Developmental changes in structural and functional properties of hippocampal AMPARs parallels the emergence of deliberative spatial navigation in juvenile rats
The neural mechanisms that support the late postnatal development of spatial navigation are currently unknown. We investigated this in rats and found that an increase in the duration of AMPAR-mediated synaptic responses in the hippocampus was related to the emergence of spatial navigation. More spec...
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Veröffentlicht in: | The Journal of neuroscience 2013-07, Vol.33 (30), p.12218-12228 |
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creator | Blair, Margaret G Nguyen, Nhu N-Q Albani, Sarah H L'Etoile, Matthew M Andrawis, Marina M Owen, Leanna M Oliveira, Rodrigo F Johnson, Matthew W Purvis, Dianna L Sanders, Erin M Stoneham, Emily T Xu, Huaying Dumas, Theodore C |
description | The neural mechanisms that support the late postnatal development of spatial navigation are currently unknown. We investigated this in rats and found that an increase in the duration of AMPAR-mediated synaptic responses in the hippocampus was related to the emergence of spatial navigation. More specifically, spontaneous alternation rate, a behavioral indicator of hippocampal integrity, increased at the end of the third postnatal week in association with increases in AMPAR response duration at SC-CA1 synapses and synaptically driven postsynaptic discharge of CA1 pyramidal neurons. Pharmacological prolongation of glutamatergic synaptic transmission in juveniles increased the spontaneous alternation rate and CA1 postsynaptic discharge and reduced the threshold for the induction of activity-dependent synaptic plasticity at SC-CA1 synapses. A decrease in GluA1 and increases in GluA3 subunit and transmembrane AMPAR regulatory protein (TARP) expression at the end of the third postnatal week provide a molecular explanation for the increase in AMPAR response duration and reduced efficacy of AMPAR modulators with increasing age. A shift in the composition of AMPARs and increased association with AMPAR protein complex accessory proteins at the end of the third postnatal week likely "turns on" the hippocampus by increasing AMPAR response duration and postsynaptic excitability and reducing the threshold for activity-dependent synaptic potentiation. |
doi_str_mv | 10.1523/JNEUROSCI.4827-12.2013 |
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We investigated this in rats and found that an increase in the duration of AMPAR-mediated synaptic responses in the hippocampus was related to the emergence of spatial navigation. More specifically, spontaneous alternation rate, a behavioral indicator of hippocampal integrity, increased at the end of the third postnatal week in association with increases in AMPAR response duration at SC-CA1 synapses and synaptically driven postsynaptic discharge of CA1 pyramidal neurons. Pharmacological prolongation of glutamatergic synaptic transmission in juveniles increased the spontaneous alternation rate and CA1 postsynaptic discharge and reduced the threshold for the induction of activity-dependent synaptic plasticity at SC-CA1 synapses. A decrease in GluA1 and increases in GluA3 subunit and transmembrane AMPAR regulatory protein (TARP) expression at the end of the third postnatal week provide a molecular explanation for the increase in AMPAR response duration and reduced efficacy of AMPAR modulators with increasing age. A shift in the composition of AMPARs and increased association with AMPAR protein complex accessory proteins at the end of the third postnatal week likely "turns on" the hippocampus by increasing AMPAR response duration and postsynaptic excitability and reducing the threshold for activity-dependent synaptic potentiation.</description><identifier>ISSN: 0270-6474</identifier><identifier>ISSN: 1529-2401</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.4827-12.2013</identifier><identifier>PMID: 23884930</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Age Factors ; Animals ; CA1 Region, Hippocampal - growth & development ; CA1 Region, Hippocampal - physiology ; Calcium Channels - physiology ; Electrophysiology ; Evoked Potentials - physiology ; Excitatory Postsynaptic Potentials - physiology ; Female ; Male ; Maze Learning - physiology ; Neuronal Plasticity - physiology ; Organ Culture Techniques ; Oxazines - pharmacology ; Rats ; Rats, Long-Evans ; Receptors, AMPA - agonists ; Receptors, AMPA - physiology ; Space Perception - physiology ; Synapses - physiology</subject><ispartof>The Journal of neuroscience, 2013-07, Vol.33 (30), p.12218-12228</ispartof><rights>Copyright © 2013 the authors 0270-6474/13/3312218-11$15.00/0 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c566t-590771f3df4033f0bfd903c2dee6562b76215b36c09066b8c76f6c575586c8aa3</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4471169/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC4471169/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,723,776,780,881,27903,27904,53770,53772</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/23884930$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Blair, Margaret G</creatorcontrib><creatorcontrib>Nguyen, Nhu N-Q</creatorcontrib><creatorcontrib>Albani, Sarah H</creatorcontrib><creatorcontrib>L'Etoile, Matthew M</creatorcontrib><creatorcontrib>Andrawis, Marina M</creatorcontrib><creatorcontrib>Owen, Leanna M</creatorcontrib><creatorcontrib>Oliveira, Rodrigo F</creatorcontrib><creatorcontrib>Johnson, Matthew W</creatorcontrib><creatorcontrib>Purvis, Dianna L</creatorcontrib><creatorcontrib>Sanders, Erin M</creatorcontrib><creatorcontrib>Stoneham, Emily T</creatorcontrib><creatorcontrib>Xu, Huaying</creatorcontrib><creatorcontrib>Dumas, Theodore C</creatorcontrib><title>Developmental changes in structural and functional properties of hippocampal AMPARs parallels the emergence of deliberative spatial navigation in juvenile rats</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>The neural mechanisms that support the late postnatal development of spatial navigation are currently unknown. We investigated this in rats and found that an increase in the duration of AMPAR-mediated synaptic responses in the hippocampus was related to the emergence of spatial navigation. More specifically, spontaneous alternation rate, a behavioral indicator of hippocampal integrity, increased at the end of the third postnatal week in association with increases in AMPAR response duration at SC-CA1 synapses and synaptically driven postsynaptic discharge of CA1 pyramidal neurons. Pharmacological prolongation of glutamatergic synaptic transmission in juveniles increased the spontaneous alternation rate and CA1 postsynaptic discharge and reduced the threshold for the induction of activity-dependent synaptic plasticity at SC-CA1 synapses. A decrease in GluA1 and increases in GluA3 subunit and transmembrane AMPAR regulatory protein (TARP) expression at the end of the third postnatal week provide a molecular explanation for the increase in AMPAR response duration and reduced efficacy of AMPAR modulators with increasing age. A shift in the composition of AMPARs and increased association with AMPAR protein complex accessory proteins at the end of the third postnatal week likely "turns on" the hippocampus by increasing AMPAR response duration and postsynaptic excitability and reducing the threshold for activity-dependent synaptic potentiation.</description><subject>Age Factors</subject><subject>Animals</subject><subject>CA1 Region, Hippocampal - growth & development</subject><subject>CA1 Region, Hippocampal - physiology</subject><subject>Calcium Channels - physiology</subject><subject>Electrophysiology</subject><subject>Evoked Potentials - physiology</subject><subject>Excitatory Postsynaptic Potentials - physiology</subject><subject>Female</subject><subject>Male</subject><subject>Maze Learning - physiology</subject><subject>Neuronal Plasticity - physiology</subject><subject>Organ Culture Techniques</subject><subject>Oxazines - pharmacology</subject><subject>Rats</subject><subject>Rats, Long-Evans</subject><subject>Receptors, AMPA - agonists</subject><subject>Receptors, AMPA - physiology</subject><subject>Space Perception - physiology</subject><subject>Synapses - physiology</subject><issn>0270-6474</issn><issn>1529-2401</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFks1u1DAUhS0EokPhFSov2WTwT2wnG6TRUKCoUFTo2nKcmxlXiWPsJBJPw6viqGUEK1ZX9v3Osa99ELqgZEsF428-fbm8u735tr_alhVTBWVbRih_gja5WxesJPQp2hCmSCFLVZ6hFyndE0IUoeo5OmO8qsqakw369Q4W6McwgJ9Mj-3R-AMk7DxOU5ztNMe8a3yLu9nbyY0-L0McA8TJZW7s8NGFMFozhNzZff66u004mKzqoU94OgKGAeIBvIWVbqF3DUQzuQVwCrlmmTeLO5jVfT34fl7Aux5wptJL9KwzfYJXj_Uc3b2__L7_WFzffLja764LK6ScClETpWjH264knHek6dqacMtaACkka5RkVDRcWlITKZvKKtlJK5QQlbSVMfwcvX3wDXMzQGvzc-QZdIhuMPGnHo3T_3a8O-rDuOiyVJTKOhu8fjSI448Z0qQHlyz0vfEwzklTIahkqmb8_2hJeWaFEBmVD6iNY0oRutONKNFrEPQpCHoNgqZMr0HIwou_5znJ_vw8_w3C8LSO</recordid><startdate>20130724</startdate><enddate>20130724</enddate><creator>Blair, Margaret G</creator><creator>Nguyen, Nhu N-Q</creator><creator>Albani, Sarah H</creator><creator>L'Etoile, Matthew M</creator><creator>Andrawis, Marina M</creator><creator>Owen, Leanna M</creator><creator>Oliveira, Rodrigo F</creator><creator>Johnson, Matthew W</creator><creator>Purvis, Dianna L</creator><creator>Sanders, Erin M</creator><creator>Stoneham, Emily T</creator><creator>Xu, Huaying</creator><creator>Dumas, Theodore C</creator><general>Society for Neuroscience</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>7X8</scope><scope>7QG</scope><scope>7TK</scope><scope>5PM</scope></search><sort><creationdate>20130724</creationdate><title>Developmental changes in structural and functional properties of hippocampal AMPARs parallels the emergence of deliberative spatial navigation in juvenile rats</title><author>Blair, Margaret G ; 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We investigated this in rats and found that an increase in the duration of AMPAR-mediated synaptic responses in the hippocampus was related to the emergence of spatial navigation. More specifically, spontaneous alternation rate, a behavioral indicator of hippocampal integrity, increased at the end of the third postnatal week in association with increases in AMPAR response duration at SC-CA1 synapses and synaptically driven postsynaptic discharge of CA1 pyramidal neurons. Pharmacological prolongation of glutamatergic synaptic transmission in juveniles increased the spontaneous alternation rate and CA1 postsynaptic discharge and reduced the threshold for the induction of activity-dependent synaptic plasticity at SC-CA1 synapses. A decrease in GluA1 and increases in GluA3 subunit and transmembrane AMPAR regulatory protein (TARP) expression at the end of the third postnatal week provide a molecular explanation for the increase in AMPAR response duration and reduced efficacy of AMPAR modulators with increasing age. A shift in the composition of AMPARs and increased association with AMPAR protein complex accessory proteins at the end of the third postnatal week likely "turns on" the hippocampus by increasing AMPAR response duration and postsynaptic excitability and reducing the threshold for activity-dependent synaptic potentiation.</abstract><cop>United States</cop><pub>Society for Neuroscience</pub><pmid>23884930</pmid><doi>10.1523/JNEUROSCI.4827-12.2013</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Age Factors Animals CA1 Region, Hippocampal - growth & development CA1 Region, Hippocampal - physiology Calcium Channels - physiology Electrophysiology Evoked Potentials - physiology Excitatory Postsynaptic Potentials - physiology Female Male Maze Learning - physiology Neuronal Plasticity - physiology Organ Culture Techniques Oxazines - pharmacology Rats Rats, Long-Evans Receptors, AMPA - agonists Receptors, AMPA - physiology Space Perception - physiology Synapses - physiology |
title | Developmental changes in structural and functional properties of hippocampal AMPARs parallels the emergence of deliberative spatial navigation in juvenile rats |
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