Autoinhibition of Serotonin Cells: An Intrinsic Regulatory Mechanism Sensitive to the Pattern of Usage of the Cells
After periods of high-frequency firing, the normal rhythmically active serotonin (5HT)-containing neurosecretory neurons of the lobster ventral nerve cord display a period of suppressed spike generation and reduced synaptic input that we refer to as "autoinhibition." The duration of this a...
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Veröffentlicht in: | Proceedings of the National Academy of Sciences - PNAS 1999-03, Vol.96 (5), p.2473-2478 |
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description | After periods of high-frequency firing, the normal rhythmically active serotonin (5HT)-containing neurosecretory neurons of the lobster ventral nerve cord display a period of suppressed spike generation and reduced synaptic input that we refer to as "autoinhibition." The duration of this autoinhibition is directly related to the magnitude and duration of the current injection triggering the high-frequency firing. More interesting, however, is that the autoinhibition is inversely related to the initial firing frequency of these cells within their normal range of firing (0.5-3 Hz). This allows more active 5HT neurons to resume firing after shorter durations of inhibiton than cells that initially fired at slower rates. Although superfused 5HT inhibits the spontaneous firing of these cells, the persistence of autoinhibition in saline with no added calcium, in cadmium-containing saline, and in lobsters depleted of serotonin suggests that intrinsic membrane properties account for the autoinhibition. A similar autoinhibition is seen in spontaneously active octopamine neurons but is absent from spontaneously active γ -aminobutyric acid cells. Thus, this might be a characteristic feature of amine-containing neurosecretory neurons. The 5HT cells of vertebrate brain nuclei share similarities in firing frequencies, spike shapes, and inhibition by 5HT with the lobster cells that were the focus of this study. However, the mechanism suggested to underlie autoinhibition in vertebrate neurons is that 5HT released from activated or neighboring cells acts back on inhibitory autoreceptors that are found on the dendrites and cell bodies of these neurons. |
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The duration of this autoinhibition is directly related to the magnitude and duration of the current injection triggering the high-frequency firing. More interesting, however, is that the autoinhibition is inversely related to the initial firing frequency of these cells within their normal range of firing (0.5-3 Hz). This allows more active 5HT neurons to resume firing after shorter durations of inhibiton than cells that initially fired at slower rates. Although superfused 5HT inhibits the spontaneous firing of these cells, the persistence of autoinhibition in saline with no added calcium, in cadmium-containing saline, and in lobsters depleted of serotonin suggests that intrinsic membrane properties account for the autoinhibition. A similar autoinhibition is seen in spontaneously active octopamine neurons but is absent from spontaneously active γ -aminobutyric acid cells. Thus, this might be a characteristic feature of amine-containing neurosecretory neurons. The 5HT cells of vertebrate brain nuclei share similarities in firing frequencies, spike shapes, and inhibition by 5HT with the lobster cells that were the focus of this study. However, the mechanism suggested to underlie autoinhibition in vertebrate neurons is that 5HT released from activated or neighboring cells acts back on inhibitory autoreceptors that are found on the dendrites and cell bodies of these neurons.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.96.5.2473</identifier><identifier>PMID: 10051667</identifier><language>eng</language><publisher>United States: National Academy of Sciences of the United States of America</publisher><subject>Action potentials ; Amines ; Animals ; Behavioral neuroscience ; Biological Sciences ; Calcium ; Cells ; Electrophysiology ; Evoked Potentials - drug effects ; Evoked Potentials - physiology ; Ganglia ; Homeostasis ; In Vitro Techniques ; Lobsters ; Nephropidae ; Neuroglia ; Neurology ; Neurons ; Neurons - drug effects ; Neurons - physiology ; Neurosecretory cells ; Serotonin - pharmacology ; Serotonin - physiology ; Shellfish ; Time Factors ; Vertebrates</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 1999-03, Vol.96 (5), p.2473-2478</ispartof><rights>Copyright 1993-1999 The National Academy of Sciences of the United States of America</rights><rights>Copyright National Academy of Sciences Mar 2, 1999</rights><rights>Copyright © 1999, The National Academy of Sciences 1999</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c514t-ce807aa01ac104e64907158ad92b0a183a8d4e6bde05f362bdc4ed4b025664323</citedby><cites>FETCH-LOGICAL-c514t-ce807aa01ac104e64907158ad92b0a183a8d4e6bde05f362bdc4ed4b025664323</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/96/5.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/47086$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/47086$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,803,885,27924,27925,53791,53793,58017,58250</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/10051667$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Heinrich, Ralf</creatorcontrib><creatorcontrib>Cromarty, Stuart I.</creatorcontrib><creatorcontrib>Horner, Michael</creatorcontrib><creatorcontrib>Edwards, Donald H.</creatorcontrib><creatorcontrib>Kravitz, Edward A.</creatorcontrib><title>Autoinhibition of Serotonin Cells: An Intrinsic Regulatory Mechanism Sensitive to the Pattern of Usage of the Cells</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>After periods of high-frequency firing, the normal rhythmically active serotonin (5HT)-containing neurosecretory neurons of the lobster ventral nerve cord display a period of suppressed spike generation and reduced synaptic input that we refer to as "autoinhibition." The duration of this autoinhibition is directly related to the magnitude and duration of the current injection triggering the high-frequency firing. More interesting, however, is that the autoinhibition is inversely related to the initial firing frequency of these cells within their normal range of firing (0.5-3 Hz). This allows more active 5HT neurons to resume firing after shorter durations of inhibiton than cells that initially fired at slower rates. Although superfused 5HT inhibits the spontaneous firing of these cells, the persistence of autoinhibition in saline with no added calcium, in cadmium-containing saline, and in lobsters depleted of serotonin suggests that intrinsic membrane properties account for the autoinhibition. A similar autoinhibition is seen in spontaneously active octopamine neurons but is absent from spontaneously active γ -aminobutyric acid cells. Thus, this might be a characteristic feature of amine-containing neurosecretory neurons. The 5HT cells of vertebrate brain nuclei share similarities in firing frequencies, spike shapes, and inhibition by 5HT with the lobster cells that were the focus of this study. However, the mechanism suggested to underlie autoinhibition in vertebrate neurons is that 5HT released from activated or neighboring cells acts back on inhibitory autoreceptors that are found on the dendrites and cell bodies of these neurons.</description><subject>Action potentials</subject><subject>Amines</subject><subject>Animals</subject><subject>Behavioral neuroscience</subject><subject>Biological Sciences</subject><subject>Calcium</subject><subject>Cells</subject><subject>Electrophysiology</subject><subject>Evoked Potentials - drug effects</subject><subject>Evoked Potentials - physiology</subject><subject>Ganglia</subject><subject>Homeostasis</subject><subject>In Vitro Techniques</subject><subject>Lobsters</subject><subject>Nephropidae</subject><subject>Neuroglia</subject><subject>Neurology</subject><subject>Neurons</subject><subject>Neurons - drug effects</subject><subject>Neurons - physiology</subject><subject>Neurosecretory cells</subject><subject>Serotonin - pharmacology</subject><subject>Serotonin - physiology</subject><subject>Shellfish</subject><subject>Time Factors</subject><subject>Vertebrates</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1999</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNqFks9v0zAcxS3ExMrgygEJZHHYLeHrn0kQl6oCNmkIBOxsOYnbukrtznYm9t_jrGUqHOBky9_Pe_LzM0IvCJQEKvZ253QsG1mKkvKKPUIzAg0pJG_gMZoB0KqoOeWn6GmMGwBoRA1P0CkBEETKaobifEzeurVtbbLeYb_E303wyTvr8MIMQ3yH5w5fuhSsi7bD38xqHHTy4Q5_Nt1aOxu3WZJnyd4anDxOa4O_6pRMuLe7jnplps10fu_4DJ0s9RDN88N6hq4_fvixuCiuvny6XMyvik4QnorO1FBpDUR3BLiZMlVE1LpvaAua1EzXfT5uewNiySRt-46bnrdAhZScUXaG3u99d2O7NX1ncgg9qF2wWx3ulNdW_Tlxdq1W_lZRWUOT5ecHefA3o4lJbW3scgDtjB-jko0ERgn_L0gqkg0rlsE3f4EbPwaX30BRIIwKIiBD5R7qgo8xmOXDhQmoqXM1da4aqYSaOs-C18cxj_B9yRl4dQAm4e_xscH5v-ZqOQ5DMj9TBl_uwU3MH-CB5BXUkv0C2_nJxA</recordid><startdate>19990302</startdate><enddate>19990302</enddate><creator>Heinrich, Ralf</creator><creator>Cromarty, Stuart I.</creator><creator>Horner, Michael</creator><creator>Edwards, Donald H.</creator><creator>Kravitz, Edward A.</creator><general>National Academy of Sciences of the United States of America</general><general>National Acad Sciences</general><general>National Academy of Sciences</general><general>The National Academy of Sciences</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>7QG</scope><scope>7QL</scope><scope>7QP</scope><scope>7QR</scope><scope>7SN</scope><scope>7SS</scope><scope>7T5</scope><scope>7TK</scope><scope>7TM</scope><scope>7TO</scope><scope>7U9</scope><scope>8FD</scope><scope>C1K</scope><scope>FR3</scope><scope>H94</scope><scope>M7N</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>19990302</creationdate><title>Autoinhibition of Serotonin Cells: An Intrinsic Regulatory Mechanism Sensitive to the Pattern of Usage of the Cells</title><author>Heinrich, Ralf ; 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subjects | Action potentials Amines Animals Behavioral neuroscience Biological Sciences Calcium Cells Electrophysiology Evoked Potentials - drug effects Evoked Potentials - physiology Ganglia Homeostasis In Vitro Techniques Lobsters Nephropidae Neuroglia Neurology Neurons Neurons - drug effects Neurons - physiology Neurosecretory cells Serotonin - pharmacology Serotonin - physiology Shellfish Time Factors Vertebrates |
title | Autoinhibition of Serotonin Cells: An Intrinsic Regulatory Mechanism Sensitive to the Pattern of Usage of the Cells |
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