REM Sleep Microstates in the Human Anterior Thalamus
Rapid eye movement (REM) sleep is an elusive neural state that is associated with a variety of functions from physiological regulatory mechanisms to complex cognitive processing. REM periods consist of the alternation of phasic and tonic REM microstates that differ in spontaneous and evoked neural a...
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creator | Simor, Péter Szalárdy, Orsolya Gombos, Ferenc Ujma, Péter Przemyslaw Jordán, Zsófia Halász, László Erőss, Loránd Fabó, Dániel Bódizs, Róbert |
description | Rapid eye movement (REM) sleep is an elusive neural state that is associated with a variety of functions from physiological regulatory mechanisms to complex cognitive processing. REM periods consist of the alternation of phasic and tonic REM microstates that differ in spontaneous and evoked neural activity. Although previous studies indicate, that cortical and thalamocortical activity differs across phasic and tonic microstates, the characterization of neural activity, particularly in subcortical structures that are critical in the initiation and maintenance of REM sleep is still limited in humans. Here, we examined electric activity patterns of the anterior nuclei of the thalamus as well as their functional connectivity with scalp EEG recordings during REM microstates and wakefulness in a group of epilepsy patients (
= 12, 7 females). Anterothalamic local field potentials (LFPs) showed increased high-α and β frequency power in tonic compared with phasic REM, emerging as an intermediate state between phasic REM and wakefulness. Moreover, we observed increased thalamocortical synchronization in phasic compared with tonic REM sleep, especially in the slow and fast frequency ranges. Wake-like activity in tonic REM sleep may index the regulation of arousal and vigilance facilitating environmental alertness. On the other hand, increased thalamocortical synchronization may reflect the intrinsic activity of frontolimbic networks supporting emotional and memory processes during phasic REM sleep. In sum, our findings highlight that the heterogeneity of phasic and tonic REM sleep is not limited to cortical activity, but is also manifested by anterothalamic LFPs and thalamocortical synchronization.
REM sleep is a heterogeneous sleep state that features the alternation of two microstates, phasic and tonic rapid eye movement (REM). These states differ in sensory processing, awakening thresholds, and cortical activity. Nevertheless, the characterization of these microstates, particularly in subcortical structures is still limited in humans. We had the unique opportunity to examine electric activity patterns of the anterior nuclei of the thalamus (ANTs) as well as their functional connectivity with scalp EEG recordings during REM microstates and wakefulness. Our findings show that the heterogeneity of phasic and tonic REM sleep is not limited to cortical activity, but is also manifested in the level of the thalamus and thalamocortical networks. |
doi_str_mv | 10.1523/JNEUROSCI.1899-20.2021 |
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= 12, 7 females). Anterothalamic local field potentials (LFPs) showed increased high-α and β frequency power in tonic compared with phasic REM, emerging as an intermediate state between phasic REM and wakefulness. Moreover, we observed increased thalamocortical synchronization in phasic compared with tonic REM sleep, especially in the slow and fast frequency ranges. Wake-like activity in tonic REM sleep may index the regulation of arousal and vigilance facilitating environmental alertness. On the other hand, increased thalamocortical synchronization may reflect the intrinsic activity of frontolimbic networks supporting emotional and memory processes during phasic REM sleep. In sum, our findings highlight that the heterogeneity of phasic and tonic REM sleep is not limited to cortical activity, but is also manifested by anterothalamic LFPs and thalamocortical synchronization.
REM sleep is a heterogeneous sleep state that features the alternation of two microstates, phasic and tonic rapid eye movement (REM). These states differ in sensory processing, awakening thresholds, and cortical activity. Nevertheless, the characterization of these microstates, particularly in subcortical structures is still limited in humans. We had the unique opportunity to examine electric activity patterns of the anterior nuclei of the thalamus (ANTs) as well as their functional connectivity with scalp EEG recordings during REM microstates and wakefulness. Our findings show that the heterogeneity of phasic and tonic REM sleep is not limited to cortical activity, but is also manifested in the level of the thalamus and thalamocortical networks.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.1899-20.2021</identifier><identifier>PMID: 33863786</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Activity patterns ; Adolescent ; Adult ; Alertness ; Anterior Thalamic Nuclei - physiology ; Arousal ; Cognitive ability ; EEG ; Electroencephalography ; Epilepsy ; Female ; Frequency ranges ; Heterogeneity ; Human motion ; Humans ; Information processing ; Male ; Middle Aged ; Regulatory mechanisms (biology) ; REM sleep ; Sleep ; Sleep and wakefulness ; Sleep, REM - physiology ; Synchronism ; Synchronization ; Thalamus ; Vigilance ; Wakefulness ; Wakefulness - physiology ; Young Adult</subject><ispartof>The Journal of neuroscience, 2021-06, Vol.41 (26), p.5677-5686</ispartof><rights>Copyright © 2021 the authors.</rights><rights>Copyright Society for Neuroscience Jun 30, 2021</rights><rights>Copyright © 2021 the authors 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c442t-6ae266e6f659ca8923595ec99989b4bddccec20abd9b06a8cad4eb7d1f1c95e93</citedby><orcidid>0000-0002-7255-0541 ; 0000-0001-5141-5351 ; 0000-0003-0695-166X</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/PMC8244978/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8244978/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27903,27904,53770,53772</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33863786$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Simor, Péter</creatorcontrib><creatorcontrib>Szalárdy, Orsolya</creatorcontrib><creatorcontrib>Gombos, Ferenc</creatorcontrib><creatorcontrib>Ujma, Péter Przemyslaw</creatorcontrib><creatorcontrib>Jordán, Zsófia</creatorcontrib><creatorcontrib>Halász, László</creatorcontrib><creatorcontrib>Erőss, Loránd</creatorcontrib><creatorcontrib>Fabó, Dániel</creatorcontrib><creatorcontrib>Bódizs, Róbert</creatorcontrib><title>REM Sleep Microstates in the Human Anterior Thalamus</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>Rapid eye movement (REM) sleep is an elusive neural state that is associated with a variety of functions from physiological regulatory mechanisms to complex cognitive processing. REM periods consist of the alternation of phasic and tonic REM microstates that differ in spontaneous and evoked neural activity. Although previous studies indicate, that cortical and thalamocortical activity differs across phasic and tonic microstates, the characterization of neural activity, particularly in subcortical structures that are critical in the initiation and maintenance of REM sleep is still limited in humans. Here, we examined electric activity patterns of the anterior nuclei of the thalamus as well as their functional connectivity with scalp EEG recordings during REM microstates and wakefulness in a group of epilepsy patients (
= 12, 7 females). Anterothalamic local field potentials (LFPs) showed increased high-α and β frequency power in tonic compared with phasic REM, emerging as an intermediate state between phasic REM and wakefulness. Moreover, we observed increased thalamocortical synchronization in phasic compared with tonic REM sleep, especially in the slow and fast frequency ranges. Wake-like activity in tonic REM sleep may index the regulation of arousal and vigilance facilitating environmental alertness. On the other hand, increased thalamocortical synchronization may reflect the intrinsic activity of frontolimbic networks supporting emotional and memory processes during phasic REM sleep. In sum, our findings highlight that the heterogeneity of phasic and tonic REM sleep is not limited to cortical activity, but is also manifested by anterothalamic LFPs and thalamocortical synchronization.
REM sleep is a heterogeneous sleep state that features the alternation of two microstates, phasic and tonic rapid eye movement (REM). These states differ in sensory processing, awakening thresholds, and cortical activity. Nevertheless, the characterization of these microstates, particularly in subcortical structures is still limited in humans. We had the unique opportunity to examine electric activity patterns of the anterior nuclei of the thalamus (ANTs) as well as their functional connectivity with scalp EEG recordings during REM microstates and wakefulness. Our findings show that the heterogeneity of phasic and tonic REM sleep is not limited to cortical activity, but is also manifested in the level of the thalamus and thalamocortical networks.</description><subject>Activity patterns</subject><subject>Adolescent</subject><subject>Adult</subject><subject>Alertness</subject><subject>Anterior Thalamic Nuclei - physiology</subject><subject>Arousal</subject><subject>Cognitive ability</subject><subject>EEG</subject><subject>Electroencephalography</subject><subject>Epilepsy</subject><subject>Female</subject><subject>Frequency ranges</subject><subject>Heterogeneity</subject><subject>Human motion</subject><subject>Humans</subject><subject>Information processing</subject><subject>Male</subject><subject>Middle Aged</subject><subject>Regulatory mechanisms (biology)</subject><subject>REM sleep</subject><subject>Sleep</subject><subject>Sleep and wakefulness</subject><subject>Sleep, REM - physiology</subject><subject>Synchronism</subject><subject>Synchronization</subject><subject>Thalamus</subject><subject>Vigilance</subject><subject>Wakefulness</subject><subject>Wakefulness - physiology</subject><subject>Young Adult</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpdkV1LwzAUhoMobk7_wih4401nkqZpcyOMMd1kc7CP65CmZ66jHzNpBf-9KZtDvQqH85yXnPMg1Cd4QEIaPL6-jTfLxWo0HZBYCJ_iAcWUXKCu67qSYXKJuphG2OcsYh10Y-0eYxxhEl2jThDEPIhi3kVsOZ57qxzg4M0zbSpbqxqsl5VevQNv0hSq9IZlDSarjLfeqVwVjb1FV1uVW7g7vT20eR6vRxN_tniZjoYzXzNGa58roJwD3_JQaBULGoQiBC2EiEXCkjTVGjTFKklFgrmKtUoZJFFKtkQ7UAQ99HTMPTRJAamGsjYqlweTFcp8yUpl8m-nzHbyvfqUMWVMRLELeDgFmOqjAVvLIrMa8lyVUDVW0pAwTtzhiEPv_6H7qjGlW89RIaEh5jxyFD9S7amsge35MwTLVow8i5GtGEmxbMW4wf7vVc5jPyaCb8wLipM</recordid><startdate>20210630</startdate><enddate>20210630</enddate><creator>Simor, Péter</creator><creator>Szalárdy, Orsolya</creator><creator>Gombos, Ferenc</creator><creator>Ujma, Péter Przemyslaw</creator><creator>Jordán, Zsófia</creator><creator>Halász, László</creator><creator>Erőss, Loránd</creator><creator>Fabó, Dániel</creator><creator>Bódizs, Róbert</creator><general>Society for Neuroscience</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>7QG</scope><scope>7QR</scope><scope>7TK</scope><scope>7U7</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>P64</scope><scope>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-7255-0541</orcidid><orcidid>https://orcid.org/0000-0001-5141-5351</orcidid><orcidid>https://orcid.org/0000-0003-0695-166X</orcidid></search><sort><creationdate>20210630</creationdate><title>REM Sleep Microstates in the Human Anterior Thalamus</title><author>Simor, Péter ; Szalárdy, Orsolya ; Gombos, Ferenc ; Ujma, Péter Przemyslaw ; Jordán, Zsófia ; Halász, László ; Erőss, Loránd ; Fabó, Dániel ; Bódizs, Róbert</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c442t-6ae266e6f659ca8923595ec99989b4bddccec20abd9b06a8cad4eb7d1f1c95e93</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>Activity patterns</topic><topic>Adolescent</topic><topic>Adult</topic><topic>Alertness</topic><topic>Anterior Thalamic Nuclei - physiology</topic><topic>Arousal</topic><topic>Cognitive ability</topic><topic>EEG</topic><topic>Electroencephalography</topic><topic>Epilepsy</topic><topic>Female</topic><topic>Frequency ranges</topic><topic>Heterogeneity</topic><topic>Human motion</topic><topic>Humans</topic><topic>Information processing</topic><topic>Male</topic><topic>Middle Aged</topic><topic>Regulatory mechanisms (biology)</topic><topic>REM sleep</topic><topic>Sleep</topic><topic>Sleep and wakefulness</topic><topic>Sleep, REM - physiology</topic><topic>Synchronism</topic><topic>Synchronization</topic><topic>Thalamus</topic><topic>Vigilance</topic><topic>Wakefulness</topic><topic>Wakefulness - physiology</topic><topic>Young Adult</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Simor, Péter</creatorcontrib><creatorcontrib>Szalárdy, Orsolya</creatorcontrib><creatorcontrib>Gombos, Ferenc</creatorcontrib><creatorcontrib>Ujma, Péter Przemyslaw</creatorcontrib><creatorcontrib>Jordán, Zsófia</creatorcontrib><creatorcontrib>Halász, László</creatorcontrib><creatorcontrib>Erőss, Loránd</creatorcontrib><creatorcontrib>Fabó, Dániel</creatorcontrib><creatorcontrib>Bódizs, Róbert</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Toxicology Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Simor, Péter</au><au>Szalárdy, Orsolya</au><au>Gombos, Ferenc</au><au>Ujma, Péter Przemyslaw</au><au>Jordán, Zsófia</au><au>Halász, László</au><au>Erőss, Loránd</au><au>Fabó, Dániel</au><au>Bódizs, Róbert</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>REM Sleep Microstates in the Human Anterior Thalamus</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2021-06-30</date><risdate>2021</risdate><volume>41</volume><issue>26</issue><spage>5677</spage><epage>5686</epage><pages>5677-5686</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>Rapid eye movement (REM) sleep is an elusive neural state that is associated with a variety of functions from physiological regulatory mechanisms to complex cognitive processing. REM periods consist of the alternation of phasic and tonic REM microstates that differ in spontaneous and evoked neural activity. Although previous studies indicate, that cortical and thalamocortical activity differs across phasic and tonic microstates, the characterization of neural activity, particularly in subcortical structures that are critical in the initiation and maintenance of REM sleep is still limited in humans. Here, we examined electric activity patterns of the anterior nuclei of the thalamus as well as their functional connectivity with scalp EEG recordings during REM microstates and wakefulness in a group of epilepsy patients (
= 12, 7 females). Anterothalamic local field potentials (LFPs) showed increased high-α and β frequency power in tonic compared with phasic REM, emerging as an intermediate state between phasic REM and wakefulness. Moreover, we observed increased thalamocortical synchronization in phasic compared with tonic REM sleep, especially in the slow and fast frequency ranges. Wake-like activity in tonic REM sleep may index the regulation of arousal and vigilance facilitating environmental alertness. On the other hand, increased thalamocortical synchronization may reflect the intrinsic activity of frontolimbic networks supporting emotional and memory processes during phasic REM sleep. In sum, our findings highlight that the heterogeneity of phasic and tonic REM sleep is not limited to cortical activity, but is also manifested by anterothalamic LFPs and thalamocortical synchronization.
REM sleep is a heterogeneous sleep state that features the alternation of two microstates, phasic and tonic rapid eye movement (REM). These states differ in sensory processing, awakening thresholds, and cortical activity. Nevertheless, the characterization of these microstates, particularly in subcortical structures is still limited in humans. We had the unique opportunity to examine electric activity patterns of the anterior nuclei of the thalamus (ANTs) as well as their functional connectivity with scalp EEG recordings during REM microstates and wakefulness. Our findings show that the heterogeneity of phasic and tonic REM sleep is not limited to cortical activity, but is also manifested in the level of the thalamus and thalamocortical networks.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>33863786</pmid><doi>10.1523/JNEUROSCI.1899-20.2021</doi><tpages>10</tpages><orcidid>https://orcid.org/0000-0002-7255-0541</orcidid><orcidid>https://orcid.org/0000-0001-5141-5351</orcidid><orcidid>https://orcid.org/0000-0003-0695-166X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | Activity patterns Adolescent Adult Alertness Anterior Thalamic Nuclei - physiology Arousal Cognitive ability EEG Electroencephalography Epilepsy Female Frequency ranges Heterogeneity Human motion Humans Information processing Male Middle Aged Regulatory mechanisms (biology) REM sleep Sleep Sleep and wakefulness Sleep, REM - physiology Synchronism Synchronization Thalamus Vigilance Wakefulness Wakefulness - physiology Young Adult |
title | REM Sleep Microstates in the Human Anterior Thalamus |
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