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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
Main Authors: Wood, Debra E, Stein, Wolfgang, Nusbaum, Michael P
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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.
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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. 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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 &amp; 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 &amp; inhibitors</topic><topic>Neurotransmitter Agents - metabolism</topic><topic>Oligopeptides - metabolism</topic><topic>Periodicity</topic><topic>Receptors, Invertebrate Peptide - metabolism</topic><topic>Receptors, Tachykinin - antagonists &amp; inhibitors</topic><topic>Receptors, Tachykinin - metabolism</topic><topic>Substance P - analogs &amp; derivatives</topic><topic>Substance P - pharmacology</topic><topic>Tachykinins - antagonists &amp; 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. 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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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