Layer-specific modulation of neocortical dendritic inhibition during active wakefulness
γ-Aminobutyric acid (GABA)ergic inputs are strategically positioned to gate synaptic integration along the dendritic arbor of pyramidal cells. However, their spatiotemporal dynamics during behavior are poorly understood. Using an optical-tagging electrophysiological approach to record and label soma...
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| Veröffentlicht in: | Science (American Association for the Advancement of Science) 2017-03, Vol.355 (6328), p.954-959 |
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| creator | Muñoz, William Tremblay, Robin Levenstein, Daniel Rudy, Bernardo |
| description | γ-Aminobutyric acid (GABA)ergic inputs are strategically positioned to gate synaptic integration along the dendritic arbor of pyramidal cells. However, their spatiotemporal dynamics during behavior are poorly understood. Using an optical-tagging electrophysiological approach to record and label somatostatin-expressing (Sst) interneurons (GABAergic neurons specialized for dendritic inhibition), we discovered a layer-specific modulation of their activity in behaving mice. Sst interneuron subtypes, residing in different cortical layers and innervating complementary laminar domains, exhibited opposite activity changes during transitions to active wakefulness. The relative weight of vasoactive intestinal peptide–expressing (Vip) interneuron–mediated inhibition of distinct Sst interneurons and cholinergic modulation determined their in vivo activity. These results reveal a state-dependent laminar influence of Sst interneuron–mediated inhibition, with implications for the compartmentalized regulation of dendritic signaling in the mammalian neocortex. |
| doi_str_mv | 10.1126/science.aag2599 |
| format | Article |
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However, their spatiotemporal dynamics during behavior are poorly understood. Using an optical-tagging electrophysiological approach to record and label somatostatin-expressing (Sst) interneurons (GABAergic neurons specialized for dendritic inhibition), we discovered a layer-specific modulation of their activity in behaving mice. Sst interneuron subtypes, residing in different cortical layers and innervating complementary laminar domains, exhibited opposite activity changes during transitions to active wakefulness. The relative weight of vasoactive intestinal peptide–expressing (Vip) interneuron–mediated inhibition of distinct Sst interneurons and cholinergic modulation determined their in vivo activity. These results reveal a state-dependent laminar influence of Sst interneuron–mediated inhibition, with implications for the compartmentalized regulation of dendritic signaling in the mammalian neocortex.</description><identifier>ISSN: 0036-8075</identifier><identifier>ISSN: 1095-9203</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.aag2599</identifier><identifier>PMID: 28254942</identifier><language>eng</language><publisher>United States: American Association for the Advancement of Science</publisher><subject>Acetylcholine - metabolism ; Animals ; Attention ; Behavior ; Brain ; Dendrites ; Dendrites - physiology ; Dendritic cells ; Dendritic structure ; Female ; GABAergic Neurons - metabolism ; GABAergic Neurons - physiology ; gamma-Aminobutyric Acid - metabolism ; In vivo methods and tests ; Inhibition ; Interneurons - metabolism ; Interneurons - physiology ; Laminar wakes ; Male ; Mice ; Mice, Knockout ; Modulation ; Neocortex - cytology ; Neocortex - physiology ; Neural Inhibition ; Neurons ; Patching ; Pyramidal Cells - physiology ; Receptors, Muscarinic - metabolism ; Recording ; Rodents ; Somatostatin - metabolism ; Vasoactive Intestinal Peptide - metabolism ; Wakefulness ; Wakefulness - physiology ; γ-Aminobutyric acid receptors</subject><ispartof>Science (American Association for the Advancement of Science), 2017-03, Vol.355 (6328), p.954-959</ispartof><rights>Copyright © 2017 American Association for the Advancement of Science</rights><rights>Copyright © 2017, American Association for the Advancement of Science.</rights><rights>Copyright © 2017, American Association for the Advancement of Science</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c492t-d9b043294e5fe56752925bd6838c7624798666df4d5e17efad2534ffb548718b3</citedby><cites>FETCH-LOGICAL-c492t-d9b043294e5fe56752925bd6838c7624798666df4d5e17efad2534ffb548718b3</cites><orcidid>0000-0002-5507-9145 ; 0000-0003-3434-1201 ; 0000-0003-1367-7136 ; 0000-0002-1354-3472</orcidid></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/24918454$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/24918454$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>314,776,780,799,2871,2872,27901,27902,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/28254942$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Muñoz, William</creatorcontrib><creatorcontrib>Tremblay, Robin</creatorcontrib><creatorcontrib>Levenstein, Daniel</creatorcontrib><creatorcontrib>Rudy, Bernardo</creatorcontrib><title>Layer-specific modulation of neocortical dendritic inhibition during active wakefulness</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>γ-Aminobutyric acid (GABA)ergic inputs are strategically positioned to gate synaptic integration along the dendritic arbor of pyramidal cells. 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These results reveal a state-dependent laminar influence of Sst interneuron–mediated inhibition, with implications for the compartmentalized regulation of dendritic signaling in the mammalian neocortex.</description><subject>Acetylcholine - metabolism</subject><subject>Animals</subject><subject>Attention</subject><subject>Behavior</subject><subject>Brain</subject><subject>Dendrites</subject><subject>Dendrites - physiology</subject><subject>Dendritic cells</subject><subject>Dendritic structure</subject><subject>Female</subject><subject>GABAergic Neurons - metabolism</subject><subject>GABAergic Neurons - physiology</subject><subject>gamma-Aminobutyric Acid - metabolism</subject><subject>In vivo methods and tests</subject><subject>Inhibition</subject><subject>Interneurons - metabolism</subject><subject>Interneurons - physiology</subject><subject>Laminar wakes</subject><subject>Male</subject><subject>Mice</subject><subject>Mice, Knockout</subject><subject>Modulation</subject><subject>Neocortex - cytology</subject><subject>Neocortex - physiology</subject><subject>Neural Inhibition</subject><subject>Neurons</subject><subject>Patching</subject><subject>Pyramidal Cells - physiology</subject><subject>Receptors, Muscarinic - metabolism</subject><subject>Recording</subject><subject>Rodents</subject><subject>Somatostatin - metabolism</subject><subject>Vasoactive Intestinal Peptide - metabolism</subject><subject>Wakefulness</subject><subject>Wakefulness - physiology</subject><subject>γ-Aminobutyric acid receptors</subject><issn>0036-8075</issn><issn>1095-9203</issn><issn>1095-9203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2017</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqN0btrHDEQB2BhEuzzo06VsJDGzdp6jLRSGUxecJAmweWilUaOLnuri7Tr4P8-iu-SgCtXI5hPwww_Ql4xesUYV9fFRZwcXll7x6UxR2TFqJGt4VS8ICtKhWo17eQJOS1lQ2ntGXFMTrjmEgzwFbld2wfMbdmhiyG6Zpv8Mto5pqlJoZkwuZTn6OzYeJx8jvXdxOl7HOKj8UuO011j3Rzvsfllf2BYxglLOScvgx0LXhzqGfn24f3Xm0_t-svHzzfv1q0Dw-fWm4GC4AZQBpSqk9xwOXilhXad4tAZrZTyAbxE1mGwnksBIQwSdMf0IM7I5X7uLqefC5a538bicBxt3X0pPdNGGCqA6WfQDgCY6qDSt0_oJi15qodUpYEazamq6nqvXE6lZAz9LsetzQ89o_2fePpDPP0hnvrjzWHuMmzR__N_86jg9R5sypzy_z4YpkGC-A0mcJbj</recordid><startdate>20170303</startdate><enddate>20170303</enddate><creator>Muñoz, William</creator><creator>Tremblay, Robin</creator><creator>Levenstein, Daniel</creator><creator>Rudy, Bernardo</creator><general>American Association for the Advancement of Science</general><general>The American Association for the Advancement of Science</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>7QF</scope><scope>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QQ</scope><scope>7QR</scope><scope>7SC</scope><scope>7SE</scope><scope>7SN</scope><scope>7SP</scope><scope>7SR</scope><scope>7SS</scope><scope>7T7</scope><scope>7TA</scope><scope>7TB</scope><scope>7TK</scope><scope>7TM</scope><scope>7U5</scope><scope>7U9</scope><scope>8BQ</scope><scope>8FD</scope><scope>C1K</scope><scope>F28</scope><scope>FR3</scope><scope>H8D</scope><scope>H8G</scope><scope>H94</scope><scope>JG9</scope><scope>JQ2</scope><scope>K9.</scope><scope>KR7</scope><scope>L7M</scope><scope>L~C</scope><scope>L~D</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><orcidid>https://orcid.org/0000-0002-5507-9145</orcidid><orcidid>https://orcid.org/0000-0003-3434-1201</orcidid><orcidid>https://orcid.org/0000-0003-1367-7136</orcidid><orcidid>https://orcid.org/0000-0002-1354-3472</orcidid></search><sort><creationdate>20170303</creationdate><title>Layer-specific modulation of neocortical dendritic inhibition during active wakefulness</title><author>Muñoz, William ; Tremblay, Robin ; Levenstein, Daniel ; Rudy, Bernardo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c492t-d9b043294e5fe56752925bd6838c7624798666df4d5e17efad2534ffb548718b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2017</creationdate><topic>Acetylcholine - metabolism</topic><topic>Animals</topic><topic>Attention</topic><topic>Behavior</topic><topic>Brain</topic><topic>Dendrites</topic><topic>Dendrites - physiology</topic><topic>Dendritic cells</topic><topic>Dendritic structure</topic><topic>Female</topic><topic>GABAergic Neurons - metabolism</topic><topic>GABAergic Neurons - physiology</topic><topic>gamma-Aminobutyric Acid - metabolism</topic><topic>In vivo methods and tests</topic><topic>Inhibition</topic><topic>Interneurons - metabolism</topic><topic>Interneurons - physiology</topic><topic>Laminar wakes</topic><topic>Male</topic><topic>Mice</topic><topic>Mice, Knockout</topic><topic>Modulation</topic><topic>Neocortex - cytology</topic><topic>Neocortex - physiology</topic><topic>Neural Inhibition</topic><topic>Neurons</topic><topic>Patching</topic><topic>Pyramidal Cells - physiology</topic><topic>Receptors, Muscarinic - metabolism</topic><topic>Recording</topic><topic>Rodents</topic><topic>Somatostatin - metabolism</topic><topic>Vasoactive Intestinal Peptide - metabolism</topic><topic>Wakefulness</topic><topic>Wakefulness - physiology</topic><topic>γ-Aminobutyric acid receptors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Muñoz, William</creatorcontrib><creatorcontrib>Tremblay, Robin</creatorcontrib><creatorcontrib>Levenstein, Daniel</creatorcontrib><creatorcontrib>Rudy, Bernardo</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Aluminium Industry Abstracts</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Ceramic Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Computer and Information Systems Abstracts</collection><collection>Corrosion Abstracts</collection><collection>Ecology Abstracts</collection><collection>Electronics & Communications Abstracts</collection><collection>Engineered Materials Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Industrial and Applied Microbiology Abstracts (Microbiology A)</collection><collection>Materials Business File</collection><collection>Mechanical & Transportation Engineering Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Solid State and Superconductivity Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>METADEX</collection><collection>Technology Research Database</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ANTE: Abstracts in New Technology & Engineering</collection><collection>Engineering Research Database</collection><collection>Aerospace Database</collection><collection>Copper Technical Reference Library</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>Materials Research Database</collection><collection>ProQuest Computer Science Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Civil Engineering Abstracts</collection><collection>Advanced Technologies Database with Aerospace</collection><collection>Computer and Information Systems Abstracts Academic</collection><collection>Computer and Information Systems Abstracts Professional</collection><collection>Algology Mycology and Protozoology Abstracts (Microbiology C)</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><jtitle>Science (American Association for the Advancement of Science)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Muñoz, William</au><au>Tremblay, Robin</au><au>Levenstein, Daniel</au><au>Rudy, Bernardo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Layer-specific modulation of neocortical dendritic inhibition during active wakefulness</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><addtitle>Science</addtitle><date>2017-03-03</date><risdate>2017</risdate><volume>355</volume><issue>6328</issue><spage>954</spage><epage>959</epage><pages>954-959</pages><issn>0036-8075</issn><issn>1095-9203</issn><eissn>1095-9203</eissn><abstract>γ-Aminobutyric acid (GABA)ergic inputs are strategically positioned to gate synaptic integration along the dendritic arbor of pyramidal cells. However, their spatiotemporal dynamics during behavior are poorly understood. Using an optical-tagging electrophysiological approach to record and label somatostatin-expressing (Sst) interneurons (GABAergic neurons specialized for dendritic inhibition), we discovered a layer-specific modulation of their activity in behaving mice. Sst interneuron subtypes, residing in different cortical layers and innervating complementary laminar domains, exhibited opposite activity changes during transitions to active wakefulness. The relative weight of vasoactive intestinal peptide–expressing (Vip) interneuron–mediated inhibition of distinct Sst interneurons and cholinergic modulation determined their in vivo activity. These results reveal a state-dependent laminar influence of Sst interneuron–mediated inhibition, with implications for the compartmentalized regulation of dendritic signaling in the mammalian neocortex.</abstract><cop>United States</cop><pub>American Association for the Advancement of Science</pub><pmid>28254942</pmid><doi>10.1126/science.aag2599</doi><tpages>6</tpages><orcidid>https://orcid.org/0000-0002-5507-9145</orcidid><orcidid>https://orcid.org/0000-0003-3434-1201</orcidid><orcidid>https://orcid.org/0000-0003-1367-7136</orcidid><orcidid>https://orcid.org/0000-0002-1354-3472</orcidid></addata></record> |
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| source | Jstor Complete Legacy; MEDLINE; Science Magazine |
| subjects | Acetylcholine - metabolism Animals Attention Behavior Brain Dendrites Dendrites - physiology Dendritic cells Dendritic structure Female GABAergic Neurons - metabolism GABAergic Neurons - physiology gamma-Aminobutyric Acid - metabolism In vivo methods and tests Inhibition Interneurons - metabolism Interneurons - physiology Laminar wakes Male Mice Mice, Knockout Modulation Neocortex - cytology Neocortex - physiology Neural Inhibition Neurons Patching Pyramidal Cells - physiology Receptors, Muscarinic - metabolism Recording Rodents Somatostatin - metabolism Vasoactive Intestinal Peptide - metabolism Wakefulness Wakefulness - physiology γ-Aminobutyric acid receptors |
| title | Layer-specific modulation of neocortical dendritic inhibition during active wakefulness |
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