Circadian Modulation of Neurons and Astrocytes Controls Synaptic Plasticity in Hippocampal Area CA1
Most animal species operate according to a 24-h period set by the suprachiasmatic nucleus (SCN) of the hypothalamus. The rhythmic activity of the SCN modulates hippocampal-dependent memory, but the molecular and cellular mechanisms that account for this effect remain largely unknown. Here, we identi...
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Veröffentlicht in: | Cell reports (Cambridge) 2020-10, Vol.33 (2), p.108255-108255, Article 108255 |
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creator | McCauley, John P. Petroccione, Maurice A. D’Brant, Lianna Y. Todd, Gabrielle C. Affinnih, Nurat Wisnoski, Justin J. Zahid, Shergil Shree, Swasti Sousa, Alioscka A. De Guzman, Rose M. Migliore, Rosanna Brazhe, Alexey Leapman, Richard D. Khmaladze, Alexander Semyanov, Alexey Zuloaga, Damian G. Migliore, Michele Scimemi, Annalisa |
description | Most animal species operate according to a 24-h period set by the suprachiasmatic nucleus (SCN) of the hypothalamus. The rhythmic activity of the SCN modulates hippocampal-dependent memory, but the molecular and cellular mechanisms that account for this effect remain largely unknown. Here, we identify cell-type-specific structural and functional changes that occur with circadian rhythmicity in neurons and astrocytes in hippocampal area CA1. Pyramidal neurons change the surface expression of NMDA receptors. Astrocytes change their proximity to synapses. Together, these phenomena alter glutamate clearance, receptor activation, and integration of temporally clustered excitatory synaptic inputs, ultimately shaping hippocampal-dependent learning in vivo. We identify corticosterone as a key contributor to changes in synaptic strength. These findings highlight important mechanisms through which neurons and astrocytes modify the molecular composition and structure of the synaptic environment, contribute to the local storage of information in the hippocampus, and alter the temporal dynamics of cognitive processing.
[Display omitted]
•Hippocampal plasticity varies with circadian rhythmicity•Neurons reduce the surface expression of NMDA receptors during the dark phase•Astrocytes retract their processes from synapses during the dark phase•These effects alter synaptic integration and hippocampal-dependent learning
McCauley et al. shed light on the molecular and cellular mechanisms that allow hippocampal neurons and astrocytes to shape circadian changes in synaptic plasticity and hippocampal-dependent behaviors. They identify corticosterone as a key molecule mediating these effects, capable of tuning the temporal dynamics of cognitive processing in mice. |
doi_str_mv | 10.1016/j.celrep.2020.108255 |
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[Display omitted]
•Hippocampal plasticity varies with circadian rhythmicity•Neurons reduce the surface expression of NMDA receptors during the dark phase•Astrocytes retract their processes from synapses during the dark phase•These effects alter synaptic integration and hippocampal-dependent learning
McCauley et al. shed light on the molecular and cellular mechanisms that allow hippocampal neurons and astrocytes to shape circadian changes in synaptic plasticity and hippocampal-dependent behaviors. They identify corticosterone as a key molecule mediating these effects, capable of tuning the temporal dynamics of cognitive processing in mice.</description><identifier>ISSN: 2211-1247</identifier><identifier>EISSN: 2211-1247</identifier><identifier>DOI: 10.1016/j.celrep.2020.108255</identifier><identifier>PMID: 33053337</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid - metabolism ; Amino Acid Transport System X-AG - metabolism ; Animals ; astrocytes ; Astrocytes - physiology ; CA1 Region, Hippocampal - physiology ; CA1 Region, Hippocampal - ultrastructure ; Circadian Clocks - genetics ; Circadian Rhythm - physiology ; circadian rhythms ; corticosterone ; Corticosterone - metabolism ; Darkness ; Excitatory Postsynaptic Potentials - physiology ; Gene Expression Regulation ; glutamate ; Glutamic Acid - metabolism ; hippocampus ; learning and memory ; Memory - physiology ; Mice, Inbred C57BL ; Neuronal Plasticity - physiology ; Neurons - physiology ; Neuropil Threads - metabolism ; Open Field Test ; Receptors, N-Methyl-D-Aspartate - metabolism ; synapses ; Synapses - physiology ; synaptic integration ; Time Factors</subject><ispartof>Cell reports (Cambridge), 2020-10, Vol.33 (2), p.108255-108255, Article 108255</ispartof><rights>2020 The Author(s)</rights><rights>Copyright © 2020 The Author(s). Published by Elsevier Inc. All rights reserved.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c463t-462c02235fcc58d7b1e3c1b505e35cc70674394bffd58618edaa230948ae946b3</citedby><cites>FETCH-LOGICAL-c463t-462c02235fcc58d7b1e3c1b505e35cc70674394bffd58618edaa230948ae946b3</cites><orcidid>0000-0001-9034-7849 ; 0000-0002-2429-079X ; 0000-0001-7628-8811 ; 0000-0001-6476-8535 ; 0000-0003-0330-3595 ; 0000-0003-4333-4310 ; 0000-0002-9771-2623 ; 0000-0001-7591-6855 ; 0000-0001-7443-5363 ; 0000-0003-4975-093X</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,864,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33053337$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>McCauley, John P.</creatorcontrib><creatorcontrib>Petroccione, Maurice A.</creatorcontrib><creatorcontrib>D’Brant, Lianna Y.</creatorcontrib><creatorcontrib>Todd, Gabrielle C.</creatorcontrib><creatorcontrib>Affinnih, Nurat</creatorcontrib><creatorcontrib>Wisnoski, Justin J.</creatorcontrib><creatorcontrib>Zahid, Shergil</creatorcontrib><creatorcontrib>Shree, Swasti</creatorcontrib><creatorcontrib>Sousa, Alioscka A.</creatorcontrib><creatorcontrib>De Guzman, Rose M.</creatorcontrib><creatorcontrib>Migliore, Rosanna</creatorcontrib><creatorcontrib>Brazhe, Alexey</creatorcontrib><creatorcontrib>Leapman, Richard D.</creatorcontrib><creatorcontrib>Khmaladze, Alexander</creatorcontrib><creatorcontrib>Semyanov, Alexey</creatorcontrib><creatorcontrib>Zuloaga, Damian G.</creatorcontrib><creatorcontrib>Migliore, Michele</creatorcontrib><creatorcontrib>Scimemi, Annalisa</creatorcontrib><title>Circadian Modulation of Neurons and Astrocytes Controls Synaptic Plasticity in Hippocampal Area CA1</title><title>Cell reports (Cambridge)</title><addtitle>Cell Rep</addtitle><description>Most animal species operate according to a 24-h period set by the suprachiasmatic nucleus (SCN) of the hypothalamus. The rhythmic activity of the SCN modulates hippocampal-dependent memory, but the molecular and cellular mechanisms that account for this effect remain largely unknown. Here, we identify cell-type-specific structural and functional changes that occur with circadian rhythmicity in neurons and astrocytes in hippocampal area CA1. Pyramidal neurons change the surface expression of NMDA receptors. Astrocytes change their proximity to synapses. Together, these phenomena alter glutamate clearance, receptor activation, and integration of temporally clustered excitatory synaptic inputs, ultimately shaping hippocampal-dependent learning in vivo. We identify corticosterone as a key contributor to changes in synaptic strength. These findings highlight important mechanisms through which neurons and astrocytes modify the molecular composition and structure of the synaptic environment, contribute to the local storage of information in the hippocampus, and alter the temporal dynamics of cognitive processing.
[Display omitted]
•Hippocampal plasticity varies with circadian rhythmicity•Neurons reduce the surface expression of NMDA receptors during the dark phase•Astrocytes retract their processes from synapses during the dark phase•These effects alter synaptic integration and hippocampal-dependent learning
McCauley et al. shed light on the molecular and cellular mechanisms that allow hippocampal neurons and astrocytes to shape circadian changes in synaptic plasticity and hippocampal-dependent behaviors. They identify corticosterone as a key molecule mediating these effects, capable of tuning the temporal dynamics of cognitive processing in mice.</description><subject>alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid - metabolism</subject><subject>Amino Acid Transport System X-AG - metabolism</subject><subject>Animals</subject><subject>astrocytes</subject><subject>Astrocytes - physiology</subject><subject>CA1 Region, Hippocampal - physiology</subject><subject>CA1 Region, Hippocampal - ultrastructure</subject><subject>Circadian Clocks - genetics</subject><subject>Circadian Rhythm - physiology</subject><subject>circadian rhythms</subject><subject>corticosterone</subject><subject>Corticosterone - metabolism</subject><subject>Darkness</subject><subject>Excitatory Postsynaptic Potentials - physiology</subject><subject>Gene Expression Regulation</subject><subject>glutamate</subject><subject>Glutamic Acid - metabolism</subject><subject>hippocampus</subject><subject>learning and memory</subject><subject>Memory - physiology</subject><subject>Mice, Inbred C57BL</subject><subject>Neuronal Plasticity - physiology</subject><subject>Neurons - physiology</subject><subject>Neuropil Threads - metabolism</subject><subject>Open Field Test</subject><subject>Receptors, N-Methyl-D-Aspartate - metabolism</subject><subject>synapses</subject><subject>Synapses - physiology</subject><subject>synaptic integration</subject><subject>Time Factors</subject><issn>2211-1247</issn><issn>2211-1247</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kctuFDEQRS1ERKIkf4CQl2xm8LMfG6RRixCkQCIBa8tdrgaPeuzG7o40f49HkxcbvKmSXXWrfA8hbzlbc8arD9s14JhwWgsmDleN0PoVOROC8xUXqn79Ij8llzlvWTkV47xVb8iplExLKeszAp1PYJ23gX6Nbhnt7GOgcaDfcEkxZGqDo5s8pwj7GTPtYij5mOn3fbDT7IHejTaX6Oc99YFe-2mKYHeTHekmoaXdhl-Qk8GOGS8f4jn5efXpR3e9urn9_KXb3KxAVXJeqUoAE0LqAUA3ru45SuC9ZhqlBqhZVSvZqn4YnG4q3qCzVkjWqsZiq6penpOPR91p6XfoAMuqdjRT8jub9iZab_59Cf63-RXvTV2z4iArAu8fBFL8s2Cezc7nYvRoA8YlG6E0lw0Xui2l6lgKKeaccHgaw5k5IDJbc0RkDojMEVFpe_dyxaemRyDPf8Bi1L3HZDJ4DIDOJ4TZuOj_P-EvYsek7w</recordid><startdate>20201013</startdate><enddate>20201013</enddate><creator>McCauley, John P.</creator><creator>Petroccione, Maurice A.</creator><creator>D’Brant, Lianna Y.</creator><creator>Todd, Gabrielle C.</creator><creator>Affinnih, Nurat</creator><creator>Wisnoski, Justin J.</creator><creator>Zahid, Shergil</creator><creator>Shree, Swasti</creator><creator>Sousa, Alioscka A.</creator><creator>De Guzman, Rose M.</creator><creator>Migliore, Rosanna</creator><creator>Brazhe, Alexey</creator><creator>Leapman, Richard D.</creator><creator>Khmaladze, Alexander</creator><creator>Semyanov, Alexey</creator><creator>Zuloaga, Damian G.</creator><creator>Migliore, Michele</creator><creator>Scimemi, Annalisa</creator><general>Elsevier Inc</general><scope>6I.</scope><scope>AAFTH</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>7X8</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0001-9034-7849</orcidid><orcidid>https://orcid.org/0000-0002-2429-079X</orcidid><orcidid>https://orcid.org/0000-0001-7628-8811</orcidid><orcidid>https://orcid.org/0000-0001-6476-8535</orcidid><orcidid>https://orcid.org/0000-0003-0330-3595</orcidid><orcidid>https://orcid.org/0000-0003-4333-4310</orcidid><orcidid>https://orcid.org/0000-0002-9771-2623</orcidid><orcidid>https://orcid.org/0000-0001-7591-6855</orcidid><orcidid>https://orcid.org/0000-0001-7443-5363</orcidid><orcidid>https://orcid.org/0000-0003-4975-093X</orcidid></search><sort><creationdate>20201013</creationdate><title>Circadian Modulation of Neurons and Astrocytes Controls Synaptic Plasticity in Hippocampal Area CA1</title><author>McCauley, John P. ; Petroccione, Maurice A. ; D’Brant, Lianna Y. ; Todd, Gabrielle C. ; Affinnih, Nurat ; Wisnoski, Justin J. ; Zahid, Shergil ; Shree, Swasti ; Sousa, Alioscka A. ; De Guzman, Rose M. ; Migliore, Rosanna ; Brazhe, Alexey ; Leapman, Richard D. ; Khmaladze, Alexander ; Semyanov, Alexey ; Zuloaga, Damian G. ; Migliore, Michele ; Scimemi, Annalisa</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c463t-462c02235fcc58d7b1e3c1b505e35cc70674394bffd58618edaa230948ae946b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid - metabolism</topic><topic>Amino Acid Transport System X-AG - metabolism</topic><topic>Animals</topic><topic>astrocytes</topic><topic>Astrocytes - physiology</topic><topic>CA1 Region, Hippocampal - physiology</topic><topic>CA1 Region, Hippocampal - ultrastructure</topic><topic>Circadian Clocks - genetics</topic><topic>Circadian Rhythm - physiology</topic><topic>circadian rhythms</topic><topic>corticosterone</topic><topic>Corticosterone - metabolism</topic><topic>Darkness</topic><topic>Excitatory Postsynaptic Potentials - physiology</topic><topic>Gene Expression Regulation</topic><topic>glutamate</topic><topic>Glutamic Acid - metabolism</topic><topic>hippocampus</topic><topic>learning and memory</topic><topic>Memory - physiology</topic><topic>Mice, Inbred C57BL</topic><topic>Neuronal Plasticity - physiology</topic><topic>Neurons - physiology</topic><topic>Neuropil Threads - metabolism</topic><topic>Open Field Test</topic><topic>Receptors, N-Methyl-D-Aspartate - metabolism</topic><topic>synapses</topic><topic>Synapses - physiology</topic><topic>synaptic integration</topic><topic>Time Factors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>McCauley, John P.</creatorcontrib><creatorcontrib>Petroccione, Maurice A.</creatorcontrib><creatorcontrib>D’Brant, Lianna Y.</creatorcontrib><creatorcontrib>Todd, Gabrielle C.</creatorcontrib><creatorcontrib>Affinnih, Nurat</creatorcontrib><creatorcontrib>Wisnoski, Justin J.</creatorcontrib><creatorcontrib>Zahid, Shergil</creatorcontrib><creatorcontrib>Shree, Swasti</creatorcontrib><creatorcontrib>Sousa, Alioscka A.</creatorcontrib><creatorcontrib>De Guzman, Rose M.</creatorcontrib><creatorcontrib>Migliore, Rosanna</creatorcontrib><creatorcontrib>Brazhe, Alexey</creatorcontrib><creatorcontrib>Leapman, Richard D.</creatorcontrib><creatorcontrib>Khmaladze, Alexander</creatorcontrib><creatorcontrib>Semyanov, Alexey</creatorcontrib><creatorcontrib>Zuloaga, Damian G.</creatorcontrib><creatorcontrib>Migliore, Michele</creatorcontrib><creatorcontrib>Scimemi, Annalisa</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Cell reports (Cambridge)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>McCauley, John P.</au><au>Petroccione, Maurice A.</au><au>D’Brant, Lianna Y.</au><au>Todd, Gabrielle C.</au><au>Affinnih, Nurat</au><au>Wisnoski, Justin J.</au><au>Zahid, Shergil</au><au>Shree, Swasti</au><au>Sousa, Alioscka A.</au><au>De Guzman, Rose M.</au><au>Migliore, Rosanna</au><au>Brazhe, Alexey</au><au>Leapman, Richard D.</au><au>Khmaladze, Alexander</au><au>Semyanov, Alexey</au><au>Zuloaga, Damian G.</au><au>Migliore, Michele</au><au>Scimemi, Annalisa</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Circadian Modulation of Neurons and Astrocytes Controls Synaptic Plasticity in Hippocampal Area CA1</atitle><jtitle>Cell reports (Cambridge)</jtitle><addtitle>Cell Rep</addtitle><date>2020-10-13</date><risdate>2020</risdate><volume>33</volume><issue>2</issue><spage>108255</spage><epage>108255</epage><pages>108255-108255</pages><artnum>108255</artnum><issn>2211-1247</issn><eissn>2211-1247</eissn><abstract>Most animal species operate according to a 24-h period set by the suprachiasmatic nucleus (SCN) of the hypothalamus. The rhythmic activity of the SCN modulates hippocampal-dependent memory, but the molecular and cellular mechanisms that account for this effect remain largely unknown. Here, we identify cell-type-specific structural and functional changes that occur with circadian rhythmicity in neurons and astrocytes in hippocampal area CA1. Pyramidal neurons change the surface expression of NMDA receptors. Astrocytes change their proximity to synapses. Together, these phenomena alter glutamate clearance, receptor activation, and integration of temporally clustered excitatory synaptic inputs, ultimately shaping hippocampal-dependent learning in vivo. We identify corticosterone as a key contributor to changes in synaptic strength. These findings highlight important mechanisms through which neurons and astrocytes modify the molecular composition and structure of the synaptic environment, contribute to the local storage of information in the hippocampus, and alter the temporal dynamics of cognitive processing.
[Display omitted]
•Hippocampal plasticity varies with circadian rhythmicity•Neurons reduce the surface expression of NMDA receptors during the dark phase•Astrocytes retract their processes from synapses during the dark phase•These effects alter synaptic integration and hippocampal-dependent learning
McCauley et al. shed light on the molecular and cellular mechanisms that allow hippocampal neurons and astrocytes to shape circadian changes in synaptic plasticity and hippocampal-dependent behaviors. They identify corticosterone as a key molecule mediating these effects, capable of tuning the temporal dynamics of cognitive processing in mice.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>33053337</pmid><doi>10.1016/j.celrep.2020.108255</doi><tpages>1</tpages><orcidid>https://orcid.org/0000-0001-9034-7849</orcidid><orcidid>https://orcid.org/0000-0002-2429-079X</orcidid><orcidid>https://orcid.org/0000-0001-7628-8811</orcidid><orcidid>https://orcid.org/0000-0001-6476-8535</orcidid><orcidid>https://orcid.org/0000-0003-0330-3595</orcidid><orcidid>https://orcid.org/0000-0003-4333-4310</orcidid><orcidid>https://orcid.org/0000-0002-9771-2623</orcidid><orcidid>https://orcid.org/0000-0001-7591-6855</orcidid><orcidid>https://orcid.org/0000-0001-7443-5363</orcidid><orcidid>https://orcid.org/0000-0003-4975-093X</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | alpha-Amino-3-hydroxy-5-methyl-4-isoxazolepropionic Acid - metabolism Amino Acid Transport System X-AG - metabolism Animals astrocytes Astrocytes - physiology CA1 Region, Hippocampal - physiology CA1 Region, Hippocampal - ultrastructure Circadian Clocks - genetics Circadian Rhythm - physiology circadian rhythms corticosterone Corticosterone - metabolism Darkness Excitatory Postsynaptic Potentials - physiology Gene Expression Regulation glutamate Glutamic Acid - metabolism hippocampus learning and memory Memory - physiology Mice, Inbred C57BL Neuronal Plasticity - physiology Neurons - physiology Neuropil Threads - metabolism Open Field Test Receptors, N-Methyl-D-Aspartate - metabolism synapses Synapses - physiology synaptic integration Time Factors |
title | Circadian Modulation of Neurons and Astrocytes Controls Synaptic Plasticity in Hippocampal Area CA1 |
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