Role of synchronous activation of cerebellar Purkinje cell ensembles in multi-joint movement control

It is a longstanding question in neuroscience how elaborate multi-joint movements are coordinated coherently. Microzones of cerebellar Purkinje cells (PCs) are thought to mediate this coordination by controlling the timing of particular motor domains. However, it remains to be elucidated to what ext...

Full description

Saved in:
Bibliographic Details
Published in:Current biology 2015-05, Vol.25 (9), p.1157-1165
Main Authors: Hoogland, Tycho M., De Gruijl, Jornt R., Witter, Laurens, Canto, Cathrin B., De Zeeuw, Chris I.
Format: Article
Language:eng
Subjects:
Online Access:Get full text
Tags: Add Tag
No Tags, Be the first to tag this record!
recordid cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4425462
title Role of synchronous activation of cerebellar Purkinje cell ensembles in multi-joint movement control
format Article
creator Hoogland, Tycho M.
De Gruijl, Jornt R.
Witter, Laurens
Canto, Cathrin B.
De Zeeuw, Chris I.
subjects Animals
Joints - physiology
Locomotion
Mice, Inbred C57BL
Motor Activity - physiology
Phenotype
Purkinje Cells - physiology
ispartof Current biology, 2015-05, Vol.25 (9), p.1157-1165
description It is a longstanding question in neuroscience how elaborate multi-joint movements are coordinated coherently. Microzones of cerebellar Purkinje cells (PCs) are thought to mediate this coordination by controlling the timing of particular motor domains. However, it remains to be elucidated to what extent motor coordination deficits can be correlated with abnormalities in coherent activity within these microzones and to what extent artificially evoked synchronous activity within PC-ensembles can elicit multi-joint motor behavior. To study PC ensemble correlates of limb, trunk and tail movements we developed a transparent disk-treadmill that allows quantitative read-out of locomotion and posture parameters in head-fixed mice and simultaneous cellular-resolution imaging and/or optogenetic manipulation. We show that PC ensembles in the ataxic and dystonic mouse mutant tottering have a reduced level of complex spike co-activation, which is delayed relative to movement onset and co-occurs with prolonged swing duration and reduced phase-coupling of limb movements as well as with enlarged deflections of body-axis and tail movements. Using optogenetics to increase simple spike rate in PC-ensembles, we find that preferred locomotion and posture patterns can be elicited or perturbed depending on the behavioral state. At rest, preferred sequences of limb movements can be elicited, whereas during locomotion preferred gait inhibition patterns are evoked. Our findings indicate that synchronous activation of PC-ensembles can facilitate initiation and coordination of limb and trunk movements, presumably by tuning downstream systems involved in the execution of behavioral patterns. -Tg/tg mice show affected swing duration and phase-coupling of limb movements.-PCs in ataxic tg/tg mice show delayed and reduced complex spike (CS) co-activation.-At rest, simple spike (SS) co-activation can elicit preferred locomotion sequences.-During locomotion, SS co-activation can be correlated with gait inhibition patterns.
language eng
source BACON - Elsevier - GLOBAL_SCIENCEDIRECT-OPENACCESS; Elsevier ScienceDirect Journals
identifier ISSN: 0960-9822
fulltext fulltext
issn 0960-9822
1879-0445
url http://sfxeu10.hosted.exlibrisgroup.com/loughborough?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2024-05-26T21%3A15%3A40IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-proquest_pubme&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Role%20of%20synchronous%20activation%20of%20cerebellar%20Purkinje%20cell%20ensembles%20in%20multi-joint%20movement%20control&rft.jtitle=Current%20biology&rft.au=Hoogland,%20Tycho%20M.&rft.date=2015-05-04&rft.volume=25&rft.issue=9&rft.spage=1157&rft.epage=1165&rft.pages=1157-1165&rft.issn=0960-9822&rft.eissn=1879-0445&rft_id=info:doi/10.1016/j.cub.2015.03.009&rft_dat=%3Cproquest_pubme%3E1837300200%3C/proquest_pubme%3E%3Cgrp_id%3Ecdi_FETCH-LOGICAL-c550t-fad2224d22b33f27dba3b9db3e9242381164778076686ae4db6cb6574cca62323%3C/grp_id%3E%3Coa%3E%3C/oa%3E%3Curl%3E%3C/url%3E&rft_id=info:oai/&rft_pqid=1680190148&rft_id=info:pmid/25843032
container_title Current biology
container_volume 25
container_issue 9
container_start_page 1157
container_end_page 1165
fullrecord <record><control><sourceid>proquest_pubme</sourceid><recordid>TN_cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_4425462</recordid><sourceformat>XML</sourceformat><sourcesystem>PC</sourcesystem><els_id>S0960982215003231</els_id><sourcerecordid>1837300200</sourcerecordid><originalsourceid>FETCH-LOGICAL-c550t-fad2224d22b33f27dba3b9db3e9242381164778076686ae4db6cb6574cca62323</originalsourceid><addsrcrecordid>eNqFkV2L1TAQhoso7nH1B3gjvfSmdfLRNEUQZFk_YEERvQ5JOnVT02RN2gP7700566I3ejMZMu-8zMxTVc8JtASIeDW3djMtBdK1wFqA4UF1ILIfGuC8e1gdYBDQDJLSs-pJzjMAoXIQj6sz2knOgNFDNX6JHus41fk22OsUQ9xyre3qjnp1MewViwkNeq9T_XlLP1yYsfx5X2PIuBiPuXahXja_umaOLqz1Eo-4YElsDGuK_mn1aNI-47O797z69u7y68WH5urT-48Xb68a23WwNpMeKaW8BMPYRPvRaGaG0TAcKKdMEiJ430vohZBCIx-NsEZ0PbdWC8ooO6_enHxvNrPgaMsISXt1k9yi062K2qm_K8Fdq-_xqDinHRe7wcs7gxR_bphXtbi876oDlsMoIlnPACjA_6VCAhmAcFmk5CS1KeaccLqfiIDaQapZFZBqB6mAqQKy9Lz4c5X7jt_kiuD1SYDloEeHSWXrMFgcXUK7qjG6f9j_AgJmsC8</addsrcrecordid><sourcetype>Open Access Repository</sourcetype><isCDI>true</isCDI><recordtype>article</recordtype><pqid>1680190148</pqid></control><display><type>article</type><title>Role of synchronous activation of cerebellar Purkinje cell ensembles in multi-joint movement control</title><source>BACON - Elsevier - GLOBAL_SCIENCEDIRECT-OPENACCESS</source><source>Elsevier ScienceDirect Journals</source><creator>Hoogland, Tycho M. ; De Gruijl, Jornt R. ; Witter, Laurens ; Canto, Cathrin B. ; De Zeeuw, Chris I.</creator><creatorcontrib>Hoogland, Tycho M. ; De Gruijl, Jornt R. ; Witter, Laurens ; Canto, Cathrin B. ; De Zeeuw, Chris I.</creatorcontrib><description>It is a longstanding question in neuroscience how elaborate multi-joint movements are coordinated coherently. Microzones of cerebellar Purkinje cells (PCs) are thought to mediate this coordination by controlling the timing of particular motor domains. However, it remains to be elucidated to what extent motor coordination deficits can be correlated with abnormalities in coherent activity within these microzones and to what extent artificially evoked synchronous activity within PC-ensembles can elicit multi-joint motor behavior. To study PC ensemble correlates of limb, trunk and tail movements we developed a transparent disk-treadmill that allows quantitative read-out of locomotion and posture parameters in head-fixed mice and simultaneous cellular-resolution imaging and/or optogenetic manipulation. We show that PC ensembles in the ataxic and dystonic mouse mutant tottering have a reduced level of complex spike co-activation, which is delayed relative to movement onset and co-occurs with prolonged swing duration and reduced phase-coupling of limb movements as well as with enlarged deflections of body-axis and tail movements. Using optogenetics to increase simple spike rate in PC-ensembles, we find that preferred locomotion and posture patterns can be elicited or perturbed depending on the behavioral state. At rest, preferred sequences of limb movements can be elicited, whereas during locomotion preferred gait inhibition patterns are evoked. Our findings indicate that synchronous activation of PC-ensembles can facilitate initiation and coordination of limb and trunk movements, presumably by tuning downstream systems involved in the execution of behavioral patterns. -Tg/tg mice show affected swing duration and phase-coupling of limb movements.-PCs in ataxic tg/tg mice show delayed and reduced complex spike (CS) co-activation.-At rest, simple spike (SS) co-activation can elicit preferred locomotion sequences.-During locomotion, SS co-activation can be correlated with gait inhibition patterns.</description><identifier>ISSN: 0960-9822</identifier><identifier>EISSN: 1879-0445</identifier><identifier>DOI: 10.1016/j.cub.2015.03.009</identifier><identifier>PMID: 25843032</identifier><language>eng</language><publisher>England: Elsevier Ltd</publisher><subject>Animals ; Joints - physiology ; Locomotion ; Mice, Inbred C57BL ; Motor Activity - physiology ; Phenotype ; Purkinje Cells - physiology</subject><ispartof>Current biology, 2015-05, Vol.25 (9), p.1157-1165</ispartof><rights>2015 Elsevier Ltd</rights><rights>Copyright © 2015 The Authors. Published by Elsevier Ltd.. All rights reserved.</rights><rights>2015 The Authors 2015</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c550t-fad2224d22b33f27dba3b9db3e9242381164778076686ae4db6cb6574cca62323</citedby><cites>FETCH-LOGICAL-c550t-fad2224d22b33f27dba3b9db3e9242381164778076686ae4db6cb6574cca62323</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0960982215003231$$EHTML$$P50$$Gelsevier$$Hfree_for_read</linktohtml><link.rule.ids>230,315,787,791,892,3569,27985,27986,46162</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/25843032$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Hoogland, Tycho M.</creatorcontrib><creatorcontrib>De Gruijl, Jornt R.</creatorcontrib><creatorcontrib>Witter, Laurens</creatorcontrib><creatorcontrib>Canto, Cathrin B.</creatorcontrib><creatorcontrib>De Zeeuw, Chris I.</creatorcontrib><title>Role of synchronous activation of cerebellar Purkinje cell ensembles in multi-joint movement control</title><title>Current biology</title><addtitle>Curr Biol</addtitle><description>It is a longstanding question in neuroscience how elaborate multi-joint movements are coordinated coherently. Microzones of cerebellar Purkinje cells (PCs) are thought to mediate this coordination by controlling the timing of particular motor domains. However, it remains to be elucidated to what extent motor coordination deficits can be correlated with abnormalities in coherent activity within these microzones and to what extent artificially evoked synchronous activity within PC-ensembles can elicit multi-joint motor behavior. To study PC ensemble correlates of limb, trunk and tail movements we developed a transparent disk-treadmill that allows quantitative read-out of locomotion and posture parameters in head-fixed mice and simultaneous cellular-resolution imaging and/or optogenetic manipulation. We show that PC ensembles in the ataxic and dystonic mouse mutant tottering have a reduced level of complex spike co-activation, which is delayed relative to movement onset and co-occurs with prolonged swing duration and reduced phase-coupling of limb movements as well as with enlarged deflections of body-axis and tail movements. Using optogenetics to increase simple spike rate in PC-ensembles, we find that preferred locomotion and posture patterns can be elicited or perturbed depending on the behavioral state. At rest, preferred sequences of limb movements can be elicited, whereas during locomotion preferred gait inhibition patterns are evoked. Our findings indicate that synchronous activation of PC-ensembles can facilitate initiation and coordination of limb and trunk movements, presumably by tuning downstream systems involved in the execution of behavioral patterns. -Tg/tg mice show affected swing duration and phase-coupling of limb movements.-PCs in ataxic tg/tg mice show delayed and reduced complex spike (CS) co-activation.-At rest, simple spike (SS) co-activation can elicit preferred locomotion sequences.-During locomotion, SS co-activation can be correlated with gait inhibition patterns.</description><subject>Animals</subject><subject>Joints - physiology</subject><subject>Locomotion</subject><subject>Mice, Inbred C57BL</subject><subject>Motor Activity - physiology</subject><subject>Phenotype</subject><subject>Purkinje Cells - physiology</subject><issn>0960-9822</issn><issn>1879-0445</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2015</creationdate><recordtype>article</recordtype><recordid>eNqFkV2L1TAQhoso7nH1B3gjvfSmdfLRNEUQZFk_YEERvQ5JOnVT02RN2gP7700566I3ejMZMu-8zMxTVc8JtASIeDW3djMtBdK1wFqA4UF1ILIfGuC8e1gdYBDQDJLSs-pJzjMAoXIQj6sz2knOgNFDNX6JHus41fk22OsUQ9xyre3qjnp1MewViwkNeq9T_XlLP1yYsfx5X2PIuBiPuXahXja_umaOLqz1Eo-4YElsDGuK_mn1aNI-47O797z69u7y68WH5urT-48Xb68a23WwNpMeKaW8BMPYRPvRaGaG0TAcKKdMEiJ430vohZBCIx-NsEZ0PbdWC8ooO6_enHxvNrPgaMsISXt1k9yi062K2qm_K8Fdq-_xqDinHRe7wcs7gxR_bphXtbi876oDlsMoIlnPACjA_6VCAhmAcFmk5CS1KeaccLqfiIDaQapZFZBqB6mAqQKy9Lz4c5X7jt_kiuD1SYDloEeHSWXrMFgcXUK7qjG6f9j_AgJmsC8</recordid><startdate>20150504</startdate><enddate>20150504</enddate><creator>Hoogland, Tycho M.</creator><creator>De Gruijl, Jornt R.</creator><creator>Witter, Laurens</creator><creator>Canto, Cathrin B.</creator><creator>De Zeeuw, Chris I.</creator><general>Elsevier Ltd</general><general>Cell Press</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>7X8</scope><scope>7TK</scope><scope>5PM</scope></search><sort><creationdate>20150504</creationdate><title>Role of synchronous activation of cerebellar Purkinje cell ensembles in multi-joint movement control</title><author>Hoogland, Tycho M. ; De Gruijl, Jornt R. ; Witter, Laurens ; Canto, Cathrin B. ; De Zeeuw, Chris I.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c550t-fad2224d22b33f27dba3b9db3e9242381164778076686ae4db6cb6574cca62323</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2015</creationdate><topic>Animals</topic><topic>Joints - physiology</topic><topic>Locomotion</topic><topic>Mice, Inbred C57BL</topic><topic>Motor Activity - physiology</topic><topic>Phenotype</topic><topic>Purkinje Cells - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Hoogland, Tycho M.</creatorcontrib><creatorcontrib>De Gruijl, Jornt R.</creatorcontrib><creatorcontrib>Witter, Laurens</creatorcontrib><creatorcontrib>Canto, Cathrin B.</creatorcontrib><creatorcontrib>De Zeeuw, Chris I.</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>MEDLINE - Academic</collection><collection>Neurosciences Abstracts</collection><collection>PubMed Central (Full Participant titles)</collection><jtitle>Current biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Hoogland, Tycho M.</au><au>De Gruijl, Jornt R.</au><au>Witter, Laurens</au><au>Canto, Cathrin B.</au><au>De Zeeuw, Chris I.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Role of synchronous activation of cerebellar Purkinje cell ensembles in multi-joint movement control</atitle><jtitle>Current biology</jtitle><addtitle>Curr Biol</addtitle><date>2015-05-04</date><risdate>2015</risdate><volume>25</volume><issue>9</issue><spage>1157</spage><epage>1165</epage><pages>1157-1165</pages><issn>0960-9822</issn><eissn>1879-0445</eissn><notes>ObjectType-Article-1</notes><notes>SourceType-Scholarly Journals-1</notes><notes>ObjectType-Feature-2</notes><notes>content type line 23</notes><notes>Co-first author</notes><abstract>It is a longstanding question in neuroscience how elaborate multi-joint movements are coordinated coherently. Microzones of cerebellar Purkinje cells (PCs) are thought to mediate this coordination by controlling the timing of particular motor domains. However, it remains to be elucidated to what extent motor coordination deficits can be correlated with abnormalities in coherent activity within these microzones and to what extent artificially evoked synchronous activity within PC-ensembles can elicit multi-joint motor behavior. To study PC ensemble correlates of limb, trunk and tail movements we developed a transparent disk-treadmill that allows quantitative read-out of locomotion and posture parameters in head-fixed mice and simultaneous cellular-resolution imaging and/or optogenetic manipulation. We show that PC ensembles in the ataxic and dystonic mouse mutant tottering have a reduced level of complex spike co-activation, which is delayed relative to movement onset and co-occurs with prolonged swing duration and reduced phase-coupling of limb movements as well as with enlarged deflections of body-axis and tail movements. Using optogenetics to increase simple spike rate in PC-ensembles, we find that preferred locomotion and posture patterns can be elicited or perturbed depending on the behavioral state. At rest, preferred sequences of limb movements can be elicited, whereas during locomotion preferred gait inhibition patterns are evoked. Our findings indicate that synchronous activation of PC-ensembles can facilitate initiation and coordination of limb and trunk movements, presumably by tuning downstream systems involved in the execution of behavioral patterns. -Tg/tg mice show affected swing duration and phase-coupling of limb movements.-PCs in ataxic tg/tg mice show delayed and reduced complex spike (CS) co-activation.-At rest, simple spike (SS) co-activation can elicit preferred locomotion sequences.-During locomotion, SS co-activation can be correlated with gait inhibition patterns.</abstract><cop>England</cop><pub>Elsevier Ltd</pub><pmid>25843032</pmid><doi>10.1016/j.cub.2015.03.009</doi><oa>free_for_read</oa></addata></record>