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Presynaptic 5-HT1B receptor-mediated synaptic suppression to the subplate neurons in the somatosensory cortex of neonatal rats
Serotonin (5-HT), the target of numerous psychiatric medicines, plays important roles in neural development. In this study we examined the direct effects of 5-HT on the physiological properties of neurons in the cortical subplate, a structure that develops early in life and is important for the matu...
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Published in: | Neuropharmacology 2014-02, Vol.77, p.81-89 |
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description | Serotonin (5-HT), the target of numerous psychiatric medicines, plays important roles in neural development. In this study we examined the direct effects of 5-HT on the physiological properties of neurons in the cortical subplate, a structure that develops early in life and is important for the maturation of cortical circuits. Acute brain slices were prepared from neonatal rats and the intrinsic and synaptic properties of subplate neurons (SPns) were evaluated before and after 5-HT bath-application. In all concentrations tested, 5-HT did not affect the intrinsic properties of SPns. However, thalamus-evoked excitatory postsynaptic currents (eEPSCs) in SPn were significantly suppressed by 5-HT in a dose-dependent manner. Because 5-HT did not affect AMPA- or NMDA-induced currents, it is unlikely that a 5-HT-mediated postsynaptic mechanism reduced EPSCs. Subsequent to 5-HT application, increased paired-pulse ratios and decreased MK-801 blocking rates were noted, indicating the presence of a presynaptic 5-HT receptor-mediated suppressive effect in the thalamocortical afferent (TCA)-SPn synapses. To elucidate the type(s) of 5-HT receptor involved in this process, various 5-HT receptor agonists and antagonists were tested. CP93129, a 5-HT1B receptor agonist, mimicked the effect of 5-HT and in the contrary, the 5-HT1B receptor antagonist SB224289 prevented 5-HT-mediated synaptic suppression. Our cumulative data demonstrated the presynaptic 5-HT1B receptor-mediated suppressive effect on the excitatory synapses between TCAs and SPns in the somatosensory cortex of neonatal rats. Early exposure to drugs that might interrupt 5-HT homeostasis should be considered.
[Display omitted]
•Serotonin suppresses the synaptic currents in subplate neurons of neonatal rats.•5-HT does not affect the intrinsic properties and AMPA- or NMDA-EPSCs in SPns.•Release of glutamate from TCAs onto SPns is inhibited by 5-HT.•5-HT1B agonist mimics the suppressive effect of 5-HT on SPn EPSCs.•5-HT1B antagonist prevents 5-HT-mediated synaptic suppression. |
doi_str_mv | 10.1016/j.neuropharm.2013.08.040 |
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[Display omitted]
•Serotonin suppresses the synaptic currents in subplate neurons of neonatal rats.•5-HT does not affect the intrinsic properties and AMPA- or NMDA-EPSCs in SPns.•Release of glutamate from TCAs onto SPns is inhibited by 5-HT.•5-HT1B agonist mimics the suppressive effect of 5-HT on SPn EPSCs.•5-HT1B antagonist prevents 5-HT-mediated synaptic suppression.</description><identifier>ISSN: 0028-3908</identifier><identifier>EISSN: 1873-7064</identifier><identifier>DOI: 10.1016/j.neuropharm.2013.08.040</identifier><identifier>PMID: 24055501</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Animals ; Animals, Newborn ; Antagonists ; Brain development ; Dose-Response Relationship, Drug ; Excitatory Postsynaptic Potentials - drug effects ; Excitatory Postsynaptic Potentials - physiology ; Male ; Neurons - drug effects ; Neurons - metabolism ; Piperidones - pharmacology ; Pyridines - pharmacology ; Pyrroles - pharmacology ; Rats ; Rats, Wistar ; Receptor, Serotonin, 5-HT1B - metabolism ; Serotonin - pharmacology ; Serotonin Antagonists - pharmacology ; Serotonin receptor ; Serotonin Receptor Agonists - pharmacology ; Somatosensory Cortex - drug effects ; Somatosensory Cortex - metabolism ; Spiro Compounds - pharmacology ; Synaptic transmission ; Thalamocortical afferent</subject><ispartof>Neuropharmacology, 2014-02, Vol.77, p.81-89</ispartof><rights>2013 Elsevier Ltd</rights><rights>Copyright © 2013 Elsevier Ltd. All rights reserved.</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c473t-dfd4f27eaabf40004ab6aa4e550ff7e0fb20607f121f310a9eb8e931b023bd653</citedby><cites>FETCH-LOGICAL-c473t-dfd4f27eaabf40004ab6aa4e550ff7e0fb20607f121f310a9eb8e931b023bd653</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>314,780,784,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24055501$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Liao, Chun-Chieh</creatorcontrib><creatorcontrib>Lee, Li-Jen</creatorcontrib><title>Presynaptic 5-HT1B receptor-mediated synaptic suppression to the subplate neurons in the somatosensory cortex of neonatal rats</title><title>Neuropharmacology</title><addtitle>Neuropharmacology</addtitle><description>Serotonin (5-HT), the target of numerous psychiatric medicines, plays important roles in neural development. In this study we examined the direct effects of 5-HT on the physiological properties of neurons in the cortical subplate, a structure that develops early in life and is important for the maturation of cortical circuits. Acute brain slices were prepared from neonatal rats and the intrinsic and synaptic properties of subplate neurons (SPns) were evaluated before and after 5-HT bath-application. In all concentrations tested, 5-HT did not affect the intrinsic properties of SPns. However, thalamus-evoked excitatory postsynaptic currents (eEPSCs) in SPn were significantly suppressed by 5-HT in a dose-dependent manner. Because 5-HT did not affect AMPA- or NMDA-induced currents, it is unlikely that a 5-HT-mediated postsynaptic mechanism reduced EPSCs. Subsequent to 5-HT application, increased paired-pulse ratios and decreased MK-801 blocking rates were noted, indicating the presence of a presynaptic 5-HT receptor-mediated suppressive effect in the thalamocortical afferent (TCA)-SPn synapses. To elucidate the type(s) of 5-HT receptor involved in this process, various 5-HT receptor agonists and antagonists were tested. CP93129, a 5-HT1B receptor agonist, mimicked the effect of 5-HT and in the contrary, the 5-HT1B receptor antagonist SB224289 prevented 5-HT-mediated synaptic suppression. Our cumulative data demonstrated the presynaptic 5-HT1B receptor-mediated suppressive effect on the excitatory synapses between TCAs and SPns in the somatosensory cortex of neonatal rats. Early exposure to drugs that might interrupt 5-HT homeostasis should be considered.
[Display omitted]
•Serotonin suppresses the synaptic currents in subplate neurons of neonatal rats.•5-HT does not affect the intrinsic properties and AMPA- or NMDA-EPSCs in SPns.•Release of glutamate from TCAs onto SPns is inhibited by 5-HT.•5-HT1B agonist mimics the suppressive effect of 5-HT on SPn EPSCs.•5-HT1B antagonist prevents 5-HT-mediated synaptic suppression.</description><subject>Animals</subject><subject>Animals, Newborn</subject><subject>Antagonists</subject><subject>Brain development</subject><subject>Dose-Response Relationship, Drug</subject><subject>Excitatory Postsynaptic Potentials - drug effects</subject><subject>Excitatory Postsynaptic Potentials - physiology</subject><subject>Male</subject><subject>Neurons - drug effects</subject><subject>Neurons - metabolism</subject><subject>Piperidones - pharmacology</subject><subject>Pyridines - pharmacology</subject><subject>Pyrroles - pharmacology</subject><subject>Rats</subject><subject>Rats, Wistar</subject><subject>Receptor, Serotonin, 5-HT1B - metabolism</subject><subject>Serotonin - pharmacology</subject><subject>Serotonin Antagonists - pharmacology</subject><subject>Serotonin receptor</subject><subject>Serotonin Receptor Agonists - pharmacology</subject><subject>Somatosensory Cortex - drug effects</subject><subject>Somatosensory Cortex - metabolism</subject><subject>Spiro Compounds - pharmacology</subject><subject>Synaptic transmission</subject><subject>Thalamocortical afferent</subject><issn>0028-3908</issn><issn>1873-7064</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><recordid>eNqFkUtP9CAUhonR6Hj5C4alm9YDpS2zVOMtMdGFrgltD5FJW_oBNc7G3y7j-OnSFcnJ83IuDyGUQc6AVeerfMTZu-lV-yHnwIocZA4CdsiCybrIaqjELlkAcJkVS5AH5DCEFQAIyeQ-OeACyrIEtiAfTx7DetRTtC0ts7tndkk9tjhF57MBO6sjdvSHCPM0pUCwbqTR0fiKqdRMfaLo10hjoHbc1t2gows4BufXtHU-4jt1JmFu1FH31OsYjsme0X3Ak-_3iLzcXD9f3WUPj7f3VxcPWSvqImad6YThNWrdGLFZQzeV1gLTDsbUCKbhUEFtGGemYKCX2EhcFqwBXjRdVRZH5Gz77-TdvxlDVIMNLfa9TuPMQbESQALUNf8bFdWSpytzllC5RVvvQvBo1OTtoP1aMVAbUWqlfkWpjSgFUiVRKXr63WVu0pl_gv_NJOByC2A6y5tFr0JrcWyTkuQnqs7Zv7t8AgZErJI</recordid><startdate>20140201</startdate><enddate>20140201</enddate><creator>Liao, Chun-Chieh</creator><creator>Lee, Li-Jen</creator><general>Elsevier Ltd</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>7TK</scope></search><sort><creationdate>20140201</creationdate><title>Presynaptic 5-HT1B receptor-mediated synaptic suppression to the subplate neurons in the somatosensory cortex of neonatal rats</title><author>Liao, Chun-Chieh ; Lee, Li-Jen</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c473t-dfd4f27eaabf40004ab6aa4e550ff7e0fb20607f121f310a9eb8e931b023bd653</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Animals</topic><topic>Animals, Newborn</topic><topic>Antagonists</topic><topic>Brain development</topic><topic>Dose-Response Relationship, Drug</topic><topic>Excitatory Postsynaptic Potentials - drug effects</topic><topic>Excitatory Postsynaptic Potentials - physiology</topic><topic>Male</topic><topic>Neurons - drug effects</topic><topic>Neurons - metabolism</topic><topic>Piperidones - pharmacology</topic><topic>Pyridines - pharmacology</topic><topic>Pyrroles - pharmacology</topic><topic>Rats</topic><topic>Rats, Wistar</topic><topic>Receptor, Serotonin, 5-HT1B - metabolism</topic><topic>Serotonin - pharmacology</topic><topic>Serotonin Antagonists - pharmacology</topic><topic>Serotonin receptor</topic><topic>Serotonin Receptor Agonists - pharmacology</topic><topic>Somatosensory Cortex - drug effects</topic><topic>Somatosensory Cortex - metabolism</topic><topic>Spiro Compounds - pharmacology</topic><topic>Synaptic transmission</topic><topic>Thalamocortical afferent</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Liao, Chun-Chieh</creatorcontrib><creatorcontrib>Lee, Li-Jen</creatorcontrib><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>Neurosciences Abstracts</collection><jtitle>Neuropharmacology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Liao, Chun-Chieh</au><au>Lee, Li-Jen</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Presynaptic 5-HT1B receptor-mediated synaptic suppression to the subplate neurons in the somatosensory cortex of neonatal rats</atitle><jtitle>Neuropharmacology</jtitle><addtitle>Neuropharmacology</addtitle><date>2014-02-01</date><risdate>2014</risdate><volume>77</volume><spage>81</spage><epage>89</epage><pages>81-89</pages><issn>0028-3908</issn><eissn>1873-7064</eissn><abstract>Serotonin (5-HT), the target of numerous psychiatric medicines, plays important roles in neural development. In this study we examined the direct effects of 5-HT on the physiological properties of neurons in the cortical subplate, a structure that develops early in life and is important for the maturation of cortical circuits. Acute brain slices were prepared from neonatal rats and the intrinsic and synaptic properties of subplate neurons (SPns) were evaluated before and after 5-HT bath-application. In all concentrations tested, 5-HT did not affect the intrinsic properties of SPns. However, thalamus-evoked excitatory postsynaptic currents (eEPSCs) in SPn were significantly suppressed by 5-HT in a dose-dependent manner. Because 5-HT did not affect AMPA- or NMDA-induced currents, it is unlikely that a 5-HT-mediated postsynaptic mechanism reduced EPSCs. Subsequent to 5-HT application, increased paired-pulse ratios and decreased MK-801 blocking rates were noted, indicating the presence of a presynaptic 5-HT receptor-mediated suppressive effect in the thalamocortical afferent (TCA)-SPn synapses. To elucidate the type(s) of 5-HT receptor involved in this process, various 5-HT receptor agonists and antagonists were tested. CP93129, a 5-HT1B receptor agonist, mimicked the effect of 5-HT and in the contrary, the 5-HT1B receptor antagonist SB224289 prevented 5-HT-mediated synaptic suppression. Our cumulative data demonstrated the presynaptic 5-HT1B receptor-mediated suppressive effect on the excitatory synapses between TCAs and SPns in the somatosensory cortex of neonatal rats. Early exposure to drugs that might interrupt 5-HT homeostasis should be considered.
[Display omitted]
•Serotonin suppresses the synaptic currents in subplate neurons of neonatal rats.•5-HT does not affect the intrinsic properties and AMPA- or NMDA-EPSCs in SPns.•Release of glutamate from TCAs onto SPns is inhibited by 5-HT.•5-HT1B agonist mimics the suppressive effect of 5-HT on SPn EPSCs.•5-HT1B antagonist prevents 5-HT-mediated synaptic suppression.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>24055501</pmid><doi>10.1016/j.neuropharm.2013.08.040</doi><tpages>9</tpages></addata></record> |
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subjects | Animals Animals, Newborn Antagonists Brain development Dose-Response Relationship, Drug Excitatory Postsynaptic Potentials - drug effects Excitatory Postsynaptic Potentials - physiology Male Neurons - drug effects Neurons - metabolism Piperidones - pharmacology Pyridines - pharmacology Pyrroles - pharmacology Rats Rats, Wistar Receptor, Serotonin, 5-HT1B - metabolism Serotonin - pharmacology Serotonin Antagonists - pharmacology Serotonin receptor Serotonin Receptor Agonists - pharmacology Somatosensory Cortex - drug effects Somatosensory Cortex - metabolism Spiro Compounds - pharmacology Synaptic transmission Thalamocortical afferent |
title | Presynaptic 5-HT1B receptor-mediated synaptic suppression to the subplate neurons in the somatosensory cortex of neonatal rats |
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