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Diversity of functional connectivity patterns is reduced in propofol‐induced unconsciousness
Introduction Recent evidence suggests that the conscious brain is characterized by a diverse repertoire of functional connectivity patterns while the anesthetized brain shows stereotyped activity. However, classical time‐averaged methods of connectivity dismiss dynamic and temporal characteristics o...
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Published in: | Human brain mapping 2017-10, Vol.38 (10), p.4980-4995 |
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description | Introduction
Recent evidence suggests that the conscious brain is characterized by a diverse repertoire of functional connectivity patterns while the anesthetized brain shows stereotyped activity. However, classical time‐averaged methods of connectivity dismiss dynamic and temporal characteristics of functional configurations. Here we demonstrate a new approach which characterizes time‐varying patterns of functional connectivity at the subsecond time scale.
Methods
We introduce phase‐lag entropy (PLE), a measure of the diversity of temporal patterns in the phase relationships between two signals. The proposed measure was applied to multichannel electroencephalogram (EEG), which were recorded from two distinct experimental settings: (1) propofol was administrated at a constant infusion rate for 60 min (n = 96); (2) administration of propofol by a target effect‐site concentration‐controlled infusion with simultaneous assessment of the level of consciousness (n = 10).
Results
From the first dataset, two substantial changes of the phase relationship during anesthesia was found: (1) the dynamics of the phase relationship between frontal channels became progressively less diverse and more stereotyped during unconsciousness, quantified as a reduction in PLE; and (2) the reduction in PLE was consistent across subjects. Furthermore, PLE provided better performance in the classification of states of consciousness than did phase‐lag index, a classical time‐averaged connectivity method. From the second dataset, PLE showed the highest agreement with the level of consciousness, compared to existing anesthetic depth indicators.
Conclusions
This study suggests that a scarcity of functional configurations is closely associated with anesthetically induced unconsciousness, and shows promise as a basis for a new consciousness monitoring system during general anesthesia. Hum Brain Mapp 38:4980–4995, 2017. © 2017 Wiley Periodicals, Inc. |
doi_str_mv | 10.1002/hbm.23708 |
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fullrecord | <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_6866820</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1937413655</sourcerecordid><originalsourceid>FETCH-LOGICAL-c4438-84cdcf43e8f6a4c1913a3126ad33368c851aec35bb0111e2acf0e54f8d7160a3</originalsourceid><addsrcrecordid>eNp1kc1O3DAQx60KVD7aQ1-gitRLOQQ8cex4L5X4KiBR9cK5ltcZF6OsndrJVnvjEXhGngRvA6ggcbI989NPM_4T8gnoPlBaHVzPF_sVa6h8R7aBzpqSwoxtrO-Cl7O6gS2yk9INpQCcwnuyVUnRUCH5Nvl14pYYkxtWRbCFHb0ZXPC6K0zwHvNjuW71ehgw-lS4VERsR4Nt4XzRx9AHG7r72zvnp2oWBJ-MC2PymNIHsml1l_Dj47lLrr6fXh2fl5c_zy6ODy9LU9dMlrI2rbE1Q2mFrg3MgGkGldAtY0xIIzloNIzP53kFwEobS5HXVrYNCKrZLvk2aftxvsDWoB-i7lQf3ULHlQraqZcd767V77BUQgohK5oFXx8FMfwZMQ1q4ZLBrtMe8yoqT8Q5FwJYRr-8Qm_CGPOXrSnW1MAE55namygTQ0oR7fMwQNU6NJVDU_9Cy-zn_6d_Jp9SysDBBPx1Ha7eNqnzox-T8gEKIqR8</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1937413655</pqid></control><display><type>article</type><title>Diversity of functional connectivity patterns is reduced in propofol‐induced unconsciousness</title><source>PubMed Central Free</source><creator>Lee, Heonsoo ; Noh, Gyu‐Jeong ; Joo, Pangyu ; Choi, Byung‐Moon ; Silverstein, Brian Henry ; Kim, Minkyung ; Wang, Jisung ; Jung, Woo‐Sung ; Kim, Seunghwan</creator><creatorcontrib>Lee, Heonsoo ; Noh, Gyu‐Jeong ; Joo, Pangyu ; Choi, Byung‐Moon ; Silverstein, Brian Henry ; Kim, Minkyung ; Wang, Jisung ; Jung, Woo‐Sung ; Kim, Seunghwan</creatorcontrib><description>Introduction
Recent evidence suggests that the conscious brain is characterized by a diverse repertoire of functional connectivity patterns while the anesthetized brain shows stereotyped activity. However, classical time‐averaged methods of connectivity dismiss dynamic and temporal characteristics of functional configurations. Here we demonstrate a new approach which characterizes time‐varying patterns of functional connectivity at the subsecond time scale.
Methods
We introduce phase‐lag entropy (PLE), a measure of the diversity of temporal patterns in the phase relationships between two signals. The proposed measure was applied to multichannel electroencephalogram (EEG), which were recorded from two distinct experimental settings: (1) propofol was administrated at a constant infusion rate for 60 min (n = 96); (2) administration of propofol by a target effect‐site concentration‐controlled infusion with simultaneous assessment of the level of consciousness (n = 10).
Results
From the first dataset, two substantial changes of the phase relationship during anesthesia was found: (1) the dynamics of the phase relationship between frontal channels became progressively less diverse and more stereotyped during unconsciousness, quantified as a reduction in PLE; and (2) the reduction in PLE was consistent across subjects. Furthermore, PLE provided better performance in the classification of states of consciousness than did phase‐lag index, a classical time‐averaged connectivity method. From the second dataset, PLE showed the highest agreement with the level of consciousness, compared to existing anesthetic depth indicators.
Conclusions
This study suggests that a scarcity of functional configurations is closely associated with anesthetically induced unconsciousness, and shows promise as a basis for a new consciousness monitoring system during general anesthesia. Hum Brain Mapp 38:4980–4995, 2017. © 2017 Wiley Periodicals, Inc.</description><identifier>ISSN: 1065-9471</identifier><identifier>EISSN: 1097-0193</identifier><identifier>DOI: 10.1002/hbm.23708</identifier><identifier>PMID: 28670685</identifier><language>eng</language><publisher>United States: John Wiley & Sons, Inc</publisher><subject>Anesthesia ; Anesthesia, General ; Anesthetics, Intravenous - pharmacology ; Brain ; Brain - drug effects ; Brain - physiology ; Classification ; complexity ; Consciousness ; Consciousness - drug effects ; Consciousness - physiology ; Depth indicators ; Dose-Response Relationship, Drug ; EEG ; electroencephalogram ; Electroencephalography ; Entropy ; functional connectivity ; Functional Neuroimaging ; Humans ; Hypnotics and Sedatives - pharmacology ; Neural networks ; Neural Pathways - drug effects ; Neural Pathways - physiology ; Phase relationships ; Phase transitions ; phase‐lag index ; Propofol ; Propofol - pharmacology ; Reduction ; Signal Processing, Computer-Assisted ; Unconsciousness ; Unconsciousness - chemically induced ; Unconsciousness - physiopathology</subject><ispartof>Human brain mapping, 2017-10, Vol.38 (10), p.4980-4995</ispartof><rights>2017 Wiley Periodicals, Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4438-84cdcf43e8f6a4c1913a3126ad33368c851aec35bb0111e2acf0e54f8d7160a3</citedby><cites>FETCH-LOGICAL-c4438-84cdcf43e8f6a4c1913a3126ad33368c851aec35bb0111e2acf0e54f8d7160a3</cites><orcidid>0000-0002-8294-2063</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6866820/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6866820/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28670685$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Lee, Heonsoo</creatorcontrib><creatorcontrib>Noh, Gyu‐Jeong</creatorcontrib><creatorcontrib>Joo, Pangyu</creatorcontrib><creatorcontrib>Choi, Byung‐Moon</creatorcontrib><creatorcontrib>Silverstein, Brian Henry</creatorcontrib><creatorcontrib>Kim, Minkyung</creatorcontrib><creatorcontrib>Wang, Jisung</creatorcontrib><creatorcontrib>Jung, Woo‐Sung</creatorcontrib><creatorcontrib>Kim, Seunghwan</creatorcontrib><title>Diversity of functional connectivity patterns is reduced in propofol‐induced unconsciousness</title><title>Human brain mapping</title><addtitle>Hum Brain Mapp</addtitle><description>Introduction
Recent evidence suggests that the conscious brain is characterized by a diverse repertoire of functional connectivity patterns while the anesthetized brain shows stereotyped activity. However, classical time‐averaged methods of connectivity dismiss dynamic and temporal characteristics of functional configurations. Here we demonstrate a new approach which characterizes time‐varying patterns of functional connectivity at the subsecond time scale.
Methods
We introduce phase‐lag entropy (PLE), a measure of the diversity of temporal patterns in the phase relationships between two signals. The proposed measure was applied to multichannel electroencephalogram (EEG), which were recorded from two distinct experimental settings: (1) propofol was administrated at a constant infusion rate for 60 min (n = 96); (2) administration of propofol by a target effect‐site concentration‐controlled infusion with simultaneous assessment of the level of consciousness (n = 10).
Results
From the first dataset, two substantial changes of the phase relationship during anesthesia was found: (1) the dynamics of the phase relationship between frontal channels became progressively less diverse and more stereotyped during unconsciousness, quantified as a reduction in PLE; and (2) the reduction in PLE was consistent across subjects. Furthermore, PLE provided better performance in the classification of states of consciousness than did phase‐lag index, a classical time‐averaged connectivity method. From the second dataset, PLE showed the highest agreement with the level of consciousness, compared to existing anesthetic depth indicators.
Conclusions
This study suggests that a scarcity of functional configurations is closely associated with anesthetically induced unconsciousness, and shows promise as a basis for a new consciousness monitoring system during general anesthesia. Hum Brain Mapp 38:4980–4995, 2017. © 2017 Wiley Periodicals, Inc.</description><subject>Anesthesia</subject><subject>Anesthesia, General</subject><subject>Anesthetics, Intravenous - pharmacology</subject><subject>Brain</subject><subject>Brain - drug effects</subject><subject>Brain - physiology</subject><subject>Classification</subject><subject>complexity</subject><subject>Consciousness</subject><subject>Consciousness - drug effects</subject><subject>Consciousness - physiology</subject><subject>Depth indicators</subject><subject>Dose-Response Relationship, Drug</subject><subject>EEG</subject><subject>electroencephalogram</subject><subject>Electroencephalography</subject><subject>Entropy</subject><subject>functional connectivity</subject><subject>Functional Neuroimaging</subject><subject>Humans</subject><subject>Hypnotics and Sedatives - pharmacology</subject><subject>Neural networks</subject><subject>Neural Pathways - drug effects</subject><subject>Neural Pathways - physiology</subject><subject>Phase relationships</subject><subject>Phase transitions</subject><subject>phase‐lag index</subject><subject>Propofol</subject><subject>Propofol - pharmacology</subject><subject>Reduction</subject><subject>Signal Processing, Computer-Assisted</subject><subject>Unconsciousness</subject><subject>Unconsciousness - chemically induced</subject><subject>Unconsciousness - physiopathology</subject><issn>1065-9471</issn><issn>1097-0193</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><recordid>eNp1kc1O3DAQx60KVD7aQ1-gitRLOQQ8cex4L5X4KiBR9cK5ltcZF6OsndrJVnvjEXhGngRvA6ggcbI989NPM_4T8gnoPlBaHVzPF_sVa6h8R7aBzpqSwoxtrO-Cl7O6gS2yk9INpQCcwnuyVUnRUCH5Nvl14pYYkxtWRbCFHb0ZXPC6K0zwHvNjuW71ehgw-lS4VERsR4Nt4XzRx9AHG7r72zvnp2oWBJ-MC2PymNIHsml1l_Dj47lLrr6fXh2fl5c_zy6ODy9LU9dMlrI2rbE1Q2mFrg3MgGkGldAtY0xIIzloNIzP53kFwEobS5HXVrYNCKrZLvk2aftxvsDWoB-i7lQf3ULHlQraqZcd767V77BUQgohK5oFXx8FMfwZMQ1q4ZLBrtMe8yoqT8Q5FwJYRr-8Qm_CGPOXrSnW1MAE55namygTQ0oR7fMwQNU6NJVDU_9Cy-zn_6d_Jp9SysDBBPx1Ha7eNqnzox-T8gEKIqR8</recordid><startdate>201710</startdate><enddate>201710</enddate><creator>Lee, Heonsoo</creator><creator>Noh, Gyu‐Jeong</creator><creator>Joo, Pangyu</creator><creator>Choi, Byung‐Moon</creator><creator>Silverstein, Brian Henry</creator><creator>Kim, Minkyung</creator><creator>Wang, Jisung</creator><creator>Jung, Woo‐Sung</creator><creator>Kim, Seunghwan</creator><general>John Wiley & Sons, Inc</general><general>John Wiley and Sons Inc</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>K9.</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-8294-2063</orcidid></search><sort><creationdate>201710</creationdate><title>Diversity of functional connectivity patterns is reduced in propofol‐induced unconsciousness</title><author>Lee, Heonsoo ; Noh, Gyu‐Jeong ; Joo, Pangyu ; Choi, Byung‐Moon ; Silverstein, Brian Henry ; Kim, Minkyung ; Wang, Jisung ; Jung, Woo‐Sung ; Kim, Seunghwan</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4438-84cdcf43e8f6a4c1913a3126ad33368c851aec35bb0111e2acf0e54f8d7160a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Anesthesia</topic><topic>Anesthesia, General</topic><topic>Anesthetics, Intravenous - pharmacology</topic><topic>Brain</topic><topic>Brain - drug effects</topic><topic>Brain - physiology</topic><topic>Classification</topic><topic>complexity</topic><topic>Consciousness</topic><topic>Consciousness - drug effects</topic><topic>Consciousness - physiology</topic><topic>Depth indicators</topic><topic>Dose-Response Relationship, Drug</topic><topic>EEG</topic><topic>electroencephalogram</topic><topic>Electroencephalography</topic><topic>Entropy</topic><topic>functional connectivity</topic><topic>Functional Neuroimaging</topic><topic>Humans</topic><topic>Hypnotics and Sedatives - pharmacology</topic><topic>Neural networks</topic><topic>Neural Pathways - drug effects</topic><topic>Neural Pathways - physiology</topic><topic>Phase relationships</topic><topic>Phase transitions</topic><topic>phase‐lag index</topic><topic>Propofol</topic><topic>Propofol - pharmacology</topic><topic>Reduction</topic><topic>Signal Processing, Computer-Assisted</topic><topic>Unconsciousness</topic><topic>Unconsciousness - chemically induced</topic><topic>Unconsciousness - physiopathology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Lee, Heonsoo</creatorcontrib><creatorcontrib>Noh, Gyu‐Jeong</creatorcontrib><creatorcontrib>Joo, Pangyu</creatorcontrib><creatorcontrib>Choi, Byung‐Moon</creatorcontrib><creatorcontrib>Silverstein, Brian Henry</creatorcontrib><creatorcontrib>Kim, Minkyung</creatorcontrib><creatorcontrib>Wang, Jisung</creatorcontrib><creatorcontrib>Jung, Woo‐Sung</creatorcontrib><creatorcontrib>Kim, Seunghwan</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Human brain mapping</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Lee, Heonsoo</au><au>Noh, Gyu‐Jeong</au><au>Joo, Pangyu</au><au>Choi, Byung‐Moon</au><au>Silverstein, Brian Henry</au><au>Kim, Minkyung</au><au>Wang, Jisung</au><au>Jung, Woo‐Sung</au><au>Kim, Seunghwan</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Diversity of functional connectivity patterns is reduced in propofol‐induced unconsciousness</atitle><jtitle>Human brain mapping</jtitle><addtitle>Hum Brain Mapp</addtitle><date>2017-10</date><risdate>2017</risdate><volume>38</volume><issue>10</issue><spage>4980</spage><epage>4995</epage><pages>4980-4995</pages><issn>1065-9471</issn><eissn>1097-0193</eissn><abstract>Introduction
Recent evidence suggests that the conscious brain is characterized by a diverse repertoire of functional connectivity patterns while the anesthetized brain shows stereotyped activity. However, classical time‐averaged methods of connectivity dismiss dynamic and temporal characteristics of functional configurations. Here we demonstrate a new approach which characterizes time‐varying patterns of functional connectivity at the subsecond time scale.
Methods
We introduce phase‐lag entropy (PLE), a measure of the diversity of temporal patterns in the phase relationships between two signals. The proposed measure was applied to multichannel electroencephalogram (EEG), which were recorded from two distinct experimental settings: (1) propofol was administrated at a constant infusion rate for 60 min (n = 96); (2) administration of propofol by a target effect‐site concentration‐controlled infusion with simultaneous assessment of the level of consciousness (n = 10).
Results
From the first dataset, two substantial changes of the phase relationship during anesthesia was found: (1) the dynamics of the phase relationship between frontal channels became progressively less diverse and more stereotyped during unconsciousness, quantified as a reduction in PLE; and (2) the reduction in PLE was consistent across subjects. Furthermore, PLE provided better performance in the classification of states of consciousness than did phase‐lag index, a classical time‐averaged connectivity method. From the second dataset, PLE showed the highest agreement with the level of consciousness, compared to existing anesthetic depth indicators.
Conclusions
This study suggests that a scarcity of functional configurations is closely associated with anesthetically induced unconsciousness, and shows promise as a basis for a new consciousness monitoring system during general anesthesia. Hum Brain Mapp 38:4980–4995, 2017. © 2017 Wiley Periodicals, Inc.</abstract><cop>United States</cop><pub>John Wiley & Sons, Inc</pub><pmid>28670685</pmid><doi>10.1002/hbm.23708</doi><tpages>16</tpages><orcidid>https://orcid.org/0000-0002-8294-2063</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Anesthesia Anesthesia, General Anesthetics, Intravenous - pharmacology Brain Brain - drug effects Brain - physiology Classification complexity Consciousness Consciousness - drug effects Consciousness - physiology Depth indicators Dose-Response Relationship, Drug EEG electroencephalogram Electroencephalography Entropy functional connectivity Functional Neuroimaging Humans Hypnotics and Sedatives - pharmacology Neural networks Neural Pathways - drug effects Neural Pathways - physiology Phase relationships Phase transitions phase‐lag index Propofol Propofol - pharmacology Reduction Signal Processing, Computer-Assisted Unconsciousness Unconsciousness - chemically induced Unconsciousness - physiopathology |
title | Diversity of functional connectivity patterns is reduced in propofol‐induced unconsciousness |
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