  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. To address this issue, we employed chronically
implanted multielectrode arrays (MEA) to record avalanches of spikes from the
cerebral cortex (V1 and S1) and hippocampus (HP) 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. 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 V1, S1 and HP. 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.
