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Differential effects of propofol and ketamine on critical brain dynamics

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 prompt...

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Autores principales: Varley, Thomas F., Sporns, Olaf, Puce, Aina, Beggs, John
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2020
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7785236/
https://www.ncbi.nlm.nih.gov/pubmed/33347455
http://dx.doi.org/10.1371/journal.pcbi.1008418
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author Varley, Thomas F.
Sporns, Olaf
Puce, Aina
Beggs, John
author_facet Varley, Thomas F.
Sporns, Olaf
Puce, Aina
Beggs, John
author_sort Varley, Thomas F.
collection PubMed
description 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.
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spelling pubmed-77852362021-01-13 Differential effects of propofol and ketamine on critical brain dynamics Varley, Thomas F. Sporns, Olaf Puce, Aina Beggs, John PLoS Comput Biol Research Article 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. Public Library of Science 2020-12-21 /pmc/articles/PMC7785236/ /pubmed/33347455 http://dx.doi.org/10.1371/journal.pcbi.1008418 Text en © 2020 Varley et al http://creativecommons.org/licenses/by/4.0/ This is an open access article distributed under the terms of the Creative Commons Attribution License (http://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Varley, Thomas F.
Sporns, Olaf
Puce, Aina
Beggs, John
Differential effects of propofol and ketamine on critical brain dynamics
title Differential effects of propofol and ketamine on critical brain dynamics
title_full Differential effects of propofol and ketamine on critical brain dynamics
title_fullStr Differential effects of propofol and ketamine on critical brain dynamics
title_full_unstemmed Differential effects of propofol and ketamine on critical brain dynamics
title_short Differential effects of propofol and ketamine on critical brain dynamics
title_sort differential effects of propofol and ketamine on critical brain dynamics
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC7785236/
https://www.ncbi.nlm.nih.gov/pubmed/33347455
http://dx.doi.org/10.1371/journal.pcbi.1008418
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