Suppression of preoptic sleep-regulatory neuronal activity during corticotropin-releasing factor-induced sleep disturbance

Corticotropin releasing factor (CRF) is implicated in sleep and arousal regulation. Exogenous CRF causes sleep suppression that is associated with activation of at least two important arousal systems: pontine noradrenergic and hypothalamic orexin/hypocretin neurons. It is not known whether CRF also...

Ausführliche Beschreibung

Gespeichert in:
Bibliographische Detailangaben
Veröffentlicht in:American journal of physiology. Regulatory, integrative and comparative physiology integrative and comparative physiology, 2015-11, Vol.309 (9), p.R1092-R1100
Hauptverfasser: Gvilia, Irma, Suntsova, Natalia, Kumar, Sunil, McGinty, Dennis, Szymusiak, Ronald
Format: Artikel
Sprache:eng
Schlagworte:
Online-Zugang:Volltext
Tags: Tag hinzufügen
Keine Tags, Fügen Sie den ersten Tag hinzu!
container_end_page R1100
container_issue 9
container_start_page R1092
container_title American journal of physiology. Regulatory, integrative and comparative physiology
container_volume 309
creator Gvilia, Irma
Suntsova, Natalia
Kumar, Sunil
McGinty, Dennis
Szymusiak, Ronald
description Corticotropin releasing factor (CRF) is implicated in sleep and arousal regulation. Exogenous CRF causes sleep suppression that is associated with activation of at least two important arousal systems: pontine noradrenergic and hypothalamic orexin/hypocretin neurons. It is not known whether CRF also impacts sleep-promoting neuronal systems. We hypothesized that CRF-mediated changes in wake and sleep involve decreased activity of hypothalamic sleep-regulatory neurons localized in the preoptic area. To test this hypothesis, we examined the effects of intracerebroventricular administration of CRF on sleep-wake measures and c-Fos expression in GABAergic neurons in the median preoptic nucleus (MnPN) and ventrolateral preoptic area (VLPO) in different experimental conditions. Administration of CRF (0.1 nmol) during baseline rest phase led to delayed sleep onset and decreases in total amount and mean duration of non-rapid eye movement (NREM) sleep. Administration of CRF during acute sleep deprivation (SD) resulted in suppression of recovery sleep and decreased c-Fos expression in MnPN/VLPO GABAergic neurons. Compared with vehicle controls, intracerebroventricular CRF potentiated disturbances of both NREM and REM sleep in rats exposed to a species-specific psychological stressor, the dirty cage of a male conspecific. The number of MnPN/VLPO GABAergic neurons expressing c-Fos was reduced in the CRF-treated group of dirty cage-exposed rats. These findings confirm the involvement of CRF in wake-sleep cycle regulation and suggest that increased CRF signaling in the brain 1) negatively affects homeostatic responses to sleep loss, 2) exacerbates stress-induced disturbances of sleep, and 3) suppresses the activity of sleep-regulatory neurons of the MnPN and VLPO.
doi_str_mv 10.1152/ajpregu.00176.2015
format Article
fullrecord <record><control><sourceid>proquest_cross</sourceid><recordid>TN_cdi_proquest_miscellaneous_1837342395</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><sourcerecordid>1837342395</sourcerecordid><originalsourceid>FETCH-LOGICAL-c474t-fdb89b463de7be139d3ae7d87cb44b003f382aaba216903edf539490dfc2adc3</originalsourceid><addsrcrecordid>eNqFkctKxDAUhoMoznh5ARdScOOmY5KT3pYi3mDAhe5LmpwOGTpNTRphfHpTZ3ThxlVC8v0fnPMTcsHogrGM38j14HAVFpSyIl9wyrIDMo8fPGWioodkTiGHNGesmpET79eUUgECjsmM5wBQlGJOPl_DEC3eG9sntk3i3Q6jUYnvEId08ndytG6b9Bic7WWXSDWaDzNuEx2c6VeJsi4G7OjsYPqY6FD66b2NoHWp6XVQqHfCRBs_BtfIXuEZOWpl5_F8f56St4f7t7undPny-Hx3u0yVKMSYtropq0bkoLFokEGlQWKhy0I1QjSUQgsll7KRnOUVBdRtBlWcX7eKS63glFzvtIOz7wH9WG-MV9h1skcbfM1KKEBwqLL_0YJXkHGa5RG9-oOubXBxPRMFrIybZpOQ7yjlrPcO23pwZiPdtma0njqs9x3W3x3WU4cxdLlXh2aD-jfyUxp8AbcLnPY</addsrcrecordid><sourcetype>Aggregation Database</sourcetype><iscdi>true</iscdi><recordtype>article</recordtype><pqid>1731804315</pqid></control><display><type>article</type><title>Suppression of preoptic sleep-regulatory neuronal activity during corticotropin-releasing factor-induced sleep disturbance</title><source>MEDLINE</source><source>American Physiological Society</source><source>Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals</source><source>Alma/SFX Local Collection</source><creator>Gvilia, Irma ; Suntsova, Natalia ; Kumar, Sunil ; McGinty, Dennis ; Szymusiak, Ronald</creator><creatorcontrib>Gvilia, Irma ; Suntsova, Natalia ; Kumar, Sunil ; McGinty, Dennis ; Szymusiak, Ronald</creatorcontrib><description>Corticotropin releasing factor (CRF) is implicated in sleep and arousal regulation. Exogenous CRF causes sleep suppression that is associated with activation of at least two important arousal systems: pontine noradrenergic and hypothalamic orexin/hypocretin neurons. It is not known whether CRF also impacts sleep-promoting neuronal systems. We hypothesized that CRF-mediated changes in wake and sleep involve decreased activity of hypothalamic sleep-regulatory neurons localized in the preoptic area. To test this hypothesis, we examined the effects of intracerebroventricular administration of CRF on sleep-wake measures and c-Fos expression in GABAergic neurons in the median preoptic nucleus (MnPN) and ventrolateral preoptic area (VLPO) in different experimental conditions. Administration of CRF (0.1 nmol) during baseline rest phase led to delayed sleep onset and decreases in total amount and mean duration of non-rapid eye movement (NREM) sleep. Administration of CRF during acute sleep deprivation (SD) resulted in suppression of recovery sleep and decreased c-Fos expression in MnPN/VLPO GABAergic neurons. Compared with vehicle controls, intracerebroventricular CRF potentiated disturbances of both NREM and REM sleep in rats exposed to a species-specific psychological stressor, the dirty cage of a male conspecific. The number of MnPN/VLPO GABAergic neurons expressing c-Fos was reduced in the CRF-treated group of dirty cage-exposed rats. These findings confirm the involvement of CRF in wake-sleep cycle regulation and suggest that increased CRF signaling in the brain 1) negatively affects homeostatic responses to sleep loss, 2) exacerbates stress-induced disturbances of sleep, and 3) suppresses the activity of sleep-regulatory neurons of the MnPN and VLPO.</description><identifier>ISSN: 0363-6119</identifier><identifier>EISSN: 1522-1490</identifier><identifier>DOI: 10.1152/ajpregu.00176.2015</identifier><identifier>PMID: 26333784</identifier><identifier>CODEN: AJPRDO</identifier><language>eng</language><publisher>United States: American Physiological Society</publisher><subject>Animals ; Brain ; Corticotropin-Releasing Hormone - administration &amp; dosage ; Corticotropin-Releasing Hormone - pharmacokinetics ; Eye movements ; GABAergic Neurons - drug effects ; GABAergic Neurons - metabolism ; Male ; Neural Inhibition - drug effects ; Neurons ; Preoptic Area - drug effects ; Preoptic Area - metabolism ; Rats ; Rats, Sprague-Dawley ; Sleep ; Sleep Stages - drug effects ; Sleep Wake Disorders - chemically induced ; Sleep Wake Disorders - metabolism ; Wakefulness - drug effects</subject><ispartof>American journal of physiology. Regulatory, integrative and comparative physiology, 2015-11, Vol.309 (9), p.R1092-R1100</ispartof><rights>Copyright American Physiological Society Nov 1, 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c474t-fdb89b463de7be139d3ae7d87cb44b003f382aaba216903edf539490dfc2adc3</citedby><cites>FETCH-LOGICAL-c474t-fdb89b463de7be139d3ae7d87cb44b003f382aaba216903edf539490dfc2adc3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,776,780,3026,27901,27902</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/26333784$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Gvilia, Irma</creatorcontrib><creatorcontrib>Suntsova, Natalia</creatorcontrib><creatorcontrib>Kumar, Sunil</creatorcontrib><creatorcontrib>McGinty, Dennis</creatorcontrib><creatorcontrib>Szymusiak, Ronald</creatorcontrib><title>Suppression of preoptic sleep-regulatory neuronal activity during corticotropin-releasing factor-induced sleep disturbance</title><title>American journal of physiology. Regulatory, integrative and comparative physiology</title><addtitle>Am J Physiol Regul Integr Comp Physiol</addtitle><description>Corticotropin releasing factor (CRF) is implicated in sleep and arousal regulation. Exogenous CRF causes sleep suppression that is associated with activation of at least two important arousal systems: pontine noradrenergic and hypothalamic orexin/hypocretin neurons. It is not known whether CRF also impacts sleep-promoting neuronal systems. We hypothesized that CRF-mediated changes in wake and sleep involve decreased activity of hypothalamic sleep-regulatory neurons localized in the preoptic area. To test this hypothesis, we examined the effects of intracerebroventricular administration of CRF on sleep-wake measures and c-Fos expression in GABAergic neurons in the median preoptic nucleus (MnPN) and ventrolateral preoptic area (VLPO) in different experimental conditions. Administration of CRF (0.1 nmol) during baseline rest phase led to delayed sleep onset and decreases in total amount and mean duration of non-rapid eye movement (NREM) sleep. Administration of CRF during acute sleep deprivation (SD) resulted in suppression of recovery sleep and decreased c-Fos expression in MnPN/VLPO GABAergic neurons. Compared with vehicle controls, intracerebroventricular CRF potentiated disturbances of both NREM and REM sleep in rats exposed to a species-specific psychological stressor, the dirty cage of a male conspecific. The number of MnPN/VLPO GABAergic neurons expressing c-Fos was reduced in the CRF-treated group of dirty cage-exposed rats. These findings confirm the involvement of CRF in wake-sleep cycle regulation and suggest that increased CRF signaling in the brain 1) negatively affects homeostatic responses to sleep loss, 2) exacerbates stress-induced disturbances of sleep, and 3) suppresses the activity of sleep-regulatory neurons of the MnPN and VLPO.</description><subject>Animals</subject><subject>Brain</subject><subject>Corticotropin-Releasing Hormone - administration &amp; dosage</subject><subject>Corticotropin-Releasing Hormone - pharmacokinetics</subject><subject>Eye movements</subject><subject>GABAergic Neurons - drug effects</subject><subject>GABAergic Neurons - metabolism</subject><subject>Male</subject><subject>Neural Inhibition - drug effects</subject><subject>Neurons</subject><subject>Preoptic Area - drug effects</subject><subject>Preoptic Area - metabolism</subject><subject>Rats</subject><subject>Rats, Sprague-Dawley</subject><subject>Sleep</subject><subject>Sleep Stages - drug effects</subject><subject>Sleep Wake Disorders - chemically induced</subject><subject>Sleep Wake Disorders - metabolism</subject><subject>Wakefulness - drug effects</subject><issn>0363-6119</issn><issn>1522-1490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFkctKxDAUhoMoznh5ARdScOOmY5KT3pYi3mDAhe5LmpwOGTpNTRphfHpTZ3ThxlVC8v0fnPMTcsHogrGM38j14HAVFpSyIl9wyrIDMo8fPGWioodkTiGHNGesmpET79eUUgECjsmM5wBQlGJOPl_DEC3eG9sntk3i3Q6jUYnvEId08ndytG6b9Bic7WWXSDWaDzNuEx2c6VeJsi4G7OjsYPqY6FD66b2NoHWp6XVQqHfCRBs_BtfIXuEZOWpl5_F8f56St4f7t7undPny-Hx3u0yVKMSYtropq0bkoLFokEGlQWKhy0I1QjSUQgsll7KRnOUVBdRtBlWcX7eKS63glFzvtIOz7wH9WG-MV9h1skcbfM1KKEBwqLL_0YJXkHGa5RG9-oOubXBxPRMFrIybZpOQ7yjlrPcO23pwZiPdtma0njqs9x3W3x3WU4cxdLlXh2aD-jfyUxp8AbcLnPY</recordid><startdate>20151101</startdate><enddate>20151101</enddate><creator>Gvilia, Irma</creator><creator>Suntsova, Natalia</creator><creator>Kumar, Sunil</creator><creator>McGinty, Dennis</creator><creator>Szymusiak, Ronald</creator><general>American Physiological Society</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>7QP</scope><scope>7QR</scope><scope>7TS</scope><scope>7U7</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>P64</scope><scope>7X8</scope><scope>7TK</scope></search><sort><creationdate>20151101</creationdate><title>Suppression of preoptic sleep-regulatory neuronal activity during corticotropin-releasing factor-induced sleep disturbance</title><author>Gvilia, Irma ; Suntsova, Natalia ; Kumar, Sunil ; McGinty, Dennis ; Szymusiak, Ronald</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c474t-fdb89b463de7be139d3ae7d87cb44b003f382aaba216903edf539490dfc2adc3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Brain</topic><topic>Corticotropin-Releasing Hormone - administration &amp; dosage</topic><topic>Corticotropin-Releasing Hormone - pharmacokinetics</topic><topic>Eye movements</topic><topic>GABAergic Neurons - drug effects</topic><topic>GABAergic Neurons - metabolism</topic><topic>Male</topic><topic>Neural Inhibition - drug effects</topic><topic>Neurons</topic><topic>Preoptic Area - drug effects</topic><topic>Preoptic Area - metabolism</topic><topic>Rats</topic><topic>Rats, Sprague-Dawley</topic><topic>Sleep</topic><topic>Sleep Stages - drug effects</topic><topic>Sleep Wake Disorders - chemically induced</topic><topic>Sleep Wake Disorders - metabolism</topic><topic>Wakefulness - drug effects</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Gvilia, Irma</creatorcontrib><creatorcontrib>Suntsova, Natalia</creatorcontrib><creatorcontrib>Kumar, Sunil</creatorcontrib><creatorcontrib>McGinty, Dennis</creatorcontrib><creatorcontrib>Szymusiak, Ronald</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium &amp; Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Physical Education Index</collection><collection>Toxicology Abstracts</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>Engineering Research Database</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>MEDLINE - Academic</collection><collection>Neurosciences Abstracts</collection><jtitle>American journal of physiology. Regulatory, integrative and comparative physiology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Gvilia, Irma</au><au>Suntsova, Natalia</au><au>Kumar, Sunil</au><au>McGinty, Dennis</au><au>Szymusiak, Ronald</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Suppression of preoptic sleep-regulatory neuronal activity during corticotropin-releasing factor-induced sleep disturbance</atitle><jtitle>American journal of physiology. Regulatory, integrative and comparative physiology</jtitle><addtitle>Am J Physiol Regul Integr Comp Physiol</addtitle><date>2015-11-01</date><risdate>2015</risdate><volume>309</volume><issue>9</issue><spage>R1092</spage><epage>R1100</epage><pages>R1092-R1100</pages><issn>0363-6119</issn><eissn>1522-1490</eissn><coden>AJPRDO</coden><abstract>Corticotropin releasing factor (CRF) is implicated in sleep and arousal regulation. Exogenous CRF causes sleep suppression that is associated with activation of at least two important arousal systems: pontine noradrenergic and hypothalamic orexin/hypocretin neurons. It is not known whether CRF also impacts sleep-promoting neuronal systems. We hypothesized that CRF-mediated changes in wake and sleep involve decreased activity of hypothalamic sleep-regulatory neurons localized in the preoptic area. To test this hypothesis, we examined the effects of intracerebroventricular administration of CRF on sleep-wake measures and c-Fos expression in GABAergic neurons in the median preoptic nucleus (MnPN) and ventrolateral preoptic area (VLPO) in different experimental conditions. Administration of CRF (0.1 nmol) during baseline rest phase led to delayed sleep onset and decreases in total amount and mean duration of non-rapid eye movement (NREM) sleep. Administration of CRF during acute sleep deprivation (SD) resulted in suppression of recovery sleep and decreased c-Fos expression in MnPN/VLPO GABAergic neurons. Compared with vehicle controls, intracerebroventricular CRF potentiated disturbances of both NREM and REM sleep in rats exposed to a species-specific psychological stressor, the dirty cage of a male conspecific. The number of MnPN/VLPO GABAergic neurons expressing c-Fos was reduced in the CRF-treated group of dirty cage-exposed rats. These findings confirm the involvement of CRF in wake-sleep cycle regulation and suggest that increased CRF signaling in the brain 1) negatively affects homeostatic responses to sleep loss, 2) exacerbates stress-induced disturbances of sleep, and 3) suppresses the activity of sleep-regulatory neurons of the MnPN and VLPO.</abstract><cop>United States</cop><pub>American Physiological Society</pub><pmid>26333784</pmid><doi>10.1152/ajpregu.00176.2015</doi><oa>free_for_read</oa></addata></record>
fulltext fulltext
identifier ISSN: 0363-6119
ispartof American journal of physiology. Regulatory, integrative and comparative physiology, 2015-11, Vol.309 (9), p.R1092-R1100
issn 0363-6119
1522-1490
language eng
recordid cdi_proquest_miscellaneous_1837342395
source MEDLINE; American Physiological Society; Elektronische Zeitschriftenbibliothek - Frei zugängliche E-Journals; Alma/SFX Local Collection
subjects Animals
Brain
Corticotropin-Releasing Hormone - administration & dosage
Corticotropin-Releasing Hormone - pharmacokinetics
Eye movements
GABAergic Neurons - drug effects
GABAergic Neurons - metabolism
Male
Neural Inhibition - drug effects
Neurons
Preoptic Area - drug effects
Preoptic Area - metabolism
Rats
Rats, Sprague-Dawley
Sleep
Sleep Stages - drug effects
Sleep Wake Disorders - chemically induced
Sleep Wake Disorders - metabolism
Wakefulness - drug effects
title Suppression of preoptic sleep-regulatory neuronal activity during corticotropin-releasing factor-induced sleep disturbance
url https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-03T09%3A24%3A55IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_cross&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Suppression%20of%20preoptic%20sleep-regulatory%20neuronal%20activity%20during%20corticotropin-releasing%20factor-induced%20sleep%20disturbance&rft.jtitle=American%20journal%20of%20physiology.%20Regulatory,%20integrative%20and%20comparative%20physiology&rft.au=Gvilia,%20Irma&rft.date=2015-11-01&rft.volume=309&rft.issue=9&rft.spage=R1092&rft.epage=R1100&rft.pages=R1092-R1100&rft.issn=0363-6119&rft.eissn=1522-1490&rft.coden=AJPRDO&rft_id=info:doi/10.1152/ajpregu.00176.2015&rft_dat=%3Cproquest_cross%3E1837342395%3C/proquest_cross%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1731804315&rft_id=info:pmid/26333784&rfr_iscdi=true