A critical time window for dopamine actions on the structural plasticity of dendritic spines
Animal behaviors are reinforced by subsequent rewards following within a narrow time window. Such reward signals are primarily coded by dopamine, which modulates the synaptic connections of medium spiny neurons in the striatum. The mechanisms of the narrow timing detection, however, remain unknown....
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Veröffentlicht in: | Science (American Association for the Advancement of Science) 2014-09, Vol.345 (6204), p.1616-1620 |
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creator | Yagishita, Sho Hayashi-Takagi, Akiko Ellis-Davies, Graham C.R. Urakubo, Hidetoshi Ishii, Shin Kasai, Haruo |
description | Animal behaviors are reinforced by subsequent rewards following within a narrow time window. Such reward signals are primarily coded by dopamine, which modulates the synaptic connections of medium spiny neurons in the striatum. The mechanisms of the narrow timing detection, however, remain unknown. Here, we optically stimulated dopaminergic and glutamatergic inputs separately and found that dopamine promoted spine enlargement only during a narrow time window (0.3 to 2 seconds) after the glutamatergic inputs. The temporal contingency was detected by rapid regulation of adenosine 3′,5′-cyclic monophosphate in thin distal dendrites, in which protein-kinase A was activated only within the time window because of a high phosphodiesterase activity. Thus, we describe a molecular basis of reinforcement plasticity at the level of single dendritic spines. |
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Such reward signals are primarily coded by dopamine, which modulates the synaptic connections of medium spiny neurons in the striatum. The mechanisms of the narrow timing detection, however, remain unknown. Here, we optically stimulated dopaminergic and glutamatergic inputs separately and found that dopamine promoted spine enlargement only during a narrow time window (0.3 to 2 seconds) after the glutamatergic inputs. The temporal contingency was detected by rapid regulation of adenosine 3′,5′-cyclic monophosphate in thin distal dendrites, in which protein-kinase A was activated only within the time window because of a high phosphodiesterase activity. Thus, we describe a molecular basis of reinforcement plasticity at the level of single dendritic spines.</description><identifier>ISSN: 0036-8075</identifier><identifier>EISSN: 1095-9203</identifier><identifier>DOI: 10.1126/science.1255514</identifier><identifier>PMID: 25258080</identifier><identifier>CODEN: SCIEAS</identifier><language>eng</language><publisher>United States: American Association for the Advancement of Science</publisher><subject>Animal behavior ; Animals ; Cyclic AMP - metabolism ; Cyclic AMP-Dependent Protein Kinases - metabolism ; dendrites ; Dendritic Spines - drug effects ; Dendritic Spines - physiology ; Dendritic structure ; Dopamine ; Dopamine - pharmacology ; Dopamine Plasma Membrane Transport Proteins - genetics ; Dopamine Plasma Membrane Transport Proteins - metabolism ; drug abuse ; Drug Addiction ; Electrical Synapses - drug effects ; Electrical Synapses - physiology ; Enlargement ; Glutamic Acid - physiology ; learning ; Learning - drug effects ; Learning - physiology ; Mental Disorders ; Mice ; Neurobiology ; Neuronal Plasticity - drug effects ; neurotransmitters ; Phosphoric Diester Hydrolases - metabolism ; Plasticity ; Reinforcement ; Reward ; Schizophrenia ; Spine ; synapse ; Time Factors ; Time measurements ; Windows (intervals)</subject><ispartof>Science (American Association for the Advancement of Science), 2014-09, Vol.345 (6204), p.1616-1620</ispartof><rights>Copyright © 2014 American Association for the Advancement of Science</rights><rights>Copyright © 2014, American Association for the Advancement of Science.</rights><rights>Copyright © 2014, American Association for the Advancement of Science</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c579t-d9f61bf4e78ed6e6ef17f85d6561a318b5e4df974f7ab56ab43d01e1836fed733</citedby><cites>FETCH-LOGICAL-c579t-d9f61bf4e78ed6e6ef17f85d6561a318b5e4df974f7ab56ab43d01e1836fed733</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/24917704$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/24917704$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,776,780,799,881,2871,2872,27901,27902,57992,58225</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25258080$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Yagishita, Sho</creatorcontrib><creatorcontrib>Hayashi-Takagi, Akiko</creatorcontrib><creatorcontrib>Ellis-Davies, Graham C.R.</creatorcontrib><creatorcontrib>Urakubo, Hidetoshi</creatorcontrib><creatorcontrib>Ishii, Shin</creatorcontrib><creatorcontrib>Kasai, Haruo</creatorcontrib><title>A critical time window for dopamine actions on the structural plasticity of dendritic spines</title><title>Science (American Association for the Advancement of Science)</title><addtitle>Science</addtitle><description>Animal behaviors are reinforced by subsequent rewards following within a narrow time window. Such reward signals are primarily coded by dopamine, which modulates the synaptic connections of medium spiny neurons in the striatum. The mechanisms of the narrow timing detection, however, remain unknown. Here, we optically stimulated dopaminergic and glutamatergic inputs separately and found that dopamine promoted spine enlargement only during a narrow time window (0.3 to 2 seconds) after the glutamatergic inputs. The temporal contingency was detected by rapid regulation of adenosine 3′,5′-cyclic monophosphate in thin distal dendrites, in which protein-kinase A was activated only within the time window because of a high phosphodiesterase activity. Thus, we describe a molecular basis of reinforcement plasticity at the level of single dendritic spines.</description><subject>Animal behavior</subject><subject>Animals</subject><subject>Cyclic AMP - metabolism</subject><subject>Cyclic AMP-Dependent Protein Kinases - metabolism</subject><subject>dendrites</subject><subject>Dendritic Spines - drug effects</subject><subject>Dendritic Spines - physiology</subject><subject>Dendritic structure</subject><subject>Dopamine</subject><subject>Dopamine - pharmacology</subject><subject>Dopamine Plasma Membrane Transport Proteins - genetics</subject><subject>Dopamine Plasma Membrane Transport Proteins - metabolism</subject><subject>drug abuse</subject><subject>Drug Addiction</subject><subject>Electrical Synapses - drug effects</subject><subject>Electrical Synapses - physiology</subject><subject>Enlargement</subject><subject>Glutamic Acid - physiology</subject><subject>learning</subject><subject>Learning - drug effects</subject><subject>Learning - physiology</subject><subject>Mental Disorders</subject><subject>Mice</subject><subject>Neurobiology</subject><subject>Neuronal Plasticity - drug effects</subject><subject>neurotransmitters</subject><subject>Phosphoric Diester Hydrolases - metabolism</subject><subject>Plasticity</subject><subject>Reinforcement</subject><subject>Reward</subject><subject>Schizophrenia</subject><subject>Spine</subject><subject>synapse</subject><subject>Time Factors</subject><subject>Time measurements</subject><subject>Windows (intervals)</subject><issn>0036-8075</issn><issn>1095-9203</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFks1vFSEUxYnR2Gd17UpD4sbNtDAMMGxMmsavpIkb3ZkQBi6Wlxl4AmPT_16e71k_Nl2xuL9zwj33IPSckjNKe3FebIBo4Yz2nHM6PEAbShTvVE_YQ7QhhIluJJKfoCelbAlpM8Ueo5Oe93wkI9mgrxfY5lCDNTOuYQF8E6JLN9injF3amSVEwMbWkGLBKeJ6DbjUvNq65ibZzaY0cai3OHnsILpfZrjsmq48RY-8mQs8O76n6Mu7t58vP3RXn95_vLy46iyXqnZOeUEnP4AcwQkQ4Kn0I3eCC2oYHScOg_NKDl6aiQszDcwRCnRkwoOTjJ2iNwff3Tot4CzE2j6ndzksJt_qZIL-dxLDtf6Wfuih77mUohm8Phrk9H2FUvUSioV5NhHSWnTfomNStsjvRakizVVycr8r5UK0c1FFG_rqP3Sb1hxbaHuKD0pRvt_z_EDZnErJ4O9WpETv-6CPfdDHPjTFy7-TueN_F6ABLw7AttSU_8wHRaUkA_sJCoK9Aw</recordid><startdate>20140926</startdate><enddate>20140926</enddate><creator>Yagishita, Sho</creator><creator>Hayashi-Takagi, Akiko</creator><creator>Ellis-Davies, Graham C.R.</creator><creator>Urakubo, Hidetoshi</creator><creator>Ishii, Shin</creator><creator>Kasai, Haruo</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><scope>7S9</scope><scope>L.6</scope><scope>5PM</scope></search><sort><creationdate>20140926</creationdate><title>A critical time window for dopamine actions on the structural plasticity of dendritic spines</title><author>Yagishita, Sho ; Hayashi-Takagi, Akiko ; Ellis-Davies, Graham C.R. ; Urakubo, Hidetoshi ; Ishii, Shin ; Kasai, Haruo</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c579t-d9f61bf4e78ed6e6ef17f85d6561a318b5e4df974f7ab56ab43d01e1836fed733</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animal behavior</topic><topic>Animals</topic><topic>Cyclic AMP - 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Academic</collection><collection>AGRICOLA</collection><collection>AGRICOLA - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Science (American Association for the Advancement of Science)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Yagishita, Sho</au><au>Hayashi-Takagi, Akiko</au><au>Ellis-Davies, Graham C.R.</au><au>Urakubo, Hidetoshi</au><au>Ishii, Shin</au><au>Kasai, Haruo</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>A critical time window for dopamine actions on the structural plasticity of dendritic spines</atitle><jtitle>Science (American Association for the Advancement of Science)</jtitle><addtitle>Science</addtitle><date>2014-09-26</date><risdate>2014</risdate><volume>345</volume><issue>6204</issue><spage>1616</spage><epage>1620</epage><pages>1616-1620</pages><issn>0036-8075</issn><eissn>1095-9203</eissn><coden>SCIEAS</coden><abstract>Animal behaviors are reinforced by subsequent rewards following within a narrow time window. 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subjects | Animal behavior Animals Cyclic AMP - metabolism Cyclic AMP-Dependent Protein Kinases - metabolism dendrites Dendritic Spines - drug effects Dendritic Spines - physiology Dendritic structure Dopamine Dopamine - pharmacology Dopamine Plasma Membrane Transport Proteins - genetics Dopamine Plasma Membrane Transport Proteins - metabolism drug abuse Drug Addiction Electrical Synapses - drug effects Electrical Synapses - physiology Enlargement Glutamic Acid - physiology learning Learning - drug effects Learning - physiology Mental Disorders Mice Neurobiology Neuronal Plasticity - drug effects neurotransmitters Phosphoric Diester Hydrolases - metabolism Plasticity Reinforcement Reward Schizophrenia Spine synapse Time Factors Time measurements Windows (intervals) |
title | A critical time window for dopamine actions on the structural plasticity of dendritic spines |
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