Abstract

Whether the brain operates at a critical "tipping" point is a long standing scientific question, with evidence from both cellular and systems-scale studies suggesting that the brain does sit in, or near, a critical regime. Neuroimaging studies of humans in altered states of consciousness have prompted the suggestion that maintenance of critical dynamics is necessary for the emergence of consciousness and complex cognition, and that reduced or disorganized consciousness may be associated with deviations from criticality. Unfortunately, many of the cellular-level studies reporting signs of criticality were performed in non-conscious systems (in vitro neuronal cultures) or unconscious animals (e.g. anaesthetized rats). Here we attempted to address this knowledge gap by exploring critical brain dynamics in invasive ECoG recordings from multiple sessions with a single macaque as the animal transitioned from consciousness to unconsciousness under different anaesthetics (ketamine and propofol). We use a previously-validated test of criticality: avalanche dynamics to assess the differences in brain dynamics between normal consciousness and both drug-states. Propofol and ketamine were selected due to their differential effects on consciousness (ketamine, but not propofol, is known to induce an unusual state known as "dissociative anaesthesia"). Our analyses indicate that propofol dramatically restricted the size and duration of avalanches, while ketamine allowed for more awake-like dynamics to persist. In addition, propofol, but not ketamine, triggered a large reduction in the complexity of brain dynamics. All states, however, showed some signs of persistent criticality when testing for exponent relations and universal shape-collapse. Further, maintenance of critical brain dynamics may be important for regulation and control of conscious awareness.

Highlights

  • The hypothesis that the brain operates in a critical regime near a “tipping” point between different states is growing in popularity, both on neurophysiological evidence and due to appealing properties of critical, or near-critical, systems [1], that are thought to be key elements of optimal nervous system functioning

  • We found large differences between the channel rates following the administration of both ketamine and propofol

  • The correlation between channel activity rates before and after ketamine induction was 0.225 (p-value > 0.05) and the correlation between channel activity before and after propofol induction was 0.06 (p-value > 0.05). These results suggest a much higher degree of dynamical similarity within conditions scanned on different days than between conditions induced during a single scan

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Summary

Introduction

The hypothesis that the brain operates in a critical regime near a “tipping” point between different states (often, but not always, described as low and high entropy, respectively) is growing in popularity, both on neurophysiological evidence and due to appealing properties of critical, or near-critical, systems [1], that are thought to be key elements of optimal nervous system functioning In both in vivo recordings and simulations, critical systems show the widest dynamic range [2,3,4,5], which indicates that critical systems can respond to, and amplify, a broad range of signals. The “critical brain” hypothesis has not been universally accepted [21], and disagreement remains within the field as to when it is acceptable to conclude data was produced by a critical or near-critical system [17]

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