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Projection Neurons with Shared Cotransmitters Elicit Different Motor Patterns from the Same Neural Circuit
Specificity in the actions of different modulatory neurons is often attributed to their having distinct cotransmitter complements. We are assessing the validity of this hypothesis with the stomatogastric nervous system of the crab Cancer borealis. In this nervous system, the stomatogastric ganglion...
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Published in: | The Journal of neuroscience 2000-12, Vol.20 (23), p.8943-8953 |
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description | Specificity in the actions of different modulatory neurons is often attributed to their having distinct cotransmitter complements. We are assessing the validity of this hypothesis with the stomatogastric nervous system of the crab Cancer borealis. In this nervous system, the stomatogastric ganglion (STG) contains a multifunctional network that generates the gastric mill and pyloric rhythms. Two identified projection neurons [modulatory proctolin neuron (MPN) and modulatory commissural neuron 1 (MCN1)] that innervate the STG and modulate these rhythms contain GABA and the pentapeptide proctolin, but only MCN1 contains Cancer borealis tachykinin-related peptide (CabTRP Ia). Selective activation of each projection neuron elicits different rhythms from the STG. MPN elicits only a pyloric rhythm, whereas MCN1 elicits a distinct pyloric rhythm as well as a gastric mill rhythm. We tested the degree to which CabTRP Ia distinguishes the actions of MCN1 and MPN. To this end, we used the tachykinin receptor antagonist Spantide I to eliminate the actions of CabTRP Ia. With Spantide I present, MCN1 no longer elicited the gastric mill rhythm and the resulting pyloric rhythm was changed. Although this rhythm was more similar to the MPN-elicited pyloric rhythm, these rhythms remained different. Thus, CabTRP Ia partially confers the differences in rhythm generation resulting from MPN versus MCN1 activation. This result suggests that different projection neurons may use the same cotransmitters differently to elicit distinct pyloric rhythms. It also supports the hypothesis that different projection neurons use a combination of strategies, including using distinct cotransmitter complements, to elicit different outputs from the same neuronal network. |
doi_str_mv | 10.1523/jneurosci.20-23-08943.2000 |
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We are assessing the validity of this hypothesis with the stomatogastric nervous system of the crab Cancer borealis. In this nervous system, the stomatogastric ganglion (STG) contains a multifunctional network that generates the gastric mill and pyloric rhythms. Two identified projection neurons [modulatory proctolin neuron (MPN) and modulatory commissural neuron 1 (MCN1)] that innervate the STG and modulate these rhythms contain GABA and the pentapeptide proctolin, but only MCN1 contains Cancer borealis tachykinin-related peptide (CabTRP Ia). Selective activation of each projection neuron elicits different rhythms from the STG. MPN elicits only a pyloric rhythm, whereas MCN1 elicits a distinct pyloric rhythm as well as a gastric mill rhythm. We tested the degree to which CabTRP Ia distinguishes the actions of MCN1 and MPN. To this end, we used the tachykinin receptor antagonist Spantide I to eliminate the actions of CabTRP Ia. With Spantide I present, MCN1 no longer elicited the gastric mill rhythm and the resulting pyloric rhythm was changed. Although this rhythm was more similar to the MPN-elicited pyloric rhythm, these rhythms remained different. Thus, CabTRP Ia partially confers the differences in rhythm generation resulting from MPN versus MCN1 activation. This result suggests that different projection neurons may use the same cotransmitters differently to elicit distinct pyloric rhythms. It also supports the hypothesis that different projection neurons use a combination of strategies, including using distinct cotransmitter complements, to elicit different outputs from the same neuronal network.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/jneurosci.20-23-08943.2000</identifier><identifier>PMID: 11102505</identifier><language>eng</language><publisher>United States: Soc Neuroscience</publisher><subject>Action Potentials - drug effects ; Action Potentials - physiology ; Animals ; Brachyura ; Digestive System - innervation ; Enzyme Inhibitors - pharmacology ; gamma-Aminobutyric Acid - metabolism ; Ganglia, Invertebrate - cytology ; Ganglia, Invertebrate - drug effects ; Ganglia, Invertebrate - immunology ; Ganglia, Invertebrate - metabolism ; Gastric Emptying - drug effects ; Gastric Emptying - physiology ; Glycopeptides - pharmacology ; In Vitro Techniques ; Male ; Neprilysin - antagonists & inhibitors ; Nerve Net - drug effects ; Nerve Net - physiology ; Neurons - cytology ; Neurons - drug effects ; Neurons - metabolism ; Neuropeptides ; Neurotransmitter Agents - antagonists & inhibitors ; Neurotransmitter Agents - metabolism ; Oligopeptides - metabolism ; Periodicity ; Receptors, Invertebrate Peptide - metabolism ; Receptors, Tachykinin - antagonists & inhibitors ; Receptors, Tachykinin - metabolism ; Substance P - analogs & derivatives ; Substance P - pharmacology ; Tachykinins - antagonists & inhibitors ; Tachykinins - metabolism</subject><ispartof>The Journal of neuroscience, 2000-12, Vol.20 (23), p.8943-8953</ispartof><rights>Copyright © 2000 Society for Neuroscience 2000</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c511t-be00c5d37d47b1a5a9ab7cd2c5c5d46d55527edc840fde663e43b512897110593</citedby><cites>FETCH-LOGICAL-c511t-be00c5d37d47b1a5a9ab7cd2c5c5d46d55527edc840fde663e43b512897110593</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6773044/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC6773044/$$EHTML$$P50$$Gpubmedcentral$$H</linktohtml><link.rule.ids>230,314,727,780,784,885,27924,27925,53791,53793</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/11102505$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Wood, Debra E</creatorcontrib><creatorcontrib>Stein, Wolfgang</creatorcontrib><creatorcontrib>Nusbaum, Michael P</creatorcontrib><title>Projection Neurons with Shared Cotransmitters Elicit Different Motor Patterns from the Same Neural Circuit</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>Specificity in the actions of different modulatory neurons is often attributed to their having distinct cotransmitter complements. We are assessing the validity of this hypothesis with the stomatogastric nervous system of the crab Cancer borealis. In this nervous system, the stomatogastric ganglion (STG) contains a multifunctional network that generates the gastric mill and pyloric rhythms. Two identified projection neurons [modulatory proctolin neuron (MPN) and modulatory commissural neuron 1 (MCN1)] that innervate the STG and modulate these rhythms contain GABA and the pentapeptide proctolin, but only MCN1 contains Cancer borealis tachykinin-related peptide (CabTRP Ia). Selective activation of each projection neuron elicits different rhythms from the STG. MPN elicits only a pyloric rhythm, whereas MCN1 elicits a distinct pyloric rhythm as well as a gastric mill rhythm. We tested the degree to which CabTRP Ia distinguishes the actions of MCN1 and MPN. To this end, we used the tachykinin receptor antagonist Spantide I to eliminate the actions of CabTRP Ia. With Spantide I present, MCN1 no longer elicited the gastric mill rhythm and the resulting pyloric rhythm was changed. Although this rhythm was more similar to the MPN-elicited pyloric rhythm, these rhythms remained different. Thus, CabTRP Ia partially confers the differences in rhythm generation resulting from MPN versus MCN1 activation. This result suggests that different projection neurons may use the same cotransmitters differently to elicit distinct pyloric rhythms. It also supports the hypothesis that different projection neurons use a combination of strategies, including using distinct cotransmitter complements, to elicit different outputs from the same neuronal network.</description><subject>Action Potentials - drug effects</subject><subject>Action Potentials - physiology</subject><subject>Animals</subject><subject>Brachyura</subject><subject>Digestive System - innervation</subject><subject>Enzyme Inhibitors - pharmacology</subject><subject>gamma-Aminobutyric Acid - metabolism</subject><subject>Ganglia, Invertebrate - cytology</subject><subject>Ganglia, Invertebrate - drug effects</subject><subject>Ganglia, Invertebrate - immunology</subject><subject>Ganglia, Invertebrate - metabolism</subject><subject>Gastric Emptying - drug effects</subject><subject>Gastric Emptying - physiology</subject><subject>Glycopeptides - pharmacology</subject><subject>In Vitro Techniques</subject><subject>Male</subject><subject>Neprilysin - antagonists & inhibitors</subject><subject>Nerve Net - drug effects</subject><subject>Nerve Net - physiology</subject><subject>Neurons - cytology</subject><subject>Neurons - drug effects</subject><subject>Neurons - metabolism</subject><subject>Neuropeptides</subject><subject>Neurotransmitter Agents - antagonists & inhibitors</subject><subject>Neurotransmitter Agents - metabolism</subject><subject>Oligopeptides - metabolism</subject><subject>Periodicity</subject><subject>Receptors, Invertebrate Peptide - metabolism</subject><subject>Receptors, Tachykinin - antagonists & inhibitors</subject><subject>Receptors, Tachykinin - metabolism</subject><subject>Substance P - analogs & derivatives</subject><subject>Substance P - pharmacology</subject><subject>Tachykinins - antagonists & inhibitors</subject><subject>Tachykinins - metabolism</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2000</creationdate><recordtype>article</recordtype><recordid>eNpVkUtv1DAURi0EokPhLyCLBaxSbMeOExZIVRigqLQVQ9eW49w0HiVxsR0i_j1OZ8Rj5de5517rQ-gVJWdUsPztfoLZu2DsGSMZyzNSVjxPe0IeoU0iqoxxQh-jDWGSZAWX_AQ9C2GfAEmofIpOKKWECSI2aH_j3R5MtG7CV6t2Cnixsce7Xntoce2i11MYbYzgA94O1tiIP9iuAw9TxF9ddB7f6PU5lXbejTj2gHd6hAehHnBtvZltfI6edHoI8OK4nqLbj9vv9efs8vrTRX1-mRlBacwaIMSINpctlw3VQle6kaZlRqRbXrRCCCahNSUnXQtFkQPPG0FZWcn0K1Hlp-j9wXs_N2MC05hpCnXv7aj9L-W0Vf-_TLZXd-6nKqTMCedJ8Poo8O7HDCGq0QYDw6AncHNQknHBynLt9O4AmhRH8ND9aUKJWqNSX662t9-ud_WFYkSl80NUao0qFb_8d8y_pcdsEvDmAPT2rl-sBxVGPQwJp2pZloNw9eW_AaCAojw</recordid><startdate>20001201</startdate><enddate>20001201</enddate><creator>Wood, Debra E</creator><creator>Stein, Wolfgang</creator><creator>Nusbaum, Michael P</creator><general>Soc Neuroscience</general><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>5PM</scope></search><sort><creationdate>20001201</creationdate><title>Projection Neurons with Shared Cotransmitters Elicit Different Motor Patterns from the Same Neural Circuit</title><author>Wood, Debra E ; Stein, Wolfgang ; Nusbaum, Michael P</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c511t-be00c5d37d47b1a5a9ab7cd2c5c5d46d55527edc840fde663e43b512897110593</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2000</creationdate><topic>Action Potentials - drug effects</topic><topic>Action Potentials - physiology</topic><topic>Animals</topic><topic>Brachyura</topic><topic>Digestive System - innervation</topic><topic>Enzyme Inhibitors - pharmacology</topic><topic>gamma-Aminobutyric Acid - metabolism</topic><topic>Ganglia, Invertebrate - cytology</topic><topic>Ganglia, Invertebrate - drug effects</topic><topic>Ganglia, Invertebrate - immunology</topic><topic>Ganglia, Invertebrate - metabolism</topic><topic>Gastric Emptying - drug effects</topic><topic>Gastric Emptying - physiology</topic><topic>Glycopeptides - pharmacology</topic><topic>In Vitro Techniques</topic><topic>Male</topic><topic>Neprilysin - antagonists & inhibitors</topic><topic>Nerve Net - drug effects</topic><topic>Nerve Net - physiology</topic><topic>Neurons - cytology</topic><topic>Neurons - drug effects</topic><topic>Neurons - metabolism</topic><topic>Neuropeptides</topic><topic>Neurotransmitter Agents - antagonists & inhibitors</topic><topic>Neurotransmitter Agents - metabolism</topic><topic>Oligopeptides - metabolism</topic><topic>Periodicity</topic><topic>Receptors, Invertebrate Peptide - metabolism</topic><topic>Receptors, Tachykinin - antagonists & inhibitors</topic><topic>Receptors, Tachykinin - metabolism</topic><topic>Substance P - analogs & derivatives</topic><topic>Substance P - pharmacology</topic><topic>Tachykinins - antagonists & inhibitors</topic><topic>Tachykinins - metabolism</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Wood, Debra E</creatorcontrib><creatorcontrib>Stein, Wolfgang</creatorcontrib><creatorcontrib>Nusbaum, Michael P</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>PubMed Central (Full Participant titles)</collection><jtitle>The Journal of neuroscience</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Wood, Debra E</au><au>Stein, Wolfgang</au><au>Nusbaum, Michael P</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Projection Neurons with Shared Cotransmitters Elicit Different Motor Patterns from the Same Neural Circuit</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2000-12-01</date><risdate>2000</risdate><volume>20</volume><issue>23</issue><spage>8943</spage><epage>8953</epage><pages>8943-8953</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>Specificity in the actions of different modulatory neurons is often attributed to their having distinct cotransmitter complements. We are assessing the validity of this hypothesis with the stomatogastric nervous system of the crab Cancer borealis. In this nervous system, the stomatogastric ganglion (STG) contains a multifunctional network that generates the gastric mill and pyloric rhythms. Two identified projection neurons [modulatory proctolin neuron (MPN) and modulatory commissural neuron 1 (MCN1)] that innervate the STG and modulate these rhythms contain GABA and the pentapeptide proctolin, but only MCN1 contains Cancer borealis tachykinin-related peptide (CabTRP Ia). Selective activation of each projection neuron elicits different rhythms from the STG. MPN elicits only a pyloric rhythm, whereas MCN1 elicits a distinct pyloric rhythm as well as a gastric mill rhythm. We tested the degree to which CabTRP Ia distinguishes the actions of MCN1 and MPN. To this end, we used the tachykinin receptor antagonist Spantide I to eliminate the actions of CabTRP Ia. With Spantide I present, MCN1 no longer elicited the gastric mill rhythm and the resulting pyloric rhythm was changed. Although this rhythm was more similar to the MPN-elicited pyloric rhythm, these rhythms remained different. Thus, CabTRP Ia partially confers the differences in rhythm generation resulting from MPN versus MCN1 activation. This result suggests that different projection neurons may use the same cotransmitters differently to elicit distinct pyloric rhythms. It also supports the hypothesis that different projection neurons use a combination of strategies, including using distinct cotransmitter complements, to elicit different outputs from the same neuronal network.</abstract><cop>United States</cop><pub>Soc Neuroscience</pub><pmid>11102505</pmid><doi>10.1523/jneurosci.20-23-08943.2000</doi><tpages>11</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Action Potentials - drug effects Action Potentials - physiology Animals Brachyura Digestive System - innervation Enzyme Inhibitors - pharmacology gamma-Aminobutyric Acid - metabolism Ganglia, Invertebrate - cytology Ganglia, Invertebrate - drug effects Ganglia, Invertebrate - immunology Ganglia, Invertebrate - metabolism Gastric Emptying - drug effects Gastric Emptying - physiology Glycopeptides - pharmacology In Vitro Techniques Male Neprilysin - antagonists & inhibitors Nerve Net - drug effects Nerve Net - physiology Neurons - cytology Neurons - drug effects Neurons - metabolism Neuropeptides Neurotransmitter Agents - antagonists & inhibitors Neurotransmitter Agents - metabolism Oligopeptides - metabolism Periodicity Receptors, Invertebrate Peptide - metabolism Receptors, Tachykinin - antagonists & inhibitors Receptors, Tachykinin - metabolism Substance P - analogs & derivatives Substance P - pharmacology Tachykinins - antagonists & inhibitors Tachykinins - metabolism |
title | Projection Neurons with Shared Cotransmitters Elicit Different Motor Patterns from the Same Neural Circuit |
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