Neuronal Avalanches Differ from Wakefulness to Deep Sleep – Evidence from Intracranial Depth Recordings in Humans

Abstract

Neuronal activity differs between wakefulness and sleep states. In contrast, an attractor state, called self-organized critical (SOC), was proposed to govern brain dynamics because it allows for optimal information coding. But is the human brain SOC for each vigilance state despite the variations in neuronal dynamics? We characterized neuronal avalanches – spatiotemporal waves of enhanced activity - from dense intracranial depth recordings in humans. We showed that avalanche distributions closely follow a power law – the hallmark feature of SOC - for each vigilance state. However, avalanches clearly differ with vigilance states: slow wave sleep (SWS) shows large avalanches, wakefulness intermediate, and rapid eye movement (REM) sleep small ones. Our SOC model, together with the data, suggested first that the differences are mediated by global but tiny changes in synaptic strength, and second, that the changes with vigilance states reflect small deviations from criticality to the subcritical regime, implying that the human brain does not operate at criticality proper but close to SOC. Independent of criticality, the analysis confirms that SWS shows increased correlations between cortical areas, and reveals that REM sleep shows more fragmented cortical dynamics.

Breakdown of long-range temporal dependence in default mode and attention networks during deep sleep

“…The observed H exponent modulation by sleep prompts the possibility that self-organizing criticality in the human brain is not a trivial and unavoidable consequence of physical laws but rather, contributes to define the dynamical regime of conscious resting state activity, which can be changed during altered states of consciousness. A recent study reported changes in the power law distribution of neural avalanches measured with intracranial recordings during deep sleep, which is also consistent with this conjecture (53).…”

Large-scale signatures of unconsciousness are consistent with a departure from critical dynamics

“…Conversely, at the sub-or supercritical states, sensory stimulation results in a local and transient perturbation failing to propagate to more widespread networks related to conscious perception. At other spatial and temporal scales, evidence for an association between consciousness and critical dynamics has been obtained in the context of deep sleep [44], anaesthesia [45,46] and epileptic seizures [47]. Here, we introduced the coupling between anatomical and functional connectivity as a signature of the critical state, which is particularly fit for fMRI recordings, because both can be measured at the same spatial resolution using this technique.…”

Firing patterns in a random network cellular automata model of the brain

“…In a previous work, one of us showed that, under the assumption that EEG is a statistical epiphenomenon at the mesoscopic level, we can qualitative match the high amplitude deep sleep signals and the low amplitude alpha rhythms with different phases of a CA model in a complete graph [39]. The monitoring of neuronal avalanches from intracranial depth recordings in slow wave sleep, wakefulness and REM states also shows different behaviour concordant with small changes in synaptic strength [40]. In principle, the neuronal avalanche distributions could also be simulated by the CA model in order to obtain a measure of the synaptic strength in each state in terms of the excitation and inhibition probabilities.…”