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Separate Microcircuit Modules of Distinct V2a Interneurons and Motoneurons Control the Speed of Locomotion
Spinal circuits generate locomotion with variable speed as circumstances demand. These circuits have been assumed to convey equal and uniform excitation to all motoneurons whose input resistance dictates their activation sequence. However, the precise connectivity pattern between excitatory premotor...
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Published in: | Neuron (Cambridge, Mass.) Mass.), 2014-08, Vol.83 (4), p.934-943 |
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creator | Ampatzis, Konstantinos Song, Jianren Ausborn, Jessica El Manira, Abdeljabbar |
description | Spinal circuits generate locomotion with variable speed as circumstances demand. These circuits have been assumed to convey equal and uniform excitation to all motoneurons whose input resistance dictates their activation sequence. However, the precise connectivity pattern between excitatory premotor circuits and the different motoneuron types has remained unclear. Here, we generate a connectivity map in adult zebrafish between the V2a excitatory interneurons and slow, intermediate, and fast motoneurons. We show that the locomotor network does not consist of a uniform circuit as previously assumed. Instead, it can be deconstructed into three separate microcircuit modules with distinct V2a interneuron subclasses driving slow, intermediate, or fast motoneurons. This modular design enables the increase of locomotor speed by sequentially adding microcircuit layers from slow to intermediate and fast. Thus, this principle of organization of vertebrate spinal circuits represents an intrinsic mechanism to increase the locomotor speed by incrementally engaging different motor units.
•Locomotor networks are deconstructed into three distinct microcircuit modules•In each module, distinct V2a interneurons drive slow, intermediate, or fast motoneurons•The modular organization reflects the properties and activation order of motor units•Slow, intermediate, and fast modules are sequentially engaged to increase speed
Ampatzis et al. uncover an organization of the locomotor network that endows the spinal cord with an intrinsic gearshift to increase speed of locomotion by sequentially engaging three separate microcircuits, and hence gradually recruiting slow, intermediate, and fast motor units. |
doi_str_mv | 10.1016/j.neuron.2014.07.018 |
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•Locomotor networks are deconstructed into three distinct microcircuit modules•In each module, distinct V2a interneurons drive slow, intermediate, or fast motoneurons•The modular organization reflects the properties and activation order of motor units•Slow, intermediate, and fast modules are sequentially engaged to increase speed
Ampatzis et al. uncover an organization of the locomotor network that endows the spinal cord with an intrinsic gearshift to increase speed of locomotion by sequentially engaging three separate microcircuits, and hence gradually recruiting slow, intermediate, and fast motor units.</description><identifier>ISSN: 0896-6273</identifier><identifier>ISSN: 1097-4199</identifier><identifier>EISSN: 1097-4199</identifier><identifier>DOI: 10.1016/j.neuron.2014.07.018</identifier><identifier>PMID: 25123308</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>Acceleration ; Action Potentials - physiology ; Animals ; Circuits ; Danio rerio ; Interneurons - physiology ; Locomotion - physiology ; Medicin och hälsovetenskap ; Motor Neurons - physiology ; Nerve Net - cytology ; Nerve Net - physiology ; Recruitment ; Rodents ; Software ; Spinal cord ; Spinal Cord - cytology ; Spinal Cord - physiology ; Zebrafish</subject><ispartof>Neuron (Cambridge, Mass.), 2014-08, Vol.83 (4), p.934-943</ispartof><rights>2014 Elsevier Inc.</rights><rights>Copyright © 2014 Elsevier Inc. All rights reserved.</rights><rights>Copyright Elsevier Limited Aug 20, 2014</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c693t-384bfef345d26b2439cfe693f9689cdcba31e30631fc1098f6860c507d59402a3</citedby><cites>FETCH-LOGICAL-c693t-384bfef345d26b2439cfe693f9689cdcba31e30631fc1098f6860c507d59402a3</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><link.rule.ids>230,314,780,784,885,27924,27925</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25123308$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink><backlink>$$Uhttp://kipublications.ki.se/Default.aspx?queryparsed=id:129589170$$DView record from Swedish Publication Index$$Hfree_for_read</backlink></links><search><creatorcontrib>Ampatzis, Konstantinos</creatorcontrib><creatorcontrib>Song, Jianren</creatorcontrib><creatorcontrib>Ausborn, Jessica</creatorcontrib><creatorcontrib>El Manira, Abdeljabbar</creatorcontrib><title>Separate Microcircuit Modules of Distinct V2a Interneurons and Motoneurons Control the Speed of Locomotion</title><title>Neuron (Cambridge, Mass.)</title><addtitle>Neuron</addtitle><description>Spinal circuits generate locomotion with variable speed as circumstances demand. These circuits have been assumed to convey equal and uniform excitation to all motoneurons whose input resistance dictates their activation sequence. However, the precise connectivity pattern between excitatory premotor circuits and the different motoneuron types has remained unclear. Here, we generate a connectivity map in adult zebrafish between the V2a excitatory interneurons and slow, intermediate, and fast motoneurons. We show that the locomotor network does not consist of a uniform circuit as previously assumed. Instead, it can be deconstructed into three separate microcircuit modules with distinct V2a interneuron subclasses driving slow, intermediate, or fast motoneurons. This modular design enables the increase of locomotor speed by sequentially adding microcircuit layers from slow to intermediate and fast. Thus, this principle of organization of vertebrate spinal circuits represents an intrinsic mechanism to increase the locomotor speed by incrementally engaging different motor units.
•Locomotor networks are deconstructed into three distinct microcircuit modules•In each module, distinct V2a interneurons drive slow, intermediate, or fast motoneurons•The modular organization reflects the properties and activation order of motor units•Slow, intermediate, and fast modules are sequentially engaged to increase speed
Ampatzis et al. uncover an organization of the locomotor network that endows the spinal cord with an intrinsic gearshift to increase speed of locomotion by sequentially engaging three separate microcircuits, and hence gradually recruiting slow, intermediate, and fast motor units.</description><subject>Acceleration</subject><subject>Action Potentials - physiology</subject><subject>Animals</subject><subject>Circuits</subject><subject>Danio rerio</subject><subject>Interneurons - physiology</subject><subject>Locomotion - physiology</subject><subject>Medicin och hälsovetenskap</subject><subject>Motor Neurons - physiology</subject><subject>Nerve Net - cytology</subject><subject>Nerve Net - physiology</subject><subject>Recruitment</subject><subject>Rodents</subject><subject>Software</subject><subject>Spinal cord</subject><subject>Spinal Cord - cytology</subject><subject>Spinal Cord - physiology</subject><subject>Zebrafish</subject><issn>0896-6273</issn><issn>1097-4199</issn><issn>1097-4199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2014</creationdate><recordtype>article</recordtype><recordid>eNqNkk2v1CAUhonReMer_8CYJm7ctEIptGxMzPh1k7lxcdUtoXAaqR2oQDX-e6mduSYmGlfA4XnPOXBehB4TXBFM-POxcrAE76oak6bCbYVJdwftCBZt2RAh7qId7gQved3SC_QgxhFnkAlyH13UjNSU4m6HxhuYVVAJimurg9c26MWm4tqbZYJY-KF4ZWOyTqfiU62KK5cgbHVjoZzJYPLn8967FPxUpM9Q3MwAZpUfvPZHn6x3D9G9QU0RHp3WS_TxzesP-3fl4f3bq_3LQ6m5oKmkXdMPMNCGmZr3dUOFHiDfDIJ3QhvdK0qAYk7JoPNju4F3HGuGW8NEg2tFL1G55Y3fYV56OQd7VOGH9MrKU-hL3oFkRDBBMy_-ys_Bm9-is5DUgnWCtDhrn23aDH5dICZ5tFHDNCkHfomSMM67piOc_wfKGK8xxWtHT_9AR78Elz_tF4Up4XSlmo3Kc4sxwHDbOcFytYgc5TYauVpE4lZmi2TZk1PypT-CuRWdPZGBFxsAeUjfLAQZtQWnwdgAOknj7b8r_AQLQs-4</recordid><startdate>20140820</startdate><enddate>20140820</enddate><creator>Ampatzis, Konstantinos</creator><creator>Song, Jianren</creator><creator>Ausborn, Jessica</creator><creator>El Manira, Abdeljabbar</creator><general>Elsevier Inc</general><general>Elsevier Limited</general><scope>6I.</scope><scope>AAFTH</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>7QP</scope><scope>7QR</scope><scope>7TK</scope><scope>8FD</scope><scope>FR3</scope><scope>K9.</scope><scope>NAPCQ</scope><scope>P64</scope><scope>RC3</scope><scope>7X8</scope><scope>ADTPV</scope><scope>AOWAS</scope><scope>D8T</scope><scope>ZZAVC</scope></search><sort><creationdate>20140820</creationdate><title>Separate Microcircuit Modules of Distinct V2a Interneurons and Motoneurons Control the Speed of Locomotion</title><author>Ampatzis, Konstantinos ; Song, Jianren ; Ausborn, Jessica ; El Manira, Abdeljabbar</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c693t-384bfef345d26b2439cfe693f9689cdcba31e30631fc1098f6860c507d59402a3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2014</creationdate><topic>Acceleration</topic><topic>Action Potentials - physiology</topic><topic>Animals</topic><topic>Circuits</topic><topic>Danio rerio</topic><topic>Interneurons - physiology</topic><topic>Locomotion - physiology</topic><topic>Medicin och hälsovetenskap</topic><topic>Motor Neurons - physiology</topic><topic>Nerve Net - cytology</topic><topic>Nerve Net - physiology</topic><topic>Recruitment</topic><topic>Rodents</topic><topic>Software</topic><topic>Spinal cord</topic><topic>Spinal Cord - cytology</topic><topic>Spinal Cord - physiology</topic><topic>Zebrafish</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Ampatzis, Konstantinos</creatorcontrib><creatorcontrib>Song, Jianren</creatorcontrib><creatorcontrib>Ausborn, Jessica</creatorcontrib><creatorcontrib>El Manira, Abdeljabbar</creatorcontrib><collection>ScienceDirect Open Access Titles</collection><collection>Elsevier:ScienceDirect:Open Access</collection><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Technology Research Database</collection><collection>Engineering Research Database</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Nursing & Allied Health Premium</collection><collection>Biotechnology and BioEngineering Abstracts</collection><collection>Genetics Abstracts</collection><collection>MEDLINE - Academic</collection><collection>SwePub</collection><collection>SwePub Articles</collection><collection>SWEPUB Freely available online</collection><collection>SwePub Articles full text</collection><jtitle>Neuron (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Ampatzis, Konstantinos</au><au>Song, Jianren</au><au>Ausborn, Jessica</au><au>El Manira, Abdeljabbar</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Separate Microcircuit Modules of Distinct V2a Interneurons and Motoneurons Control the Speed of Locomotion</atitle><jtitle>Neuron (Cambridge, Mass.)</jtitle><addtitle>Neuron</addtitle><date>2014-08-20</date><risdate>2014</risdate><volume>83</volume><issue>4</issue><spage>934</spage><epage>943</epage><pages>934-943</pages><issn>0896-6273</issn><issn>1097-4199</issn><eissn>1097-4199</eissn><abstract>Spinal circuits generate locomotion with variable speed as circumstances demand. These circuits have been assumed to convey equal and uniform excitation to all motoneurons whose input resistance dictates their activation sequence. However, the precise connectivity pattern between excitatory premotor circuits and the different motoneuron types has remained unclear. Here, we generate a connectivity map in adult zebrafish between the V2a excitatory interneurons and slow, intermediate, and fast motoneurons. We show that the locomotor network does not consist of a uniform circuit as previously assumed. Instead, it can be deconstructed into three separate microcircuit modules with distinct V2a interneuron subclasses driving slow, intermediate, or fast motoneurons. This modular design enables the increase of locomotor speed by sequentially adding microcircuit layers from slow to intermediate and fast. Thus, this principle of organization of vertebrate spinal circuits represents an intrinsic mechanism to increase the locomotor speed by incrementally engaging different motor units.
•Locomotor networks are deconstructed into three distinct microcircuit modules•In each module, distinct V2a interneurons drive slow, intermediate, or fast motoneurons•The modular organization reflects the properties and activation order of motor units•Slow, intermediate, and fast modules are sequentially engaged to increase speed
Ampatzis et al. uncover an organization of the locomotor network that endows the spinal cord with an intrinsic gearshift to increase speed of locomotion by sequentially engaging three separate microcircuits, and hence gradually recruiting slow, intermediate, and fast motor units.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>25123308</pmid><doi>10.1016/j.neuron.2014.07.018</doi><tpages>10</tpages><oa>free_for_read</oa></addata></record> |
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subjects | Acceleration Action Potentials - physiology Animals Circuits Danio rerio Interneurons - physiology Locomotion - physiology Medicin och hälsovetenskap Motor Neurons - physiology Nerve Net - cytology Nerve Net - physiology Recruitment Rodents Software Spinal cord Spinal Cord - cytology Spinal Cord - physiology Zebrafish |
title | Separate Microcircuit Modules of Distinct V2a Interneurons and Motoneurons Control the Speed of Locomotion |
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