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Coordination and Modulation of Locomotion Pattern Generators in Drosophila Larvae: Effects of Altered Biogenic Amine Levels by the Tyramine beta Hydroxlyase Mutation
Forward locomotion of Drosophila melanogaster larvae is composed of rhythmic waves of contractions that are thought to be produced by segmentally organized central pattern generators. We present a systematic description of spike activity patterns during locomotive contraction waves in semi-intact wi...
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Published in: | The Journal of neuroscience 2006-02, Vol.26 (5), p.1486-1498 |
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description | Forward locomotion of Drosophila melanogaster larvae is composed of rhythmic waves of contractions that are thought to be produced by segmentally organized central pattern generators. We present a systematic description of spike activity patterns during locomotive contraction waves in semi-intact wild-type and mutant larval preparations. We have shown previously that Tbetah(nM18) mutants, with altered levels of octopamine and tyramine, have a locomotion deficit. By recording en passant from the segmental nerves, we investigated the coordination of the neuronal activity driving contraction waves of the abdominal body-wall muscles. Rhythmic bursts of activity that occurred concurrently with locomotive waves were frequently observed in wild-type larvae but were rarely seen in Tbetah(nM18) mutants. These centrally generated patterned activities were eliminated in the distal stumps of both wild-type and Tbetah(nM18) larvae after severing the segmental nerve from the CNS. Patterned activities persisted in the proximal stumps deprived of sensory feedback from the periphery. Simultaneous recordings demonstrated a delay in the bursting activity between different segments, with greater delay for segments that were farther apart. In contrast, bilateral recordings within a single segment revealed a well synchronized activity pattern in nerves innervating each hemisegment in both wild-type and Tbetah(nM18) larvae. Significantly, rhythmic patterns of bursts and waves could be evoked in Tbetah(nM18) mutants by head or tail stimulation despite their highly irregular spontaneous activities. These observations suggest a role of the biogenic amines in the initiation and modulation of motor pattern generation. The technique presented here can be readily extended to examine the locomotion motor program of other mutants. |
doi_str_mv | 10.1523/JNEUROSCI.4749-05.2006 |
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We present a systematic description of spike activity patterns during locomotive contraction waves in semi-intact wild-type and mutant larval preparations. We have shown previously that Tbetah(nM18) mutants, with altered levels of octopamine and tyramine, have a locomotion deficit. By recording en passant from the segmental nerves, we investigated the coordination of the neuronal activity driving contraction waves of the abdominal body-wall muscles. Rhythmic bursts of activity that occurred concurrently with locomotive waves were frequently observed in wild-type larvae but were rarely seen in Tbetah(nM18) mutants. These centrally generated patterned activities were eliminated in the distal stumps of both wild-type and Tbetah(nM18) larvae after severing the segmental nerve from the CNS. Patterned activities persisted in the proximal stumps deprived of sensory feedback from the periphery. Simultaneous recordings demonstrated a delay in the bursting activity between different segments, with greater delay for segments that were farther apart. In contrast, bilateral recordings within a single segment revealed a well synchronized activity pattern in nerves innervating each hemisegment in both wild-type and Tbetah(nM18) larvae. Significantly, rhythmic patterns of bursts and waves could be evoked in Tbetah(nM18) mutants by head or tail stimulation despite their highly irregular spontaneous activities. These observations suggest a role of the biogenic amines in the initiation and modulation of motor pattern generation. The technique presented here can be readily extended to examine the locomotion motor program of other mutants.</description><identifier>ISSN: 0270-6474</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.4749-05.2006</identifier><identifier>PMID: 16452672</identifier><language>eng</language><publisher>United States: Soc Neuroscience</publisher><subject>Abdominal Wall - innervation ; Abdominal Wall - physiology ; Action Potentials ; Animals ; Biogenic Amines - metabolism ; Central Nervous System - physiology ; Drosophila melanogaster ; Drosophila melanogaster - growth & development ; Drosophila melanogaster - metabolism ; Drosophila melanogaster - physiology ; Evoked Potentials ; Female ; Larva - physiology ; Locomotion - physiology ; Male ; Mixed Function Oxygenases - genetics ; Motor Activity - physiology ; Motor Neurons - physiology ; Muscle Contraction ; Mutation ; Neurons - physiology ; Neurons, Afferent - physiology ; Periodicity</subject><ispartof>The Journal of neuroscience, 2006-02, Vol.26 (5), p.1486-1498</ispartof><rights>Copyright © 2006 Society for Neuroscience 0270-6474/06/261486-13$15.00/0 2006</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c479t-d5577fc725d618a215575001be49b17d6224477bc4ce714a954cc0b3d25311e33</citedby><cites>FETCH-LOGICAL-c479t-d5577fc725d618a215575001be49b17d6224477bc4ce714a954cc0b3d25311e33</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/PMC2673197/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC2673197/$$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/16452672$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Fox, Lyle E</creatorcontrib><creatorcontrib>Soll, David R</creatorcontrib><creatorcontrib>Wu, Chun-Fang</creatorcontrib><title>Coordination and Modulation of Locomotion Pattern Generators in Drosophila Larvae: Effects of Altered Biogenic Amine Levels by the Tyramine beta Hydroxlyase Mutation</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>Forward locomotion of Drosophila melanogaster larvae is composed of rhythmic waves of contractions that are thought to be produced by segmentally organized central pattern generators. We present a systematic description of spike activity patterns during locomotive contraction waves in semi-intact wild-type and mutant larval preparations. We have shown previously that Tbetah(nM18) mutants, with altered levels of octopamine and tyramine, have a locomotion deficit. By recording en passant from the segmental nerves, we investigated the coordination of the neuronal activity driving contraction waves of the abdominal body-wall muscles. Rhythmic bursts of activity that occurred concurrently with locomotive waves were frequently observed in wild-type larvae but were rarely seen in Tbetah(nM18) mutants. These centrally generated patterned activities were eliminated in the distal stumps of both wild-type and Tbetah(nM18) larvae after severing the segmental nerve from the CNS. Patterned activities persisted in the proximal stumps deprived of sensory feedback from the periphery. Simultaneous recordings demonstrated a delay in the bursting activity between different segments, with greater delay for segments that were farther apart. In contrast, bilateral recordings within a single segment revealed a well synchronized activity pattern in nerves innervating each hemisegment in both wild-type and Tbetah(nM18) larvae. Significantly, rhythmic patterns of bursts and waves could be evoked in Tbetah(nM18) mutants by head or tail stimulation despite their highly irregular spontaneous activities. These observations suggest a role of the biogenic amines in the initiation and modulation of motor pattern generation. The technique presented here can be readily extended to examine the locomotion motor program of other mutants.</description><subject>Abdominal Wall - innervation</subject><subject>Abdominal Wall - physiology</subject><subject>Action Potentials</subject><subject>Animals</subject><subject>Biogenic Amines - metabolism</subject><subject>Central Nervous System - physiology</subject><subject>Drosophila melanogaster</subject><subject>Drosophila melanogaster - growth & development</subject><subject>Drosophila melanogaster - metabolism</subject><subject>Drosophila melanogaster - physiology</subject><subject>Evoked Potentials</subject><subject>Female</subject><subject>Larva - physiology</subject><subject>Locomotion - physiology</subject><subject>Male</subject><subject>Mixed Function Oxygenases - genetics</subject><subject>Motor Activity - physiology</subject><subject>Motor Neurons - physiology</subject><subject>Muscle Contraction</subject><subject>Mutation</subject><subject>Neurons - physiology</subject><subject>Neurons, Afferent - physiology</subject><subject>Periodicity</subject><issn>0270-6474</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2006</creationdate><recordtype>article</recordtype><recordid>eNqFUs1uEzEYXCEQDYVXqHzitsH2-ifLASmE0BalFEF7trzeb7NGu3ZqOwl5IN6TzY9aOHGyxt_MaPx5suyC4DHhtHj35ev8_vvtj9n1mElW5piPKcbiWTYapmVOGSbPsxGmEudiIJxlr2L8iTGWmMiX2RkRjFMh6Sj7PfM-1NbpZL1D2tXoxtfr7gh9gxbe-N4f0DedEgSHLsFB0MmHiKxDn4KPftXaTqOFDhsN79G8acCkuJdPu0ECNfpo_RKcNWjaWwdoARvoIqp2KLWA7nZBH64rSBpd7ergf3U7HQHdrNMhyevsRaO7CG9O53l2_3l-N7vKF7eX17PpIjdMlimvOZeyMZLyWpCJpmTAHGNSASsrImtBKWNSVoYZkITpkjNjcFXUlBeEQFGcZx-Ovqt11UNtwKWgO7UKttdhp7y26t-Js61a-o0allmQUg4Gb08GwT-sISbV22ig67QDv45KSEE5Kyb_JRLJRCEnfCCKI9EMi44Bmsc0BKt9FdRjFdS-Cgpzta_CILz4-y1PstPfP0Vo7bLd2gAq9rrrBjpR2-2WCsUVYRNR_AEP7cFp</recordid><startdate>20060201</startdate><enddate>20060201</enddate><creator>Fox, Lyle E</creator><creator>Soll, David R</creator><creator>Wu, Chun-Fang</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>7QG</scope><scope>7SS</scope><scope>7TK</scope><scope>7X8</scope><scope>5PM</scope></search><sort><creationdate>20060201</creationdate><title>Coordination and Modulation of Locomotion Pattern Generators in Drosophila Larvae: Effects of Altered Biogenic Amine Levels by the Tyramine beta Hydroxlyase Mutation</title><author>Fox, Lyle E ; Soll, David R ; Wu, Chun-Fang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c479t-d5577fc725d618a215575001be49b17d6224477bc4ce714a954cc0b3d25311e33</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2006</creationdate><topic>Abdominal Wall - innervation</topic><topic>Abdominal Wall - physiology</topic><topic>Action Potentials</topic><topic>Animals</topic><topic>Biogenic Amines - metabolism</topic><topic>Central Nervous System - physiology</topic><topic>Drosophila melanogaster</topic><topic>Drosophila melanogaster - growth & development</topic><topic>Drosophila melanogaster - metabolism</topic><topic>Drosophila melanogaster - physiology</topic><topic>Evoked Potentials</topic><topic>Female</topic><topic>Larva - physiology</topic><topic>Locomotion - physiology</topic><topic>Male</topic><topic>Mixed Function Oxygenases - genetics</topic><topic>Motor Activity - physiology</topic><topic>Motor Neurons - physiology</topic><topic>Muscle Contraction</topic><topic>Mutation</topic><topic>Neurons - physiology</topic><topic>Neurons, Afferent - physiology</topic><topic>Periodicity</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Fox, Lyle E</creatorcontrib><creatorcontrib>Soll, David R</creatorcontrib><creatorcontrib>Wu, Chun-Fang</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Animal Behavior Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Neurosciences Abstracts</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>Fox, Lyle E</au><au>Soll, David R</au><au>Wu, Chun-Fang</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Coordination and Modulation of Locomotion Pattern Generators in Drosophila Larvae: Effects of Altered Biogenic Amine Levels by the Tyramine beta Hydroxlyase Mutation</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2006-02-01</date><risdate>2006</risdate><volume>26</volume><issue>5</issue><spage>1486</spage><epage>1498</epage><pages>1486-1498</pages><issn>0270-6474</issn><eissn>1529-2401</eissn><abstract>Forward locomotion of Drosophila melanogaster larvae is composed of rhythmic waves of contractions that are thought to be produced by segmentally organized central pattern generators. We present a systematic description of spike activity patterns during locomotive contraction waves in semi-intact wild-type and mutant larval preparations. We have shown previously that Tbetah(nM18) mutants, with altered levels of octopamine and tyramine, have a locomotion deficit. By recording en passant from the segmental nerves, we investigated the coordination of the neuronal activity driving contraction waves of the abdominal body-wall muscles. Rhythmic bursts of activity that occurred concurrently with locomotive waves were frequently observed in wild-type larvae but were rarely seen in Tbetah(nM18) mutants. These centrally generated patterned activities were eliminated in the distal stumps of both wild-type and Tbetah(nM18) larvae after severing the segmental nerve from the CNS. Patterned activities persisted in the proximal stumps deprived of sensory feedback from the periphery. Simultaneous recordings demonstrated a delay in the bursting activity between different segments, with greater delay for segments that were farther apart. In contrast, bilateral recordings within a single segment revealed a well synchronized activity pattern in nerves innervating each hemisegment in both wild-type and Tbetah(nM18) larvae. Significantly, rhythmic patterns of bursts and waves could be evoked in Tbetah(nM18) mutants by head or tail stimulation despite their highly irregular spontaneous activities. These observations suggest a role of the biogenic amines in the initiation and modulation of motor pattern generation. The technique presented here can be readily extended to examine the locomotion motor program of other mutants.</abstract><cop>United States</cop><pub>Soc Neuroscience</pub><pmid>16452672</pmid><doi>10.1523/JNEUROSCI.4749-05.2006</doi><tpages>13</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Abdominal Wall - innervation Abdominal Wall - physiology Action Potentials Animals Biogenic Amines - metabolism Central Nervous System - physiology Drosophila melanogaster Drosophila melanogaster - growth & development Drosophila melanogaster - metabolism Drosophila melanogaster - physiology Evoked Potentials Female Larva - physiology Locomotion - physiology Male Mixed Function Oxygenases - genetics Motor Activity - physiology Motor Neurons - physiology Muscle Contraction Mutation Neurons - physiology Neurons, Afferent - physiology Periodicity |
title | Coordination and Modulation of Locomotion Pattern Generators in Drosophila Larvae: Effects of Altered Biogenic Amine Levels by the Tyramine beta Hydroxlyase Mutation |
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