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Different Classes of Glutamate Receptors Mediate Distinct Behaviors in a Single Brainstem Nucleus
We have taken advantage of the increasing understanding of glutamate neuropharmacology to probe mechanisms of well-defined vertebrate behaviors. Here we report a set of experiments that suggests distinct roles for two major classes of glutamate receptors in a discrete premotor nucleus of the brainst...
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Published in: | Proceedings of the National Academy of Sciences - PNAS 1989-11, Vol.86 (22), p.8993-8997 |
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creator | Dye, John Heiligenberg, Walter Keller, Clifford H. Kawasaki, Masashi |
description | We have taken advantage of the increasing understanding of glutamate neuropharmacology to probe mechanisms of well-defined vertebrate behaviors. Here we report a set of experiments that suggests distinct roles for two major classes of glutamate receptors in a discrete premotor nucleus of the brainstem. The medullary pacemaker nucleus of weakly electric fish is an endogenous oscillator that controls the electric organ discharge (EOD). Its regular frequency of firing is modulated during several distinct behaviors. The pacemaker nucleus continues firing regularly when isolated in vitro, and modulatory behaviors can be reproduced by stimulating the descending input pathway. Glutamate agonists applied to the pacemaker in vitro produced increases in frequency, while glutamate antagonists selectively blocked stimulus-induced modulations. Experiments with glutamate antagonists in the intact animal resulted in specific effects on two well-characterized behaviors. Our data indicate that these behaviors are separately mediated in the pacemaker by receptors displaying characteristics of the kainate/quisqualate and N-methyl-D-aspartate subtypes of glutamate receptor, respectively. |
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Here we report a set of experiments that suggests distinct roles for two major classes of glutamate receptors in a discrete premotor nucleus of the brainstem. The medullary pacemaker nucleus of weakly electric fish is an endogenous oscillator that controls the electric organ discharge (EOD). Its regular frequency of firing is modulated during several distinct behaviors. The pacemaker nucleus continues firing regularly when isolated in vitro, and modulatory behaviors can be reproduced by stimulating the descending input pathway. Glutamate agonists applied to the pacemaker in vitro produced increases in frequency, while glutamate antagonists selectively blocked stimulus-induced modulations. Experiments with glutamate antagonists in the intact animal resulted in specific effects on two well-characterized behaviors. Our data indicate that these behaviors are separately mediated in the pacemaker by receptors displaying characteristics of the kainate/quisqualate and N-methyl-D-aspartate subtypes of glutamate receptor, respectively.</description><identifier>ISSN: 0027-8424</identifier><identifier>EISSN: 1091-6490</identifier><identifier>DOI: 10.1073/pnas.86.22.8993</identifier><identifier>PMID: 2573071</identifier><identifier>CODEN: PNASA6</identifier><language>eng</language><publisher>Washington, DC: National Academy of Sciences of the United States of America</publisher><subject>2-Amino-5-phosphonovalerate - pharmacology ; Agonists ; Animal vocalization ; Animals ; Anticonvulsants - pharmacology ; Apteronotus leptorhynchus ; Artificial pacemakers ; Aspartic Acid - pharmacology ; Avoidance Learning - drug effects ; Biological and medical sciences ; Brain Stem - drug effects ; Brain Stem - physiology ; Central nervous system ; Central neurotransmission. Neuromudulation. Pathways and receptors ; Dicarboxylic acids ; Eigenmannia ; Electric fields ; Electric Fish ; Electric Organ - physiology ; Electrodes ; Excitatory amino acid antagonists ; Fundamental and applied biological sciences. Psychology ; Glutamate receptors ; Glutamates - pharmacology ; Glutamates - physiology ; Glutamic Acid ; Glutamine - pharmacology ; Kainic Acid - pharmacology ; N-Methylaspartate ; Neurobiology ; Neurons ; Oxadiazoles - pharmacology ; Pipecolic Acids - pharmacology ; Quisqualic Acid ; Receptors, Glutamate ; Receptors, Neurotransmitter - physiology ; Vertebrates: nervous system and sense organs</subject><ispartof>Proceedings of the National Academy of Sciences - PNAS, 1989-11, Vol.86 (22), p.8993-8997</ispartof><rights>1991 INIST-CNRS</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c4373-cf9ea233c9499503f95705ab0c3d189802faed9223a95190a799abd09e0bd9fd3</citedby></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Uhttp://www.pnas.org/content/86/22.cover.gif</thumbnail><linktopdf>$$Uhttps://www.jstor.org/stable/pdf/35006$$EPDF$$P50$$Gjstor$$H</linktopdf><linktohtml>$$Uhttps://www.jstor.org/stable/35006$$EHTML$$P50$$Gjstor$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793,58238,58471</link.rule.ids><backlink>$$Uhttp://pascal-francis.inist.fr/vibad/index.php?action=getRecordDetail&idt=19377888$$DView record in Pascal Francis$$Hfree_for_read</backlink><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/2573071$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Dye, John</creatorcontrib><creatorcontrib>Heiligenberg, Walter</creatorcontrib><creatorcontrib>Keller, Clifford H.</creatorcontrib><creatorcontrib>Kawasaki, Masashi</creatorcontrib><title>Different Classes of Glutamate Receptors Mediate Distinct Behaviors in a Single Brainstem Nucleus</title><title>Proceedings of the National Academy of Sciences - PNAS</title><addtitle>Proc Natl Acad Sci U S A</addtitle><description>We have taken advantage of the increasing understanding of glutamate neuropharmacology to probe mechanisms of well-defined vertebrate behaviors. Here we report a set of experiments that suggests distinct roles for two major classes of glutamate receptors in a discrete premotor nucleus of the brainstem. The medullary pacemaker nucleus of weakly electric fish is an endogenous oscillator that controls the electric organ discharge (EOD). Its regular frequency of firing is modulated during several distinct behaviors. The pacemaker nucleus continues firing regularly when isolated in vitro, and modulatory behaviors can be reproduced by stimulating the descending input pathway. Glutamate agonists applied to the pacemaker in vitro produced increases in frequency, while glutamate antagonists selectively blocked stimulus-induced modulations. Experiments with glutamate antagonists in the intact animal resulted in specific effects on two well-characterized behaviors. Our data indicate that these behaviors are separately mediated in the pacemaker by receptors displaying characteristics of the kainate/quisqualate and N-methyl-D-aspartate subtypes of glutamate receptor, respectively.</description><subject>2-Amino-5-phosphonovalerate - pharmacology</subject><subject>Agonists</subject><subject>Animal vocalization</subject><subject>Animals</subject><subject>Anticonvulsants - pharmacology</subject><subject>Apteronotus leptorhynchus</subject><subject>Artificial pacemakers</subject><subject>Aspartic Acid - pharmacology</subject><subject>Avoidance Learning - drug effects</subject><subject>Biological and medical sciences</subject><subject>Brain Stem - drug effects</subject><subject>Brain Stem - physiology</subject><subject>Central nervous system</subject><subject>Central neurotransmission. Neuromudulation. Pathways and receptors</subject><subject>Dicarboxylic acids</subject><subject>Eigenmannia</subject><subject>Electric fields</subject><subject>Electric Fish</subject><subject>Electric Organ - physiology</subject><subject>Electrodes</subject><subject>Excitatory amino acid antagonists</subject><subject>Fundamental and applied biological sciences. Psychology</subject><subject>Glutamate receptors</subject><subject>Glutamates - pharmacology</subject><subject>Glutamates - physiology</subject><subject>Glutamic Acid</subject><subject>Glutamine - pharmacology</subject><subject>Kainic Acid - pharmacology</subject><subject>N-Methylaspartate</subject><subject>Neurobiology</subject><subject>Neurons</subject><subject>Oxadiazoles - pharmacology</subject><subject>Pipecolic Acids - pharmacology</subject><subject>Quisqualic Acid</subject><subject>Receptors, Glutamate</subject><subject>Receptors, Neurotransmitter - physiology</subject><subject>Vertebrates: nervous system and sense organs</subject><issn>0027-8424</issn><issn>1091-6490</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>1989</creationdate><recordtype>article</recordtype><recordid>eNqFks1v1DAQxSMEKkvhjIQEygU4ZTuxk7XnwIFuoSAVkPg4W7POuHXlTRY7qeC_J9GGLVzgZMnvNx_Pz1n2uIRlCUqe7FpKS71aCrHUiPJOtigBy2JVIdzNFgBCFboS1f3sQUrXAIC1hqPsSNRKgioXGZ155zhy2-frQClxyjuXn4ehpy31nH9my7u-iyn_wI2fbs586n1r-_yUr-jGT5Jvc8q_-PYycH4aybep523-cbCBh_Qwu-coJH40n8fZt7dvvq7fFRefzt-vX18UtpJKFtYhk5DSYoVYg3RYK6hpA1Y2pUYNwhE3KIQkrEsEUoi0aQAZNg26Rh5nr_Z9d8Nmy40dLUUKZhf9luJP05E3fyutvzKX3Y0RqKtSj_Uv5vrYfR849Wbrk-UQqOVuSEbh-GJYqf-CZV1Votb1CJ7sQRu7lCK7wzIlmCk9M6Vn9MoIYab0xoqnf3o48HNco_581ilZCi5Sa326bYtSKa0nLy9nbhrwW74dZNwQQs8_-pF89k9yBJ7sges0foMDIWuAlfwF2TXFYg</recordid><startdate>19891101</startdate><enddate>19891101</enddate><creator>Dye, John</creator><creator>Heiligenberg, Walter</creator><creator>Keller, Clifford H.</creator><creator>Kawasaki, Masashi</creator><general>National Academy of Sciences of the United States of America</general><general>National Acad Sciences</general><scope>IQODW</scope><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>7TK</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>19891101</creationdate><title>Different Classes of Glutamate Receptors Mediate Distinct Behaviors in a Single Brainstem Nucleus</title><author>Dye, John ; Heiligenberg, Walter ; Keller, Clifford H. ; Kawasaki, Masashi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c4373-cf9ea233c9499503f95705ab0c3d189802faed9223a95190a799abd09e0bd9fd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>1989</creationdate><topic>2-Amino-5-phosphonovalerate - pharmacology</topic><topic>Agonists</topic><topic>Animal vocalization</topic><topic>Animals</topic><topic>Anticonvulsants - pharmacology</topic><topic>Apteronotus leptorhynchus</topic><topic>Artificial pacemakers</topic><topic>Aspartic Acid - pharmacology</topic><topic>Avoidance Learning - drug effects</topic><topic>Biological and medical sciences</topic><topic>Brain Stem - drug effects</topic><topic>Brain Stem - physiology</topic><topic>Central nervous system</topic><topic>Central neurotransmission. Neuromudulation. Pathways and receptors</topic><topic>Dicarboxylic acids</topic><topic>Eigenmannia</topic><topic>Electric fields</topic><topic>Electric Fish</topic><topic>Electric Organ - physiology</topic><topic>Electrodes</topic><topic>Excitatory amino acid antagonists</topic><topic>Fundamental and applied biological sciences. Psychology</topic><topic>Glutamate receptors</topic><topic>Glutamates - pharmacology</topic><topic>Glutamates - physiology</topic><topic>Glutamic Acid</topic><topic>Glutamine - pharmacology</topic><topic>Kainic Acid - pharmacology</topic><topic>N-Methylaspartate</topic><topic>Neurobiology</topic><topic>Neurons</topic><topic>Oxadiazoles - pharmacology</topic><topic>Pipecolic Acids - pharmacology</topic><topic>Quisqualic Acid</topic><topic>Receptors, Glutamate</topic><topic>Receptors, Neurotransmitter - physiology</topic><topic>Vertebrates: nervous system and sense organs</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Dye, John</creatorcontrib><creatorcontrib>Heiligenberg, Walter</creatorcontrib><creatorcontrib>Keller, Clifford H.</creatorcontrib><creatorcontrib>Kawasaki, Masashi</creatorcontrib><collection>Pascal-Francis</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Neurosciences Abstracts</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Dye, John</au><au>Heiligenberg, Walter</au><au>Keller, Clifford H.</au><au>Kawasaki, Masashi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Different Classes of Glutamate Receptors Mediate Distinct Behaviors in a Single Brainstem Nucleus</atitle><jtitle>Proceedings of the National Academy of Sciences - PNAS</jtitle><addtitle>Proc Natl Acad Sci U S A</addtitle><date>1989-11-01</date><risdate>1989</risdate><volume>86</volume><issue>22</issue><spage>8993</spage><epage>8997</epage><pages>8993-8997</pages><issn>0027-8424</issn><eissn>1091-6490</eissn><coden>PNASA6</coden><abstract>We have taken advantage of the increasing understanding of glutamate neuropharmacology to probe mechanisms of well-defined vertebrate behaviors. Here we report a set of experiments that suggests distinct roles for two major classes of glutamate receptors in a discrete premotor nucleus of the brainstem. The medullary pacemaker nucleus of weakly electric fish is an endogenous oscillator that controls the electric organ discharge (EOD). Its regular frequency of firing is modulated during several distinct behaviors. The pacemaker nucleus continues firing regularly when isolated in vitro, and modulatory behaviors can be reproduced by stimulating the descending input pathway. Glutamate agonists applied to the pacemaker in vitro produced increases in frequency, while glutamate antagonists selectively blocked stimulus-induced modulations. Experiments with glutamate antagonists in the intact animal resulted in specific effects on two well-characterized behaviors. Our data indicate that these behaviors are separately mediated in the pacemaker by receptors displaying characteristics of the kainate/quisqualate and N-methyl-D-aspartate subtypes of glutamate receptor, respectively.</abstract><cop>Washington, DC</cop><pub>National Academy of Sciences of the United States of America</pub><pmid>2573071</pmid><doi>10.1073/pnas.86.22.8993</doi><tpages>5</tpages><oa>free_for_read</oa></addata></record> |
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ispartof | Proceedings of the National Academy of Sciences - PNAS, 1989-11, Vol.86 (22), p.8993-8997 |
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subjects | 2-Amino-5-phosphonovalerate - pharmacology Agonists Animal vocalization Animals Anticonvulsants - pharmacology Apteronotus leptorhynchus Artificial pacemakers Aspartic Acid - pharmacology Avoidance Learning - drug effects Biological and medical sciences Brain Stem - drug effects Brain Stem - physiology Central nervous system Central neurotransmission. Neuromudulation. Pathways and receptors Dicarboxylic acids Eigenmannia Electric fields Electric Fish Electric Organ - physiology Electrodes Excitatory amino acid antagonists Fundamental and applied biological sciences. Psychology Glutamate receptors Glutamates - pharmacology Glutamates - physiology Glutamic Acid Glutamine - pharmacology Kainic Acid - pharmacology N-Methylaspartate Neurobiology Neurons Oxadiazoles - pharmacology Pipecolic Acids - pharmacology Quisqualic Acid Receptors, Glutamate Receptors, Neurotransmitter - physiology Vertebrates: nervous system and sense organs |
title | Different Classes of Glutamate Receptors Mediate Distinct Behaviors in a Single Brainstem Nucleus |
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