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Thalamic deep brain stimulation paradigm to reduce consciousness: Cortico-striatal dynamics implicated in mechanisms of consciousness

Anesthetic manipulations provide much-needed causal evidence for neural correlates of consciousness, but non-specific drug effects complicate their interpretation. Evidence suggests that thalamic deep brain stimulation (DBS) can either increase or decrease consciousness, depending on the stimulation...

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Autores principales: Redinbaugh, Michelle J., Afrasiabi, Mohsen, Phillips, Jessica M., Kambi, Niranjan A., Mohanta, Sounak, Raz, Aeyal, Saalmann, Yuri B.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2022
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9321468/
https://www.ncbi.nlm.nih.gov/pubmed/35816488
http://dx.doi.org/10.1371/journal.pcbi.1010294
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author Redinbaugh, Michelle J.
Afrasiabi, Mohsen
Phillips, Jessica M.
Kambi, Niranjan A.
Mohanta, Sounak
Raz, Aeyal
Saalmann, Yuri B.
author_facet Redinbaugh, Michelle J.
Afrasiabi, Mohsen
Phillips, Jessica M.
Kambi, Niranjan A.
Mohanta, Sounak
Raz, Aeyal
Saalmann, Yuri B.
author_sort Redinbaugh, Michelle J.
collection PubMed
description Anesthetic manipulations provide much-needed causal evidence for neural correlates of consciousness, but non-specific drug effects complicate their interpretation. Evidence suggests that thalamic deep brain stimulation (DBS) can either increase or decrease consciousness, depending on the stimulation target and parameters. The putative role of the central lateral thalamus (CL) in consciousness makes it an ideal DBS target to manipulate circuit-level mechanisms in cortico-striato-thalamic (CST) systems, thereby influencing consciousness and related processes. We used multi-microelectrode DBS targeted to CL in macaques while recording from frontal, parietal, and striatal regions. DBS induced episodes of abnormally long, vacant staring with low-frequency oscillations here termed vacant, perturbed consciousness (VPC). DBS modulated VPC likelihood in a frequency-specific manner. VPC events corresponded to decreases in measures of neural complexity (entropy) and integration (Φ*), proposed indices of consciousness, and substantial changes to communication in CST circuits. During VPC, power spectral density and coherence at low frequencies increased across CST circuits, especially in thalamo-parietal and cortico-striatal pathways. Decreased consciousness and neural integration corresponded to shifts in cortico-striatal network configurations that dissociated parietal and subcortical structures. Overall, the features of VPC and implicated networks were similar to those of absence epilepsy. As this same multi-microelectrode DBS method–but at different stimulation frequencies–can also increase consciousness in anesthetized macaques, it can be used to flexibly address questions of consciousness with limited confounds, as well as inform clinical investigations of other consciousness disorders.
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spelling pubmed-93214682022-07-27 Thalamic deep brain stimulation paradigm to reduce consciousness: Cortico-striatal dynamics implicated in mechanisms of consciousness Redinbaugh, Michelle J. Afrasiabi, Mohsen Phillips, Jessica M. Kambi, Niranjan A. Mohanta, Sounak Raz, Aeyal Saalmann, Yuri B. PLoS Comput Biol Research Article Anesthetic manipulations provide much-needed causal evidence for neural correlates of consciousness, but non-specific drug effects complicate their interpretation. Evidence suggests that thalamic deep brain stimulation (DBS) can either increase or decrease consciousness, depending on the stimulation target and parameters. The putative role of the central lateral thalamus (CL) in consciousness makes it an ideal DBS target to manipulate circuit-level mechanisms in cortico-striato-thalamic (CST) systems, thereby influencing consciousness and related processes. We used multi-microelectrode DBS targeted to CL in macaques while recording from frontal, parietal, and striatal regions. DBS induced episodes of abnormally long, vacant staring with low-frequency oscillations here termed vacant, perturbed consciousness (VPC). DBS modulated VPC likelihood in a frequency-specific manner. VPC events corresponded to decreases in measures of neural complexity (entropy) and integration (Φ*), proposed indices of consciousness, and substantial changes to communication in CST circuits. During VPC, power spectral density and coherence at low frequencies increased across CST circuits, especially in thalamo-parietal and cortico-striatal pathways. Decreased consciousness and neural integration corresponded to shifts in cortico-striatal network configurations that dissociated parietal and subcortical structures. Overall, the features of VPC and implicated networks were similar to those of absence epilepsy. As this same multi-microelectrode DBS method–but at different stimulation frequencies–can also increase consciousness in anesthetized macaques, it can be used to flexibly address questions of consciousness with limited confounds, as well as inform clinical investigations of other consciousness disorders. Public Library of Science 2022-07-11 /pmc/articles/PMC9321468/ /pubmed/35816488 http://dx.doi.org/10.1371/journal.pcbi.1010294 Text en © 2022 Redinbaugh et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://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
Redinbaugh, Michelle J.
Afrasiabi, Mohsen
Phillips, Jessica M.
Kambi, Niranjan A.
Mohanta, Sounak
Raz, Aeyal
Saalmann, Yuri B.
Thalamic deep brain stimulation paradigm to reduce consciousness: Cortico-striatal dynamics implicated in mechanisms of consciousness
title Thalamic deep brain stimulation paradigm to reduce consciousness: Cortico-striatal dynamics implicated in mechanisms of consciousness
title_full Thalamic deep brain stimulation paradigm to reduce consciousness: Cortico-striatal dynamics implicated in mechanisms of consciousness
title_fullStr Thalamic deep brain stimulation paradigm to reduce consciousness: Cortico-striatal dynamics implicated in mechanisms of consciousness
title_full_unstemmed Thalamic deep brain stimulation paradigm to reduce consciousness: Cortico-striatal dynamics implicated in mechanisms of consciousness
title_short Thalamic deep brain stimulation paradigm to reduce consciousness: Cortico-striatal dynamics implicated in mechanisms of consciousness
title_sort thalamic deep brain stimulation paradigm to reduce consciousness: cortico-striatal dynamics implicated in mechanisms of consciousness
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC9321468/
https://www.ncbi.nlm.nih.gov/pubmed/35816488
http://dx.doi.org/10.1371/journal.pcbi.1010294
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