Loss of consciousness is associated with stabilization of cortical activity

Autores
Solovey, Guillermo; Alonso, Leandro Martín; Yanagawa, Toru; Fujii, Naotaka; Magnasco, Marcelo Osvaldo; Cecchi, Guillermo Alberto; Proekt, Alex
Año de publicación
2015
Idioma
inglés
Tipo de recurso
artículo
Estado
versión publicada
Descripción
What aspects of neuronal activity distinguish the conscious from the unconscious brain? This has been a subject of intense interest and debate since the early days of neurophysiology. However, as any practicing anesthesiologist can attest, it is currently not possible to reliably distinguish a conscious state from an unconscious one on the basis of brain activity. Here we approach this problem from the perspective of dynamical systems theory. We argue that the brain, as a dynamical system, is self-regulated at the boundary between stable and unstable regimes, allowing it in particular to maintain high susceptibility to stimuli. To test this hypothesis, we performed stability analysis of high-density electrocorticography recordings covering an entire cerebral hemisphere in monkeys during reversible loss of consciousness. We show that, during loss of consciousness, the number of eigenmodes at the edge of instability decreases smoothly, independently of the type of anesthetic and specific features of brain activity. The eigenmodes drift back toward the unstable line during recovery of consciousness. Furthermore, we show that stability is an emergent phenomenon dependent on the correlations among activity in different cortical regions rather than signals taken in isolation. These findings support the conclusion that dynamics at the edge of instability are essential for maintaining consciousness and provide a novel and principled measure that distinguishes between the conscious and the unconscious brain. Significance Statement: What distinguishes brain activity during consciousness from that observed during unconsciousness? Answering this question has proven difficult because neither consciousness nor lack thereof have universal signatures in terms of most specific features of brain activity. For instance, different anesthetics induce different patterns of brain activity. We demonstrate that loss of consciousness is universally and reliably associated with stabilization of cortical dynamics regardless of the specific activity characteristics. To give an analogy, our analysis suggests that loss of consciousness is akin to depressing the damper pedal on the piano, which makes the sounds dissipate quicker regardless of the specific melody being played. This approach may prove useful in detecting consciousness on the basis of brain activity under anesthesia and other settings.
Fil: Solovey, Guillermo. The Rockefeller University; Estados Unidos. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Física. Laboratorio de Neurociencia Integrativa; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Cálculo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Alonso, Leandro Martín. The Rockefeller University; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Yanagawa, Toru. RIKEN Brain Science Institute; Japón
Fil: Fujii, Naotaka. RIKEN Brain Science Institute; Japón
Fil: Magnasco, Marcelo Osvaldo. The Rockefeller University; Estados Unidos
Fil: Cecchi, Guillermo Alberto. IBM Research. Thomas J. Watson Research Center; Estados Unidos
Fil: Proekt, Alex. The Rockefeller University; Estados Unidos. Weill Medical Center; Estados Unidos
Materia
ANESTHESIA
CONSCIOUSNESS
DYNAMICAL CRITICALITY
DYNAMICAL SYSTEMS
ECOG
STABILITY ANALYSIS
Nivel de accesibilidad
acceso abierto
Condiciones de uso
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
Repositorio
CONICET Digital (CONICET)
Institución
Consejo Nacional de Investigaciones Científicas y Técnicas
OAI Identificador
oai:ri.conicet.gov.ar:11336/59582

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network_name_str CONICET Digital (CONICET)
spelling Loss of consciousness is associated with stabilization of cortical activitySolovey, GuillermoAlonso, Leandro MartínYanagawa, ToruFujii, NaotakaMagnasco, Marcelo OsvaldoCecchi, Guillermo AlbertoProekt, AlexANESTHESIACONSCIOUSNESSDYNAMICAL CRITICALITYDYNAMICAL SYSTEMSECOGSTABILITY ANALYSIShttps://purl.org/becyt/ford/1.6https://purl.org/becyt/ford/1What aspects of neuronal activity distinguish the conscious from the unconscious brain? This has been a subject of intense interest and debate since the early days of neurophysiology. However, as any practicing anesthesiologist can attest, it is currently not possible to reliably distinguish a conscious state from an unconscious one on the basis of brain activity. Here we approach this problem from the perspective of dynamical systems theory. We argue that the brain, as a dynamical system, is self-regulated at the boundary between stable and unstable regimes, allowing it in particular to maintain high susceptibility to stimuli. To test this hypothesis, we performed stability analysis of high-density electrocorticography recordings covering an entire cerebral hemisphere in monkeys during reversible loss of consciousness. We show that, during loss of consciousness, the number of eigenmodes at the edge of instability decreases smoothly, independently of the type of anesthetic and specific features of brain activity. The eigenmodes drift back toward the unstable line during recovery of consciousness. Furthermore, we show that stability is an emergent phenomenon dependent on the correlations among activity in different cortical regions rather than signals taken in isolation. These findings support the conclusion that dynamics at the edge of instability are essential for maintaining consciousness and provide a novel and principled measure that distinguishes between the conscious and the unconscious brain. Significance Statement: What distinguishes brain activity during consciousness from that observed during unconsciousness? Answering this question has proven difficult because neither consciousness nor lack thereof have universal signatures in terms of most specific features of brain activity. For instance, different anesthetics induce different patterns of brain activity. We demonstrate that loss of consciousness is universally and reliably associated with stabilization of cortical dynamics regardless of the specific activity characteristics. To give an analogy, our analysis suggests that loss of consciousness is akin to depressing the damper pedal on the piano, which makes the sounds dissipate quicker regardless of the specific melody being played. This approach may prove useful in detecting consciousness on the basis of brain activity under anesthesia and other settings.Fil: Solovey, Guillermo. The Rockefeller University; Estados Unidos. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Física. Laboratorio de Neurociencia Integrativa; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Cálculo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Alonso, Leandro Martín. The Rockefeller University; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas; ArgentinaFil: Yanagawa, Toru. RIKEN Brain Science Institute; JapónFil: Fujii, Naotaka. RIKEN Brain Science Institute; JapónFil: Magnasco, Marcelo Osvaldo. The Rockefeller University; Estados UnidosFil: Cecchi, Guillermo Alberto. IBM Research. Thomas J. Watson Research Center; Estados UnidosFil: Proekt, Alex. The Rockefeller University; Estados Unidos. Weill Medical Center; Estados UnidosSociety for Neuroscience2015-07info:eu-repo/semantics/articleinfo:eu-repo/semantics/publishedVersionhttp://purl.org/coar/resource_type/c_6501info:ar-repo/semantics/articuloapplication/pdfapplication/pdfhttp://hdl.handle.net/11336/59582Solovey, Guillermo; Alonso, Leandro Martín; Yanagawa, Toru; Fujii, Naotaka; Magnasco, Marcelo Osvaldo; et al.; Loss of consciousness is associated with stabilization of cortical activity; Society for Neuroscience; Journal of Neuroscience; 35; 30; 7-2015; 10866-108770270-6474CONICET DigitalCONICETenginfo:eu-repo/semantics/altIdentifier/doi/10.1523/JNEUROSCI.4895-14.2015info:eu-repo/semantics/altIdentifier/url/http://www.jneurosci.org/content/35/30/10866info:eu-repo/semantics/openAccesshttps://creativecommons.org/licenses/by-nc-sa/2.5/ar/reponame:CONICET Digital (CONICET)instname:Consejo Nacional de Investigaciones Científicas y Técnicas2025-09-17T11:21:06Zoai:ri.conicet.gov.ar:11336/59582instacron:CONICETInstitucionalhttp://ri.conicet.gov.ar/Organismo científico-tecnológicoNo correspondehttp://ri.conicet.gov.ar/oai/requestdasensio@conicet.gov.ar; lcarlino@conicet.gov.arArgentinaNo correspondeNo correspondeNo correspondeopendoar:34982025-09-17 11:21:07.14CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicasfalse
dc.title.none.fl_str_mv Loss of consciousness is associated with stabilization of cortical activity
title Loss of consciousness is associated with stabilization of cortical activity
spellingShingle Loss of consciousness is associated with stabilization of cortical activity
Solovey, Guillermo
ANESTHESIA
CONSCIOUSNESS
DYNAMICAL CRITICALITY
DYNAMICAL SYSTEMS
ECOG
STABILITY ANALYSIS
title_short Loss of consciousness is associated with stabilization of cortical activity
title_full Loss of consciousness is associated with stabilization of cortical activity
title_fullStr Loss of consciousness is associated with stabilization of cortical activity
title_full_unstemmed Loss of consciousness is associated with stabilization of cortical activity
title_sort Loss of consciousness is associated with stabilization of cortical activity
dc.creator.none.fl_str_mv Solovey, Guillermo
Alonso, Leandro Martín
Yanagawa, Toru
Fujii, Naotaka
Magnasco, Marcelo Osvaldo
Cecchi, Guillermo Alberto
Proekt, Alex
author Solovey, Guillermo
author_facet Solovey, Guillermo
Alonso, Leandro Martín
Yanagawa, Toru
Fujii, Naotaka
Magnasco, Marcelo Osvaldo
Cecchi, Guillermo Alberto
Proekt, Alex
author_role author
author2 Alonso, Leandro Martín
Yanagawa, Toru
Fujii, Naotaka
Magnasco, Marcelo Osvaldo
Cecchi, Guillermo Alberto
Proekt, Alex
author2_role author
author
author
author
author
author
dc.subject.none.fl_str_mv ANESTHESIA
CONSCIOUSNESS
DYNAMICAL CRITICALITY
DYNAMICAL SYSTEMS
ECOG
STABILITY ANALYSIS
topic ANESTHESIA
CONSCIOUSNESS
DYNAMICAL CRITICALITY
DYNAMICAL SYSTEMS
ECOG
STABILITY ANALYSIS
purl_subject.fl_str_mv https://purl.org/becyt/ford/1.6
https://purl.org/becyt/ford/1
dc.description.none.fl_txt_mv What aspects of neuronal activity distinguish the conscious from the unconscious brain? This has been a subject of intense interest and debate since the early days of neurophysiology. However, as any practicing anesthesiologist can attest, it is currently not possible to reliably distinguish a conscious state from an unconscious one on the basis of brain activity. Here we approach this problem from the perspective of dynamical systems theory. We argue that the brain, as a dynamical system, is self-regulated at the boundary between stable and unstable regimes, allowing it in particular to maintain high susceptibility to stimuli. To test this hypothesis, we performed stability analysis of high-density electrocorticography recordings covering an entire cerebral hemisphere in monkeys during reversible loss of consciousness. We show that, during loss of consciousness, the number of eigenmodes at the edge of instability decreases smoothly, independently of the type of anesthetic and specific features of brain activity. The eigenmodes drift back toward the unstable line during recovery of consciousness. Furthermore, we show that stability is an emergent phenomenon dependent on the correlations among activity in different cortical regions rather than signals taken in isolation. These findings support the conclusion that dynamics at the edge of instability are essential for maintaining consciousness and provide a novel and principled measure that distinguishes between the conscious and the unconscious brain. Significance Statement: What distinguishes brain activity during consciousness from that observed during unconsciousness? Answering this question has proven difficult because neither consciousness nor lack thereof have universal signatures in terms of most specific features of brain activity. For instance, different anesthetics induce different patterns of brain activity. We demonstrate that loss of consciousness is universally and reliably associated with stabilization of cortical dynamics regardless of the specific activity characteristics. To give an analogy, our analysis suggests that loss of consciousness is akin to depressing the damper pedal on the piano, which makes the sounds dissipate quicker regardless of the specific melody being played. This approach may prove useful in detecting consciousness on the basis of brain activity under anesthesia and other settings.
Fil: Solovey, Guillermo. The Rockefeller University; Estados Unidos. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Departamento de Física. Laboratorio de Neurociencia Integrativa; Argentina. Universidad de Buenos Aires. Facultad de Ciencias Exactas y Naturales. Instituto de Cálculo; Argentina. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Alonso, Leandro Martín. The Rockefeller University; Estados Unidos. Consejo Nacional de Investigaciones Científicas y Técnicas; Argentina
Fil: Yanagawa, Toru. RIKEN Brain Science Institute; Japón
Fil: Fujii, Naotaka. RIKEN Brain Science Institute; Japón
Fil: Magnasco, Marcelo Osvaldo. The Rockefeller University; Estados Unidos
Fil: Cecchi, Guillermo Alberto. IBM Research. Thomas J. Watson Research Center; Estados Unidos
Fil: Proekt, Alex. The Rockefeller University; Estados Unidos. Weill Medical Center; Estados Unidos
description What aspects of neuronal activity distinguish the conscious from the unconscious brain? This has been a subject of intense interest and debate since the early days of neurophysiology. However, as any practicing anesthesiologist can attest, it is currently not possible to reliably distinguish a conscious state from an unconscious one on the basis of brain activity. Here we approach this problem from the perspective of dynamical systems theory. We argue that the brain, as a dynamical system, is self-regulated at the boundary between stable and unstable regimes, allowing it in particular to maintain high susceptibility to stimuli. To test this hypothesis, we performed stability analysis of high-density electrocorticography recordings covering an entire cerebral hemisphere in monkeys during reversible loss of consciousness. We show that, during loss of consciousness, the number of eigenmodes at the edge of instability decreases smoothly, independently of the type of anesthetic and specific features of brain activity. The eigenmodes drift back toward the unstable line during recovery of consciousness. Furthermore, we show that stability is an emergent phenomenon dependent on the correlations among activity in different cortical regions rather than signals taken in isolation. These findings support the conclusion that dynamics at the edge of instability are essential for maintaining consciousness and provide a novel and principled measure that distinguishes between the conscious and the unconscious brain. Significance Statement: What distinguishes brain activity during consciousness from that observed during unconsciousness? Answering this question has proven difficult because neither consciousness nor lack thereof have universal signatures in terms of most specific features of brain activity. For instance, different anesthetics induce different patterns of brain activity. We demonstrate that loss of consciousness is universally and reliably associated with stabilization of cortical dynamics regardless of the specific activity characteristics. To give an analogy, our analysis suggests that loss of consciousness is akin to depressing the damper pedal on the piano, which makes the sounds dissipate quicker regardless of the specific melody being played. This approach may prove useful in detecting consciousness on the basis of brain activity under anesthesia and other settings.
publishDate 2015
dc.date.none.fl_str_mv 2015-07
dc.type.none.fl_str_mv info:eu-repo/semantics/article
info:eu-repo/semantics/publishedVersion
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info:ar-repo/semantics/articulo
format article
status_str publishedVersion
dc.identifier.none.fl_str_mv http://hdl.handle.net/11336/59582
Solovey, Guillermo; Alonso, Leandro Martín; Yanagawa, Toru; Fujii, Naotaka; Magnasco, Marcelo Osvaldo; et al.; Loss of consciousness is associated with stabilization of cortical activity; Society for Neuroscience; Journal of Neuroscience; 35; 30; 7-2015; 10866-10877
0270-6474
CONICET Digital
CONICET
url http://hdl.handle.net/11336/59582
identifier_str_mv Solovey, Guillermo; Alonso, Leandro Martín; Yanagawa, Toru; Fujii, Naotaka; Magnasco, Marcelo Osvaldo; et al.; Loss of consciousness is associated with stabilization of cortical activity; Society for Neuroscience; Journal of Neuroscience; 35; 30; 7-2015; 10866-10877
0270-6474
CONICET Digital
CONICET
dc.language.none.fl_str_mv eng
language eng
dc.relation.none.fl_str_mv info:eu-repo/semantics/altIdentifier/doi/10.1523/JNEUROSCI.4895-14.2015
info:eu-repo/semantics/altIdentifier/url/http://www.jneurosci.org/content/35/30/10866
dc.rights.none.fl_str_mv info:eu-repo/semantics/openAccess
https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
eu_rights_str_mv openAccess
rights_invalid_str_mv https://creativecommons.org/licenses/by-nc-sa/2.5/ar/
dc.format.none.fl_str_mv application/pdf
application/pdf
dc.publisher.none.fl_str_mv Society for Neuroscience
publisher.none.fl_str_mv Society for Neuroscience
dc.source.none.fl_str_mv reponame:CONICET Digital (CONICET)
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reponame_str CONICET Digital (CONICET)
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repository.name.fl_str_mv CONICET Digital (CONICET) - Consejo Nacional de Investigaciones Científicas y Técnicas
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