Weekend Light Shifts Evoke Persistent Drosophila Circadian Neural Network Desynchrony
We developed a method for single-cell resolution longitudinal bioluminescence imaging of PERIOD (PER) protein and TIMELESS (TIM) oscillations in cultured male adult Drosophila brains that captures circadian circuit-wide cycling under simulated day/night cycles. Light input analysis confirms that CRY...
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| Veröffentlicht in: | The Journal of neuroscience 2021-06, Vol.41 (24), p.5173-5189 |
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| creator | Nave, Ceazar Roberts, Logan Hwu, Patrick Estrella, Jerson D. Vo, Thanh C. Nguyen, Thanh H. Tony Thai Bui Rindner, Daniel J. Pervolarakis, Nicholas Shaw, Paul J. Leise, Tanya L. Holmes, Todd C. |
| description | We developed a method for single-cell resolution longitudinal bioluminescence imaging of PERIOD (PER) protein and TIMELESS (TIM) oscillations in cultured male adult Drosophila brains that captures circadian circuit-wide cycling under simulated day/night cycles. Light input analysis confirms that CRYPTOCHROME (CRY) is the primary circadian photoreceptor and mediates clock disruption by constant light (LL), and that eye light input is redundant to CRY; 3-h light phase delays (Friday) followed by 3-h light phase advances (Monday morning) simulate the common practice of staying up later at night on weekends, sleeping in later on weekend days then returning to standard schedule Monday morning [weekend light shift (WLS)]. PER and TIM oscillations are highly synchronous across all major circadian neuronal subgroups in unshifted light schedules for 11 d. In contrast, WLS significantly dampens PER oscillator synchrony and rhythmicity in most circadian neurons during and after exposure. Lateral ventral neuron (LNv) oscillations are the first to desynchronize in WLS and the last to resynchronize in WLS. Surprisingly, the dorsal neuron group-3 (DN3s) increase their within-group synchrony in response to WLS. In vivo, WLS induces transient defects in sleep stability, learning, and memory that temporally coincide with circuit desynchrony. Our findings suggest that WLS schedules disrupt circuit-wide circadian neuronal oscillator synchrony for much of the week, thus leading to observed behavioral defects in sleep, learning, and memory. |
| doi_str_mv | 10.1523/JNEUROSCI.3074-19.2021 |
| format | Article |
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Light input analysis confirms that CRYPTOCHROME (CRY) is the primary circadian photoreceptor and mediates clock disruption by constant light (LL), and that eye light input is redundant to CRY; 3-h light phase delays (Friday) followed by 3-h light phase advances (Monday morning) simulate the common practice of staying up later at night on weekends, sleeping in later on weekend days then returning to standard schedule Monday morning [weekend light shift (WLS)]. PER and TIM oscillations are highly synchronous across all major circadian neuronal subgroups in unshifted light schedules for 11 d. In contrast, WLS significantly dampens PER oscillator synchrony and rhythmicity in most circadian neurons during and after exposure. Lateral ventral neuron (LNv) oscillations are the first to desynchronize in WLS and the last to resynchronize in WLS. Surprisingly, the dorsal neuron group-3 (DN3s) increase their within-group synchrony in response to WLS. In vivo, WLS induces transient defects in sleep stability, learning, and memory that temporally coincide with circuit desynchrony. Our findings suggest that WLS schedules disrupt circuit-wide circadian neuronal oscillator synchrony for much of the week, thus leading to observed behavioral defects in sleep, learning, and memory.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.3074-19.2021</identifier><identifier>PMID: 33931552</identifier><language>eng</language><publisher>WASHINGTON: Soc Neuroscience</publisher><subject>Animals ; Bioluminescence ; Brain - metabolism ; Brain - physiopathology ; Circadian Rhythm - physiology ; Circadian rhythms ; Circuits ; Cryptochromes - metabolism ; Defects ; Drosophila ; Drosophila Proteins - metabolism ; Eye Proteins - metabolism ; Fruit flies ; Insects ; Learning ; Learning - physiology ; Life Sciences & Biomedicine ; Light ; Male ; Memory - physiology ; Nerve Net - metabolism ; Nerve Net - physiopathology ; Neural networks ; Neurosciences ; Neurosciences & Neurology ; Night ; Oscillations ; Period Circadian Proteins - metabolism ; Schedules ; Science & Technology ; Sleep ; Sleep - physiology ; Subgroups ; Synchronization</subject><ispartof>The Journal of neuroscience, 2021-06, Vol.41 (24), p.5173-5189</ispartof><rights>Copyright © 2021 Nave, Roberts et al.</rights><rights>Copyright Society for Neuroscience Jun 16, 2021</rights><rights>Copyright © 2021 Nave, Roberts et al. 2021</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>true</woscitedreferencessubscribed><woscitedreferencescount>7</woscitedreferencescount><woscitedreferencesoriginalsourcerecordid>wos000662266400004</woscitedreferencesoriginalsourcerecordid><citedby>FETCH-LOGICAL-c442t-420431407b3da5ea2a0cd2077b178294f860e2ec40ba2b0e468b8a36b296e37d3</citedby><cites>FETCH-LOGICAL-c442t-420431407b3da5ea2a0cd2077b178294f860e2ec40ba2b0e468b8a36b296e37d3</cites><orcidid>0000-0002-5098-5296 ; 0000-0001-5061-6098 ; 0000-0002-6770-6206 ; 0000-0001-8152-8832</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/PMC8211545/pdf/$$EPDF$$P50$$Gpubmedcentral$$Hfree_for_read</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC8211545/$$EHTML$$P50$$Gpubmedcentral$$Hfree_for_read</linktohtml><link.rule.ids>230,315,729,782,786,887,27933,27934,39267,53800,53802</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33931552$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Nave, Ceazar</creatorcontrib><creatorcontrib>Roberts, Logan</creatorcontrib><creatorcontrib>Hwu, Patrick</creatorcontrib><creatorcontrib>Estrella, Jerson D.</creatorcontrib><creatorcontrib>Vo, Thanh C.</creatorcontrib><creatorcontrib>Nguyen, Thanh H.</creatorcontrib><creatorcontrib>Tony Thai Bui</creatorcontrib><creatorcontrib>Rindner, Daniel J.</creatorcontrib><creatorcontrib>Pervolarakis, Nicholas</creatorcontrib><creatorcontrib>Shaw, Paul J.</creatorcontrib><creatorcontrib>Leise, Tanya L.</creatorcontrib><creatorcontrib>Holmes, Todd C.</creatorcontrib><title>Weekend Light Shifts Evoke Persistent Drosophila Circadian Neural Network Desynchrony</title><title>The Journal of neuroscience</title><addtitle>J NEUROSCI</addtitle><addtitle>J Neurosci</addtitle><description>We developed a method for single-cell resolution longitudinal bioluminescence imaging of PERIOD (PER) protein and TIMELESS (TIM) oscillations in cultured male adult Drosophila brains that captures circadian circuit-wide cycling under simulated day/night cycles. Light input analysis confirms that CRYPTOCHROME (CRY) is the primary circadian photoreceptor and mediates clock disruption by constant light (LL), and that eye light input is redundant to CRY; 3-h light phase delays (Friday) followed by 3-h light phase advances (Monday morning) simulate the common practice of staying up later at night on weekends, sleeping in later on weekend days then returning to standard schedule Monday morning [weekend light shift (WLS)]. PER and TIM oscillations are highly synchronous across all major circadian neuronal subgroups in unshifted light schedules for 11 d. In contrast, WLS significantly dampens PER oscillator synchrony and rhythmicity in most circadian neurons during and after exposure. Lateral ventral neuron (LNv) oscillations are the first to desynchronize in WLS and the last to resynchronize in WLS. Surprisingly, the dorsal neuron group-3 (DN3s) increase their within-group synchrony in response to WLS. In vivo, WLS induces transient defects in sleep stability, learning, and memory that temporally coincide with circuit desynchrony. Our findings suggest that WLS schedules disrupt circuit-wide circadian neuronal oscillator synchrony for much of the week, thus leading to observed behavioral defects in sleep, learning, and memory.</description><subject>Animals</subject><subject>Bioluminescence</subject><subject>Brain - metabolism</subject><subject>Brain - physiopathology</subject><subject>Circadian Rhythm - physiology</subject><subject>Circadian rhythms</subject><subject>Circuits</subject><subject>Cryptochromes - metabolism</subject><subject>Defects</subject><subject>Drosophila</subject><subject>Drosophila Proteins - metabolism</subject><subject>Eye Proteins - metabolism</subject><subject>Fruit flies</subject><subject>Insects</subject><subject>Learning</subject><subject>Learning - physiology</subject><subject>Life Sciences & Biomedicine</subject><subject>Light</subject><subject>Male</subject><subject>Memory - physiology</subject><subject>Nerve Net - metabolism</subject><subject>Nerve Net - physiopathology</subject><subject>Neural networks</subject><subject>Neurosciences</subject><subject>Neurosciences & Neurology</subject><subject>Night</subject><subject>Oscillations</subject><subject>Period Circadian Proteins - metabolism</subject><subject>Schedules</subject><subject>Science & Technology</subject><subject>Sleep</subject><subject>Sleep - physiology</subject><subject>Subgroups</subject><subject>Synchronization</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>HGBXW</sourceid><sourceid>EIF</sourceid><recordid>eNqNkU9vEzEQxS0EoiHwFaqVuCChDf639u4FCW0DLYpaRIk4Wt7d2a6bxE5tb6t8-zqkRMCJ04w0v3maeQ-hU4JnpKDsw9fL-fL71XV9MWNY8pxUM4opeYYmaVrllGPyHE0wlTgXXPIT9CqEW4yxxES-RCeMVYwUBZ2g5U-AFdguW5ibIWbXg-ljyOb3bgXZN_DBhAg2ZmfeBbcdzFpntfGt7oy22SWMXq9TiQ_Or7IzCDvbDt7Z3Wv0otfrAG-e6hQtP89_1Of54urLRf1pkbec05hzijkjHMuGdboATTVuO4qlbIgsacX7UmCg0HLcaNpg4KJsSs1EQysBTHZsij4edLdjs4GuTaemi9TWm432O-W0UX9PrBnUjbtXJSWk4EUSePck4N3dCCGqjQktrNfaghuDogXFpahYJRL69h_01o3epvcSVRCZ_PwlKA5UmxwLHvrjMQSrfXLqmJzaJ6dIpfbJpcXTP185rv2OKgHvD8ADNK4PrQHbwhFL2QpBqRA8dcnVKSr_n65N1NE4W7vRRvYI6_y2hw</recordid><startdate>20210616</startdate><enddate>20210616</enddate><creator>Nave, Ceazar</creator><creator>Roberts, Logan</creator><creator>Hwu, Patrick</creator><creator>Estrella, Jerson D.</creator><creator>Vo, Thanh C.</creator><creator>Nguyen, Thanh H.</creator><creator>Tony Thai Bui</creator><creator>Rindner, Daniel J.</creator><creator>Pervolarakis, Nicholas</creator><creator>Shaw, Paul J.</creator><creator>Leise, Tanya L.</creator><creator>Holmes, Todd C.</creator><general>Soc Neuroscience</general><general>Society for Neuroscience</general><scope>BLEPL</scope><scope>DTL</scope><scope>HGBXW</scope><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/0000-0002-5098-5296</orcidid><orcidid>https://orcid.org/0000-0001-5061-6098</orcidid><orcidid>https://orcid.org/0000-0002-6770-6206</orcidid><orcidid>https://orcid.org/0000-0001-8152-8832</orcidid></search><sort><creationdate>20210616</creationdate><title>Weekend Light Shifts Evoke Persistent Drosophila Circadian Neural Network Desynchrony</title><author>Nave, Ceazar ; 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Light input analysis confirms that CRYPTOCHROME (CRY) is the primary circadian photoreceptor and mediates clock disruption by constant light (LL), and that eye light input is redundant to CRY; 3-h light phase delays (Friday) followed by 3-h light phase advances (Monday morning) simulate the common practice of staying up later at night on weekends, sleeping in later on weekend days then returning to standard schedule Monday morning [weekend light shift (WLS)]. PER and TIM oscillations are highly synchronous across all major circadian neuronal subgroups in unshifted light schedules for 11 d. In contrast, WLS significantly dampens PER oscillator synchrony and rhythmicity in most circadian neurons during and after exposure. Lateral ventral neuron (LNv) oscillations are the first to desynchronize in WLS and the last to resynchronize in WLS. Surprisingly, the dorsal neuron group-3 (DN3s) increase their within-group synchrony in response to WLS. 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| subjects | Animals Bioluminescence Brain - metabolism Brain - physiopathology Circadian Rhythm - physiology Circadian rhythms Circuits Cryptochromes - metabolism Defects Drosophila Drosophila Proteins - metabolism Eye Proteins - metabolism Fruit flies Insects Learning Learning - physiology Life Sciences & Biomedicine Light Male Memory - physiology Nerve Net - metabolism Nerve Net - physiopathology Neural networks Neurosciences Neurosciences & Neurology Night Oscillations Period Circadian Proteins - metabolism Schedules Science & Technology Sleep Sleep - physiology Subgroups Synchronization |
| title | Weekend Light Shifts Evoke Persistent Drosophila Circadian Neural Network Desynchrony |
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