Hyperactivation of B-type motor neurons results in aberrant synchrony of the Caenorhabditis elegans motor circuit
Excitatory acetylcholine motor neurons drive Caenorhabditis elegans locomotion. Coordinating the activation states of the backward-driving A and forward-driving B class motor neurons is critical for generating sinusoidal and directional locomotion. Here, we show by in vivo calcium imaging that expre...
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| Veröffentlicht in: | The Journal of neuroscience 2013-03, Vol.33 (12), p.5319-5325 |
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| creator | Qi, Yingchuan B Po, Michelle D Mac, Patrick Kawano, Taizo Jorgensen, Erik M Zhen, Mei Jin, Yishi |
| description | Excitatory acetylcholine motor neurons drive Caenorhabditis elegans locomotion. Coordinating the activation states of the backward-driving A and forward-driving B class motor neurons is critical for generating sinusoidal and directional locomotion. Here, we show by in vivo calcium imaging that expression of a hyperactive, somatodendritic ionotropic acetylcholine receptor ACR-2(gf) in A and B class motor neurons induces aberrant synchronous activity in both ventral- and dorsal-innervating B and A class motor neurons. Expression of ACR-2(gf) in either ventral- or dorsal-innervating B neurons is sufficient for triggering the aberrant synchrony that results in arrhythmic convulsions. Silencing of AVB, the premotor interneurons that innervate B motor neurons suppresses ACR-2(gf)-dependent convulsion; activating AVB by channelrhodopsin induces the onset of convulsion. These results support that the activity state of B motor neurons plays an instructive role for the coordination of motor circuit. |
| doi_str_mv | 10.1523/JNEUROSCI.4017-12.2013 |
| format | Article |
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Coordinating the activation states of the backward-driving A and forward-driving B class motor neurons is critical for generating sinusoidal and directional locomotion. Here, we show by in vivo calcium imaging that expression of a hyperactive, somatodendritic ionotropic acetylcholine receptor ACR-2(gf) in A and B class motor neurons induces aberrant synchronous activity in both ventral- and dorsal-innervating B and A class motor neurons. Expression of ACR-2(gf) in either ventral- or dorsal-innervating B neurons is sufficient for triggering the aberrant synchrony that results in arrhythmic convulsions. Silencing of AVB, the premotor interneurons that innervate B motor neurons suppresses ACR-2(gf)-dependent convulsion; activating AVB by channelrhodopsin induces the onset of convulsion. These results support that the activity state of B motor neurons plays an instructive role for the coordination of motor circuit.</description><identifier>ISSN: 0270-6474</identifier><identifier>ISSN: 1529-2401</identifier><identifier>EISSN: 1529-2401</identifier><identifier>DOI: 10.1523/JNEUROSCI.4017-12.2013</identifier><identifier>PMID: 23516296</identifier><language>eng</language><publisher>United States: Society for Neuroscience</publisher><subject>Acetylcholine - physiology ; Animals ; Animals, Genetically Modified ; Brief Communications ; Caenorhabditis elegans ; Caenorhabditis elegans - genetics ; Caenorhabditis elegans - physiology ; Caenorhabditis elegans Proteins - genetics ; Caenorhabditis elegans Proteins - physiology ; Cholinergic Neurons - physiology ; Dendrites - physiology ; Efferent Pathways - cytology ; Efferent Pathways - physiology ; Gene Expression - physiology ; Interneurons - physiology ; Locomotion - physiology ; Motor Neurons - physiology ; Nerve Tissue Proteins - genetics ; Nerve Tissue Proteins - metabolism ; Receptors, Nicotinic - genetics ; Receptors, Nicotinic - physiology ; Seizures - genetics ; Seizures - physiopathology</subject><ispartof>The Journal of neuroscience, 2013-03, Vol.33 (12), p.5319-5325</ispartof><rights>Copyright © 2013 the authors 0270-6474/13/335319-07$15.00/0 2013</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c469t-7866d59390ade765560efbd788497672f50fc1d5336ed3884676448bf49719b3</citedby><cites>FETCH-LOGICAL-c469t-7866d59390ade765560efbd788497672f50fc1d5336ed3884676448bf49719b3</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/PMC3655201/pdf/$$EPDF$$P50$$Gpubmedcentral$$H</linktopdf><linktohtml>$$Uhttps://www.ncbi.nlm.nih.gov/pmc/articles/PMC3655201/$$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/23516296$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Qi, Yingchuan B</creatorcontrib><creatorcontrib>Po, Michelle D</creatorcontrib><creatorcontrib>Mac, Patrick</creatorcontrib><creatorcontrib>Kawano, Taizo</creatorcontrib><creatorcontrib>Jorgensen, Erik M</creatorcontrib><creatorcontrib>Zhen, Mei</creatorcontrib><creatorcontrib>Jin, Yishi</creatorcontrib><title>Hyperactivation of B-type motor neurons results in aberrant synchrony of the Caenorhabditis elegans motor circuit</title><title>The Journal of neuroscience</title><addtitle>J Neurosci</addtitle><description>Excitatory acetylcholine motor neurons drive Caenorhabditis elegans locomotion. Coordinating the activation states of the backward-driving A and forward-driving B class motor neurons is critical for generating sinusoidal and directional locomotion. Here, we show by in vivo calcium imaging that expression of a hyperactive, somatodendritic ionotropic acetylcholine receptor ACR-2(gf) in A and B class motor neurons induces aberrant synchronous activity in both ventral- and dorsal-innervating B and A class motor neurons. Expression of ACR-2(gf) in either ventral- or dorsal-innervating B neurons is sufficient for triggering the aberrant synchrony that results in arrhythmic convulsions. Silencing of AVB, the premotor interneurons that innervate B motor neurons suppresses ACR-2(gf)-dependent convulsion; activating AVB by channelrhodopsin induces the onset of convulsion. These results support that the activity state of B motor neurons plays an instructive role for the coordination of motor circuit.</description><subject>Acetylcholine - physiology</subject><subject>Animals</subject><subject>Animals, Genetically Modified</subject><subject>Brief Communications</subject><subject>Caenorhabditis elegans</subject><subject>Caenorhabditis elegans - genetics</subject><subject>Caenorhabditis elegans - physiology</subject><subject>Caenorhabditis elegans Proteins - genetics</subject><subject>Caenorhabditis elegans Proteins - physiology</subject><subject>Cholinergic Neurons - physiology</subject><subject>Dendrites - physiology</subject><subject>Efferent Pathways - cytology</subject><subject>Efferent Pathways - physiology</subject><subject>Gene Expression - physiology</subject><subject>Interneurons - physiology</subject><subject>Locomotion - physiology</subject><subject>Motor Neurons - physiology</subject><subject>Nerve Tissue Proteins - genetics</subject><subject>Nerve Tissue Proteins - metabolism</subject><subject>Receptors, Nicotinic - genetics</subject><subject>Receptors, Nicotinic - physiology</subject><subject>Seizures - genetics</subject><subject>Seizures - physiopathology</subject><issn>0270-6474</issn><issn>1529-2401</issn><issn>1529-2401</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNpVUU1rFDEYDqLY7epfKDl6mW2-s3MRdKm2UlrQeg6ZzDvdyGyyTTKF_fdm2LrYU-D5DO-D0AUlKyoZv_xxd_X75_2vzc1KEKobylaMUP4GLSrbNqyCb9GCME0aJbQ4Q-c5_yGE6Cp-j84Yl1SxVi3Q0_VhD8m64p9t8THgOOCvTakg3sUSEw4wpRgyTpCnsWTsA7YdpGRDwfkQ3Layh9lVtoA3FkJMW9v1vviMYYRHW73HJOeTm3z5gN4Ndszw8eVdoodvVw-b6-b2_vvN5stt44RqS6PXSvWy5S2xPWglpSIwdL1er0WrlWaDJIOjveRcQc8rqrQSYt0NlaZtx5fo8zF2P3U76B2Ekuxo9snvbDqYaL15zQS_NY_x2fDaNd9yiT69BKT4NEEuZuezg3G0AeKUDZXzDYmQokrVUepSzDnBcKqhxMxzmdNcZp7LUGbmimq8-P-TJ9u_ffhfjBCUpg</recordid><startdate>20130320</startdate><enddate>20130320</enddate><creator>Qi, Yingchuan B</creator><creator>Po, Michelle D</creator><creator>Mac, Patrick</creator><creator>Kawano, Taizo</creator><creator>Jorgensen, Erik M</creator><creator>Zhen, Mei</creator><creator>Jin, Yishi</creator><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>7TK</scope><scope>5PM</scope></search><sort><creationdate>20130320</creationdate><title>Hyperactivation of B-type motor neurons results in aberrant synchrony of the Caenorhabditis elegans motor circuit</title><author>Qi, Yingchuan B ; Po, Michelle D ; Mac, Patrick ; Kawano, Taizo ; Jorgensen, Erik M ; Zhen, Mei ; Jin, Yishi</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c469t-7866d59390ade765560efbd788497672f50fc1d5336ed3884676448bf49719b3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Acetylcholine - physiology</topic><topic>Animals</topic><topic>Animals, Genetically Modified</topic><topic>Brief Communications</topic><topic>Caenorhabditis elegans</topic><topic>Caenorhabditis elegans - genetics</topic><topic>Caenorhabditis elegans - physiology</topic><topic>Caenorhabditis elegans Proteins - genetics</topic><topic>Caenorhabditis elegans Proteins - physiology</topic><topic>Cholinergic Neurons - physiology</topic><topic>Dendrites - physiology</topic><topic>Efferent Pathways - cytology</topic><topic>Efferent Pathways - physiology</topic><topic>Gene Expression - physiology</topic><topic>Interneurons - physiology</topic><topic>Locomotion - physiology</topic><topic>Motor Neurons - physiology</topic><topic>Nerve Tissue Proteins - genetics</topic><topic>Nerve Tissue Proteins - metabolism</topic><topic>Receptors, Nicotinic - genetics</topic><topic>Receptors, Nicotinic - physiology</topic><topic>Seizures - genetics</topic><topic>Seizures - physiopathology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Qi, Yingchuan B</creatorcontrib><creatorcontrib>Po, Michelle D</creatorcontrib><creatorcontrib>Mac, Patrick</creatorcontrib><creatorcontrib>Kawano, Taizo</creatorcontrib><creatorcontrib>Jorgensen, Erik M</creatorcontrib><creatorcontrib>Zhen, Mei</creatorcontrib><creatorcontrib>Jin, Yishi</creatorcontrib><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>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>Qi, Yingchuan B</au><au>Po, Michelle D</au><au>Mac, Patrick</au><au>Kawano, Taizo</au><au>Jorgensen, Erik M</au><au>Zhen, Mei</au><au>Jin, Yishi</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Hyperactivation of B-type motor neurons results in aberrant synchrony of the Caenorhabditis elegans motor circuit</atitle><jtitle>The Journal of neuroscience</jtitle><addtitle>J Neurosci</addtitle><date>2013-03-20</date><risdate>2013</risdate><volume>33</volume><issue>12</issue><spage>5319</spage><epage>5325</epage><pages>5319-5325</pages><issn>0270-6474</issn><issn>1529-2401</issn><eissn>1529-2401</eissn><abstract>Excitatory acetylcholine motor neurons drive Caenorhabditis elegans locomotion. Coordinating the activation states of the backward-driving A and forward-driving B class motor neurons is critical for generating sinusoidal and directional locomotion. Here, we show by in vivo calcium imaging that expression of a hyperactive, somatodendritic ionotropic acetylcholine receptor ACR-2(gf) in A and B class motor neurons induces aberrant synchronous activity in both ventral- and dorsal-innervating B and A class motor neurons. Expression of ACR-2(gf) in either ventral- or dorsal-innervating B neurons is sufficient for triggering the aberrant synchrony that results in arrhythmic convulsions. Silencing of AVB, the premotor interneurons that innervate B motor neurons suppresses ACR-2(gf)-dependent convulsion; activating AVB by channelrhodopsin induces the onset of convulsion. 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| subjects | Acetylcholine - physiology Animals Animals, Genetically Modified Brief Communications Caenorhabditis elegans Caenorhabditis elegans - genetics Caenorhabditis elegans - physiology Caenorhabditis elegans Proteins - genetics Caenorhabditis elegans Proteins - physiology Cholinergic Neurons - physiology Dendrites - physiology Efferent Pathways - cytology Efferent Pathways - physiology Gene Expression - physiology Interneurons - physiology Locomotion - physiology Motor Neurons - physiology Nerve Tissue Proteins - genetics Nerve Tissue Proteins - metabolism Receptors, Nicotinic - genetics Receptors, Nicotinic - physiology Seizures - genetics Seizures - physiopathology |
| title | Hyperactivation of B-type motor neurons results in aberrant synchrony of the Caenorhabditis elegans motor circuit |
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