Caixeta, Fábio

Belchior, Hindiael

Chialvo, Dante R

Nicolelis, Miguel AL

Ribeiro, Sidarta

United States

2011-06-21T17:32:20Z

2010-11-30

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.

Version of Record

http://www.ncbi.nlm.nih.gov/pubmed/21152422

1932-6203

https://hdl.handle.net/10161/4584

eng

en_US

Public Library of Science (PLoS)

PLoS One

10.1371/journal.pone.0014129

Plos One

Action Potentials

Anesthesia

Animals

Brain

Cerebral Cortex

Hippocampus

Male

Models, Neurological

Neurons

Rats

Rats, Long-Evans

Sleep

Synaptic Transmission

Wakefulness

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

Journal article

2010-11-30

11

5

http://www.ncbi.nlm.nih.gov/pubmed/21152422

e14129

11

Basic Science Departments

Biomedical Engineering

Clinical Science Departments

Duke

Duke Institute for Brain Sciences

Institutes and Provost's Academic Units

Neurobiology

Neurology

Neurology, Behavioral Neurology

Orthopaedics

Pratt School of Engineering

Psychology and Neuroscience

School of Medicine

Trinity College of Arts & Sciences

University Institutes and Centers

Published online

5