Diurnal changes in perineuronal nets and parvalbumin neurons in the rat medial prefrontal cortex
Perineuronal nets (PNNs) surrounding fast-spiking, parvalbumin (PV) interneurons provide excitatory:inhibitory balance, which is impaired in several disorders associated with altered diurnal rhythms, yet few studies have examined diurnal rhythms of PNNs or PV cells. We measured the intensity and num...
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Veröffentlicht in: | Brain Structure and Function 2021-05, Vol.226 (4), p.1135-1153 |
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creator | Harkness, John H. Gonzalez, Angela E. Bushana, Priyanka N. Jorgensen, Emily T. Hegarty, Deborah M. Di Nardo, Ariel A. Prochiantz, Alain Wisor, Jonathan P. Aicher, Sue A. Brown, Travis E. Sorg, Barbara A. |
description | Perineuronal nets (PNNs) surrounding fast-spiking, parvalbumin (PV) interneurons provide excitatory:inhibitory balance, which is impaired in several disorders associated with altered diurnal rhythms, yet few studies have examined diurnal rhythms of PNNs or PV cells. We measured the intensity and number of PV cells and PNNs labeled with
Wisteria floribunda
agglutinin (WFA) and also the oxidative stress marker 8-oxo-deoxyguanosine (8-oxo-dG) in rat prelimbic medial prefrontal cortex (mPFC) at Zeitgeber times (ZT) ZT0
(
lights-on, inactive phase), ZT6 (mid-inactive phase), ZT12 (lights-off, active phase), and ZT18 (mid-active phase). Relative to ZT0, the intensities of PNN and PV labeling were increased in the dark (active) phase compared with the light (inactive) phase. The intensity of 8-oxo-dG was decreased from ZT0 at all times (ZT6,12,18). We also measured GAD 65/67 and vGLUT1 puncta apposed to PV cells with and without PNNs. There were more excitatory puncta on PV cells with PNNs at ZT18 vs. ZT6, but no changes in PV cells without PNNs and no changes in inhibitory puncta. Whole-cell slice recordings in fast-spiking (PV) cells with PNNs showed an increased ratio of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor:N-methyl-D-aspartate receptor (AMPA: NMDA) at ZT18 vs. ZT6. The number of PV cells and PV/PNN cells containing orthodenticle homeobox 2 (OTX2), which maintains PNNs, showed a strong trend toward an increase from ZT6 to ZT18. Diurnal fluctuations in PNNs and PV cells are expected to alter cortical excitatory:inhibitory balance and provide new insights into treatments for diseases impacted by disturbances in sleep and circadian rhythms. |
doi_str_mv | 10.1007/s00429-021-02229-4 |
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Wisteria floribunda
agglutinin (WFA) and also the oxidative stress marker 8-oxo-deoxyguanosine (8-oxo-dG) in rat prelimbic medial prefrontal cortex (mPFC) at Zeitgeber times (ZT) ZT0
(
lights-on, inactive phase), ZT6 (mid-inactive phase), ZT12 (lights-off, active phase), and ZT18 (mid-active phase). Relative to ZT0, the intensities of PNN and PV labeling were increased in the dark (active) phase compared with the light (inactive) phase. The intensity of 8-oxo-dG was decreased from ZT0 at all times (ZT6,12,18). We also measured GAD 65/67 and vGLUT1 puncta apposed to PV cells with and without PNNs. There were more excitatory puncta on PV cells with PNNs at ZT18 vs. ZT6, but no changes in PV cells without PNNs and no changes in inhibitory puncta. Whole-cell slice recordings in fast-spiking (PV) cells with PNNs showed an increased ratio of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor:N-methyl-D-aspartate receptor (AMPA: NMDA) at ZT18 vs. ZT6. The number of PV cells and PV/PNN cells containing orthodenticle homeobox 2 (OTX2), which maintains PNNs, showed a strong trend toward an increase from ZT6 to ZT18. Diurnal fluctuations in PNNs and PV cells are expected to alter cortical excitatory:inhibitory balance and provide new insights into treatments for diseases impacted by disturbances in sleep and circadian rhythms.</description><identifier>ISSN: 1863-2653</identifier><identifier>EISSN: 1863-2661</identifier><identifier>EISSN: 0340-2061</identifier><identifier>DOI: 10.1007/s00429-021-02229-4</identifier><identifier>PMID: 33585984</identifier><language>eng</language><publisher>Berlin/Heidelberg: Springer Berlin Heidelberg</publisher><subject>8-Hydroxy-2'-Deoxyguanosine ; 8-Hydroxydeoxyguanosine ; Animals ; Biomedical and Life Sciences ; Biomedicine ; Cell Biology ; Circadian rhythm ; Circadian rhythms ; Diurnal ; Glutamate receptors ; Glutamic acid receptors (ionotropic) ; Homeobox ; Interneurons ; Life Sciences ; N-Methyl-D-aspartic acid receptors ; Nets ; Neurobiology ; Neurology ; Neurons - metabolism ; Neurons and Cognition ; Neurosciences ; Original Article ; Otx2 protein ; Oxidative stress ; Parvalbumin ; Parvalbumins - metabolism ; Perineuronal nets ; Photovoltaic cells ; Prefrontal cortex ; Prefrontal Cortex - metabolism ; Rats ; Sleep ; α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid</subject><ispartof>Brain Structure and Function, 2021-05, Vol.226 (4), p.1135-1153</ispartof><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH, DE part of Springer Nature 2021</rights><rights>The Author(s), under exclusive licence to Springer-Verlag GmbH, DE part of Springer Nature 2021.</rights><rights>Distributed under a Creative Commons Attribution 4.0 International License</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c574t-1a554eaababaa0c0272031f5c2350dc7e02c345b24435ae711ff52ccce2486fb3</citedby><cites>FETCH-LOGICAL-c574t-1a554eaababaa0c0272031f5c2350dc7e02c345b24435ae711ff52ccce2486fb3</cites><orcidid>0000-0002-4913-4910 ; 0000-0001-7626-5863</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1007/s00429-021-02229-4$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1007/s00429-021-02229-4$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>230,314,777,781,882,27905,27906,41469,42538,51300</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/33585984$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttps://hal.science/hal-03428849$$DView record in HAL$$Hfree_for_read</backlink></links><search><creatorcontrib>Harkness, John H.</creatorcontrib><creatorcontrib>Gonzalez, Angela E.</creatorcontrib><creatorcontrib>Bushana, Priyanka N.</creatorcontrib><creatorcontrib>Jorgensen, Emily T.</creatorcontrib><creatorcontrib>Hegarty, Deborah M.</creatorcontrib><creatorcontrib>Di Nardo, Ariel A.</creatorcontrib><creatorcontrib>Prochiantz, Alain</creatorcontrib><creatorcontrib>Wisor, Jonathan P.</creatorcontrib><creatorcontrib>Aicher, Sue A.</creatorcontrib><creatorcontrib>Brown, Travis E.</creatorcontrib><creatorcontrib>Sorg, Barbara A.</creatorcontrib><title>Diurnal changes in perineuronal nets and parvalbumin neurons in the rat medial prefrontal cortex</title><title>Brain Structure and Function</title><addtitle>Brain Struct Funct</addtitle><addtitle>Brain Struct Funct</addtitle><description>Perineuronal nets (PNNs) surrounding fast-spiking, parvalbumin (PV) interneurons provide excitatory:inhibitory balance, which is impaired in several disorders associated with altered diurnal rhythms, yet few studies have examined diurnal rhythms of PNNs or PV cells. We measured the intensity and number of PV cells and PNNs labeled with
Wisteria floribunda
agglutinin (WFA) and also the oxidative stress marker 8-oxo-deoxyguanosine (8-oxo-dG) in rat prelimbic medial prefrontal cortex (mPFC) at Zeitgeber times (ZT) ZT0
(
lights-on, inactive phase), ZT6 (mid-inactive phase), ZT12 (lights-off, active phase), and ZT18 (mid-active phase). Relative to ZT0, the intensities of PNN and PV labeling were increased in the dark (active) phase compared with the light (inactive) phase. The intensity of 8-oxo-dG was decreased from ZT0 at all times (ZT6,12,18). We also measured GAD 65/67 and vGLUT1 puncta apposed to PV cells with and without PNNs. There were more excitatory puncta on PV cells with PNNs at ZT18 vs. ZT6, but no changes in PV cells without PNNs and no changes in inhibitory puncta. Whole-cell slice recordings in fast-spiking (PV) cells with PNNs showed an increased ratio of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor:N-methyl-D-aspartate receptor (AMPA: NMDA) at ZT18 vs. ZT6. The number of PV cells and PV/PNN cells containing orthodenticle homeobox 2 (OTX2), which maintains PNNs, showed a strong trend toward an increase from ZT6 to ZT18. Diurnal fluctuations in PNNs and PV cells are expected to alter cortical excitatory:inhibitory balance and provide new insights into treatments for diseases impacted by disturbances in sleep and circadian rhythms.</description><subject>8-Hydroxy-2'-Deoxyguanosine</subject><subject>8-Hydroxydeoxyguanosine</subject><subject>Animals</subject><subject>Biomedical and Life Sciences</subject><subject>Biomedicine</subject><subject>Cell Biology</subject><subject>Circadian rhythm</subject><subject>Circadian rhythms</subject><subject>Diurnal</subject><subject>Glutamate receptors</subject><subject>Glutamic acid receptors (ionotropic)</subject><subject>Homeobox</subject><subject>Interneurons</subject><subject>Life Sciences</subject><subject>N-Methyl-D-aspartic acid receptors</subject><subject>Nets</subject><subject>Neurobiology</subject><subject>Neurology</subject><subject>Neurons - metabolism</subject><subject>Neurons and Cognition</subject><subject>Neurosciences</subject><subject>Original Article</subject><subject>Otx2 protein</subject><subject>Oxidative stress</subject><subject>Parvalbumin</subject><subject>Parvalbumins - metabolism</subject><subject>Perineuronal nets</subject><subject>Photovoltaic cells</subject><subject>Prefrontal cortex</subject><subject>Prefrontal Cortex - metabolism</subject><subject>Rats</subject><subject>Sleep</subject><subject>α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid</subject><issn>1863-2653</issn><issn>1863-2661</issn><issn>0340-2061</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2021</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>ABUWG</sourceid><sourceid>AFKRA</sourceid><sourceid>AZQEC</sourceid><sourceid>BENPR</sourceid><sourceid>CCPQU</sourceid><sourceid>DWQXO</sourceid><sourceid>GNUQQ</sourceid><recordid>eNp9kU1v1DAQhi0EoqXwBzigSFzgEBh_JfYFqWqBIq3EBc7G8U66qbJOsJNV-fed3ZQFekCW5ZHnmXfGfhl7yeEdB6jfZwAlbAmC0xYUqUfslJtKlqKq-ONjrOUJe5bzDYC2htun7ERKbShWp-zHZTen6PsibHy8xlx0sRgxdRHnNOzvI0658HFdjD7tfN_MWyKW7AGeNlgkPxVbXHeEjwlbSk17xSFNePucPWl9n_HF_XnGvn_6-O3iqlx9_fzl4nxVBl2rqeRea4XeN7Q8BBC1AMlbHYTUsA41gghS6UYoJbXHmvO21SKEgEKZqm3kGfuw6I5zQ7MEjFPyvRtTt_Xplxt85_7NxG7jroedM2Aqaw0JvF0ENg_Krs5Xbn8HUgljlN1xYt_cN0vDzxnz5LZdDtj3PuIwZ0czWW2tUhWhrx-gN8Phx4nSHCqpKwCixEKFNORMf3icgIPbm-0Wsx2Z7Q5mO0VFr_5-8rHkt7sEyAXIlCJ305_e_5G9A1y_thg</recordid><startdate>20210501</startdate><enddate>20210501</enddate><creator>Harkness, John H.</creator><creator>Gonzalez, Angela E.</creator><creator>Bushana, Priyanka N.</creator><creator>Jorgensen, Emily T.</creator><creator>Hegarty, Deborah M.</creator><creator>Di Nardo, Ariel A.</creator><creator>Prochiantz, Alain</creator><creator>Wisor, Jonathan P.</creator><creator>Aicher, Sue A.</creator><creator>Brown, Travis E.</creator><creator>Sorg, Barbara A.</creator><general>Springer Berlin Heidelberg</general><general>Springer Nature B.V</general><general>Springer Verlag</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>3V.</scope><scope>7RV</scope><scope>7TK</scope><scope>7X7</scope><scope>7XB</scope><scope>88A</scope><scope>88E</scope><scope>88G</scope><scope>8AO</scope><scope>8FE</scope><scope>8FH</scope><scope>8FI</scope><scope>8FJ</scope><scope>8FK</scope><scope>ABUWG</scope><scope>AFKRA</scope><scope>AZQEC</scope><scope>BBNVY</scope><scope>BENPR</scope><scope>BHPHI</scope><scope>CCPQU</scope><scope>DWQXO</scope><scope>FYUFA</scope><scope>GHDGH</scope><scope>GNUQQ</scope><scope>HCIFZ</scope><scope>K9.</scope><scope>KB0</scope><scope>LK8</scope><scope>M0S</scope><scope>M1P</scope><scope>M2M</scope><scope>M7P</scope><scope>NAPCQ</scope><scope>PQEST</scope><scope>PQQKQ</scope><scope>PQUKI</scope><scope>PRINS</scope><scope>PSYQQ</scope><scope>Q9U</scope><scope>7X8</scope><scope>1XC</scope><scope>VOOES</scope><scope>5PM</scope><orcidid>https://orcid.org/0000-0002-4913-4910</orcidid><orcidid>https://orcid.org/0000-0001-7626-5863</orcidid></search><sort><creationdate>20210501</creationdate><title>Diurnal changes in perineuronal nets and parvalbumin neurons in the rat medial prefrontal cortex</title><author>Harkness, John H. ; Gonzalez, Angela E. ; Bushana, Priyanka N. ; Jorgensen, Emily T. ; Hegarty, Deborah M. ; Di Nardo, Ariel A. ; Prochiantz, Alain ; Wisor, Jonathan P. ; Aicher, Sue A. ; Brown, Travis E. ; Sorg, Barbara A.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c574t-1a554eaababaa0c0272031f5c2350dc7e02c345b24435ae711ff52ccce2486fb3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2021</creationdate><topic>8-Hydroxy-2'-Deoxyguanosine</topic><topic>8-Hydroxydeoxyguanosine</topic><topic>Animals</topic><topic>Biomedical and Life Sciences</topic><topic>Biomedicine</topic><topic>Cell Biology</topic><topic>Circadian rhythm</topic><topic>Circadian rhythms</topic><topic>Diurnal</topic><topic>Glutamate receptors</topic><topic>Glutamic acid receptors (ionotropic)</topic><topic>Homeobox</topic><topic>Interneurons</topic><topic>Life Sciences</topic><topic>N-Methyl-D-aspartic acid receptors</topic><topic>Nets</topic><topic>Neurobiology</topic><topic>Neurology</topic><topic>Neurons - metabolism</topic><topic>Neurons and Cognition</topic><topic>Neurosciences</topic><topic>Original Article</topic><topic>Otx2 protein</topic><topic>Oxidative stress</topic><topic>Parvalbumin</topic><topic>Parvalbumins - metabolism</topic><topic>Perineuronal nets</topic><topic>Photovoltaic cells</topic><topic>Prefrontal cortex</topic><topic>Prefrontal Cortex - metabolism</topic><topic>Rats</topic><topic>Sleep</topic><topic>α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Harkness, John H.</creatorcontrib><creatorcontrib>Gonzalez, Angela E.</creatorcontrib><creatorcontrib>Bushana, Priyanka N.</creatorcontrib><creatorcontrib>Jorgensen, Emily T.</creatorcontrib><creatorcontrib>Hegarty, Deborah M.</creatorcontrib><creatorcontrib>Di Nardo, Ariel A.</creatorcontrib><creatorcontrib>Prochiantz, Alain</creatorcontrib><creatorcontrib>Wisor, Jonathan P.</creatorcontrib><creatorcontrib>Aicher, Sue A.</creatorcontrib><creatorcontrib>Brown, Travis E.</creatorcontrib><creatorcontrib>Sorg, Barbara A.</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Nursing & Allied Health Database</collection><collection>Neurosciences Abstracts</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>ProQuest Pharma Collection</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest Central UK/Ireland</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>ProQuest Central</collection><collection>Natural Science Collection</collection><collection>ProQuest One Community College</collection><collection>ProQuest Central Korea</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>ProQuest Biological Science Collection</collection><collection>Health & Medical Collection (Alumni Edition)</collection><collection>Medical Database</collection><collection>ProQuest Psychology</collection><collection>Biological Science Database</collection><collection>Nursing & Allied Health Premium</collection><collection>ProQuest One Academic Eastern Edition (DO NOT USE)</collection><collection>ProQuest One Academic</collection><collection>ProQuest One Academic UKI Edition</collection><collection>ProQuest Central China</collection><collection>ProQuest One Psychology</collection><collection>ProQuest Central Basic</collection><collection>MEDLINE - Academic</collection><collection>Hyper Article en Ligne (HAL)</collection><collection>Hyper Article en Ligne (HAL) (Open Access)</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Brain Structure and Function</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Harkness, John H.</au><au>Gonzalez, Angela E.</au><au>Bushana, Priyanka N.</au><au>Jorgensen, Emily T.</au><au>Hegarty, Deborah M.</au><au>Di Nardo, Ariel A.</au><au>Prochiantz, Alain</au><au>Wisor, Jonathan P.</au><au>Aicher, Sue A.</au><au>Brown, Travis E.</au><au>Sorg, Barbara A.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Diurnal changes in perineuronal nets and parvalbumin neurons in the rat medial prefrontal cortex</atitle><jtitle>Brain Structure and Function</jtitle><stitle>Brain Struct Funct</stitle><addtitle>Brain Struct Funct</addtitle><date>2021-05-01</date><risdate>2021</risdate><volume>226</volume><issue>4</issue><spage>1135</spage><epage>1153</epage><pages>1135-1153</pages><issn>1863-2653</issn><eissn>1863-2661</eissn><eissn>0340-2061</eissn><abstract>Perineuronal nets (PNNs) surrounding fast-spiking, parvalbumin (PV) interneurons provide excitatory:inhibitory balance, which is impaired in several disorders associated with altered diurnal rhythms, yet few studies have examined diurnal rhythms of PNNs or PV cells. We measured the intensity and number of PV cells and PNNs labeled with
Wisteria floribunda
agglutinin (WFA) and also the oxidative stress marker 8-oxo-deoxyguanosine (8-oxo-dG) in rat prelimbic medial prefrontal cortex (mPFC) at Zeitgeber times (ZT) ZT0
(
lights-on, inactive phase), ZT6 (mid-inactive phase), ZT12 (lights-off, active phase), and ZT18 (mid-active phase). Relative to ZT0, the intensities of PNN and PV labeling were increased in the dark (active) phase compared with the light (inactive) phase. The intensity of 8-oxo-dG was decreased from ZT0 at all times (ZT6,12,18). We also measured GAD 65/67 and vGLUT1 puncta apposed to PV cells with and without PNNs. There were more excitatory puncta on PV cells with PNNs at ZT18 vs. ZT6, but no changes in PV cells without PNNs and no changes in inhibitory puncta. Whole-cell slice recordings in fast-spiking (PV) cells with PNNs showed an increased ratio of α-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid receptor:N-methyl-D-aspartate receptor (AMPA: NMDA) at ZT18 vs. ZT6. The number of PV cells and PV/PNN cells containing orthodenticle homeobox 2 (OTX2), which maintains PNNs, showed a strong trend toward an increase from ZT6 to ZT18. Diurnal fluctuations in PNNs and PV cells are expected to alter cortical excitatory:inhibitory balance and provide new insights into treatments for diseases impacted by disturbances in sleep and circadian rhythms.</abstract><cop>Berlin/Heidelberg</cop><pub>Springer Berlin Heidelberg</pub><pmid>33585984</pmid><doi>10.1007/s00429-021-02229-4</doi><tpages>19</tpages><orcidid>https://orcid.org/0000-0002-4913-4910</orcidid><orcidid>https://orcid.org/0000-0001-7626-5863</orcidid><oa>free_for_read</oa></addata></record> |
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subjects | 8-Hydroxy-2'-Deoxyguanosine 8-Hydroxydeoxyguanosine Animals Biomedical and Life Sciences Biomedicine Cell Biology Circadian rhythm Circadian rhythms Diurnal Glutamate receptors Glutamic acid receptors (ionotropic) Homeobox Interneurons Life Sciences N-Methyl-D-aspartic acid receptors Nets Neurobiology Neurology Neurons - metabolism Neurons and Cognition Neurosciences Original Article Otx2 protein Oxidative stress Parvalbumin Parvalbumins - metabolism Perineuronal nets Photovoltaic cells Prefrontal cortex Prefrontal Cortex - metabolism Rats Sleep α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid |
title | Diurnal changes in perineuronal nets and parvalbumin neurons in the rat medial prefrontal cortex |
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