Emergence of reproducible spatiotemporal activity during motor learning
Inhibitory neuron activity is found to be relatively stable during motor learning whereas excitatory neuron activity is much more dynamic — the results indicate that a large number of neurons exhibit activity changes early on during motor learning, but this population is refined with subsequent prac...
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description | Inhibitory neuron activity is found to be relatively stable during motor learning whereas excitatory neuron activity is much more dynamic — the results indicate that a large number of neurons exhibit activity changes early on during motor learning, but this population is refined with subsequent practice.
Motor cortex change during learning
How the brain learns to make adaptive body movements is a central question in systems neuroscience. Motor learning is thought to drive dramatic plasticity in motor circuits, but the extent of this plasticity in large neuronal populations is unclear. Takaki Komiyama and colleagues used techniques including a genetically encoded calcium indicator and chronic
in vivo
two-photon imaging in the motor cortex during a two-week forelimb motor learning task in mice, and found that inhibitory neuron activity is relatively stable during motor learning while excitatory neuron plasticity is much more dynamic. The results indicate that a large number of neurons exhibit activity level changes early on during motor learning, but this population is refined with subsequent practice.
The motor cortex is capable of reliably driving complex movements
1
,
2
yet exhibits considerable plasticity during motor learning
3
,
4
,
5
,
6
,
7
,
8
,
9
,
10
. These observations suggest that the fundamental relationship between motor cortex activity and movement may not be fixed but is instead shaped by learning; however, to what extent and how motor learning shapes this relationship are not fully understood. Here we addressed this issue by using
in vivo
two-photon calcium imaging
11
to monitor the activity of the same population of hundreds of layer 2/3 neurons while mice learned a forelimb lever-press task over two weeks. Excitatory and inhibitory neurons were identified by transgenic labelling
12
,
13
. Inhibitory neuron activity was relatively stable and balanced local excitatory neuron activity on a movement-by-movement basis, whereas excitatory neuron activity showed higher dynamism during the initial phase of learning. The dynamics of excitatory neurons during the initial phase involved the expansion of the movement-related population which explored various activity patterns even during similar movements. This was followed by a refinement into a smaller population exhibiting reproducible spatiotemporal sequences of activity. This pattern of activity associated with the learned movement was unique to expert animals and not observed during similar mo |
doi_str_mv | 10.1038/nature13235 |
format | Article |
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Motor cortex change during learning
How the brain learns to make adaptive body movements is a central question in systems neuroscience. Motor learning is thought to drive dramatic plasticity in motor circuits, but the extent of this plasticity in large neuronal populations is unclear. Takaki Komiyama and colleagues used techniques including a genetically encoded calcium indicator and chronic
in vivo
two-photon imaging in the motor cortex during a two-week forelimb motor learning task in mice, and found that inhibitory neuron activity is relatively stable during motor learning while excitatory neuron plasticity is much more dynamic. The results indicate that a large number of neurons exhibit activity level changes early on during motor learning, but this population is refined with subsequent practice.
The motor cortex is capable of reliably driving complex movements
1
,
2
yet exhibits considerable plasticity during motor learning
3
,
4
,
5
,
6
,
7
,
8
,
9
,
10
. These observations suggest that the fundamental relationship between motor cortex activity and movement may not be fixed but is instead shaped by learning; however, to what extent and how motor learning shapes this relationship are not fully understood. Here we addressed this issue by using
in vivo
two-photon calcium imaging
11
to monitor the activity of the same population of hundreds of layer 2/3 neurons while mice learned a forelimb lever-press task over two weeks. Excitatory and inhibitory neurons were identified by transgenic labelling
12
,
13
. Inhibitory neuron activity was relatively stable and balanced local excitatory neuron activity on a movement-by-movement basis, whereas excitatory neuron activity showed higher dynamism during the initial phase of learning. The dynamics of excitatory neurons during the initial phase involved the expansion of the movement-related population which explored various activity patterns even during similar movements. This was followed by a refinement into a smaller population exhibiting reproducible spatiotemporal sequences of activity. This pattern of activity associated with the learned movement was unique to expert animals and not observed during similar movements made during the naive phase, and the relationship between neuronal activity and individual movements became more consistent with learning. These changes in population activity coincided with a transient increase in dendritic spine turnover in these neurons. Our results indicate that a novel and reproducible activity–movement relationship develops as a result of motor learning, and we speculate that synaptic plasticity within the motor cortex underlies the emergence of reproducible spatiotemporal activity patterns for learned movements. These results underscore the profound influence of learning on the way that the cortex produces movements.</description><identifier>ISSN: 0028-0836</identifier><identifier>EISSN: 1476-4687</identifier><identifier>DOI: 10.1038/nature13235</identifier><identifier>PMID: 24805237</identifier><identifier>CODEN: NATUAS</identifier><language>eng</language><publisher>London: Nature Publishing Group UK</publisher><subject>14 ; 14/35 ; 14/69 ; 631/378/1595/2618 ; 631/378/2597/2599 ; 631/378/2632/1663 ; 64/60 ; 9/74 ; Animals ; Brain ; Calcium - metabolism ; Dendritic Spines - physiology ; Female ; Forelimb - physiology ; Humanities and Social Sciences ; Learning ; Learning - physiology ; letter ; Male ; Mice ; Models, Neurological ; Motor ability ; Motor cortex ; Motor Cortex - physiology ; Motor learning ; Motor Skills - physiology ; multidisciplinary ; Neural Inhibition ; Neuronal Plasticity - physiology ; Neurons ; Physiological aspects ; Physiological research ; Plasticity ; Reproducibility of Results ; Science ; Spatio-Temporal Analysis ; Spine</subject><ispartof>Nature (London), 2014-06, Vol.510 (7504), p.263-267</ispartof><rights>Springer Nature Limited 2014</rights><rights>COPYRIGHT 2014 Nature Publishing Group</rights><rights>Copyright Nature Publishing Group Jun 12, 2014</rights><lds50>peer_reviewed</lds50><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c520t-c6c41f984e97dd4bee83234c45b3e0d50548aae208127a4a9e8f108deb1f30b93</citedby><cites>FETCH-LOGICAL-c520t-c6c41f984e97dd4bee83234c45b3e0d50548aae208127a4a9e8f108deb1f30b93</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktopdf>$$Uhttps://link.springer.com/content/pdf/10.1038/nature13235$$EPDF$$P50$$Gspringer$$H</linktopdf><linktohtml>$$Uhttps://link.springer.com/10.1038/nature13235$$EHTML$$P50$$Gspringer$$H</linktohtml><link.rule.ids>314,776,780,27901,27902,41464,42533,51294</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/24805237$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Peters, Andrew J.</creatorcontrib><creatorcontrib>Chen, Simon X.</creatorcontrib><creatorcontrib>Komiyama, Takaki</creatorcontrib><title>Emergence of reproducible spatiotemporal activity during motor learning</title><title>Nature (London)</title><addtitle>Nature</addtitle><addtitle>Nature</addtitle><description>Inhibitory neuron activity is found to be relatively stable during motor learning whereas excitatory neuron activity is much more dynamic — the results indicate that a large number of neurons exhibit activity changes early on during motor learning, but this population is refined with subsequent practice.
Motor cortex change during learning
How the brain learns to make adaptive body movements is a central question in systems neuroscience. Motor learning is thought to drive dramatic plasticity in motor circuits, but the extent of this plasticity in large neuronal populations is unclear. Takaki Komiyama and colleagues used techniques including a genetically encoded calcium indicator and chronic
in vivo
two-photon imaging in the motor cortex during a two-week forelimb motor learning task in mice, and found that inhibitory neuron activity is relatively stable during motor learning while excitatory neuron plasticity is much more dynamic. The results indicate that a large number of neurons exhibit activity level changes early on during motor learning, but this population is refined with subsequent practice.
The motor cortex is capable of reliably driving complex movements
1
,
2
yet exhibits considerable plasticity during motor learning
3
,
4
,
5
,
6
,
7
,
8
,
9
,
10
. These observations suggest that the fundamental relationship between motor cortex activity and movement may not be fixed but is instead shaped by learning; however, to what extent and how motor learning shapes this relationship are not fully understood. Here we addressed this issue by using
in vivo
two-photon calcium imaging
11
to monitor the activity of the same population of hundreds of layer 2/3 neurons while mice learned a forelimb lever-press task over two weeks. Excitatory and inhibitory neurons were identified by transgenic labelling
12
,
13
. Inhibitory neuron activity was relatively stable and balanced local excitatory neuron activity on a movement-by-movement basis, whereas excitatory neuron activity showed higher dynamism during the initial phase of learning. The dynamics of excitatory neurons during the initial phase involved the expansion of the movement-related population which explored various activity patterns even during similar movements. This was followed by a refinement into a smaller population exhibiting reproducible spatiotemporal sequences of activity. This pattern of activity associated with the learned movement was unique to expert animals and not observed during similar movements made during the naive phase, and the relationship between neuronal activity and individual movements became more consistent with learning. These changes in population activity coincided with a transient increase in dendritic spine turnover in these neurons. Our results indicate that a novel and reproducible activity–movement relationship develops as a result of motor learning, and we speculate that synaptic plasticity within the motor cortex underlies the emergence of reproducible spatiotemporal activity patterns for learned movements. These results underscore the profound influence of learning on the way that the cortex produces movements.</description><subject>14</subject><subject>14/35</subject><subject>14/69</subject><subject>631/378/1595/2618</subject><subject>631/378/2597/2599</subject><subject>631/378/2632/1663</subject><subject>64/60</subject><subject>9/74</subject><subject>Animals</subject><subject>Brain</subject><subject>Calcium - metabolism</subject><subject>Dendritic Spines - physiology</subject><subject>Female</subject><subject>Forelimb - physiology</subject><subject>Humanities and Social Sciences</subject><subject>Learning</subject><subject>Learning - physiology</subject><subject>letter</subject><subject>Male</subject><subject>Mice</subject><subject>Models, Neurological</subject><subject>Motor ability</subject><subject>Motor cortex</subject><subject>Motor Cortex - physiology</subject><subject>Motor learning</subject><subject>Motor Skills - physiology</subject><subject>multidisciplinary</subject><subject>Neural Inhibition</subject><subject>Neuronal Plasticity - 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metabolism</topic><topic>Dendritic Spines - physiology</topic><topic>Female</topic><topic>Forelimb - physiology</topic><topic>Humanities and Social Sciences</topic><topic>Learning</topic><topic>Learning - physiology</topic><topic>letter</topic><topic>Male</topic><topic>Mice</topic><topic>Models, Neurological</topic><topic>Motor ability</topic><topic>Motor cortex</topic><topic>Motor Cortex - physiology</topic><topic>Motor learning</topic><topic>Motor Skills - physiology</topic><topic>multidisciplinary</topic><topic>Neural Inhibition</topic><topic>Neuronal Plasticity - physiology</topic><topic>Neurons</topic><topic>Physiological aspects</topic><topic>Physiological research</topic><topic>Plasticity</topic><topic>Reproducibility of Results</topic><topic>Science</topic><topic>Spatio-Temporal Analysis</topic><topic>Spine</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Peters, Andrew J.</creatorcontrib><creatorcontrib>Chen, Simon X.</creatorcontrib><creatorcontrib>Komiyama, Takaki</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>ProQuest Central (Corporate)</collection><collection>Animal Behavior Abstracts</collection><collection>Bacteriology Abstracts (Microbiology B)</collection><collection>Calcium & Calcified Tissue Abstracts</collection><collection>Chemoreception Abstracts</collection><collection>Nursing & Allied Health Database</collection><collection>Ecology Abstracts</collection><collection>Entomology Abstracts (Full archive)</collection><collection>Environment Abstracts</collection><collection>Immunology Abstracts</collection><collection>Meteorological & Geoastrophysical Abstracts</collection><collection>Neurosciences Abstracts</collection><collection>Nucleic Acids Abstracts</collection><collection>Oncogenes and Growth Factors Abstracts</collection><collection>Virology and AIDS Abstracts</collection><collection>Agricultural Science Collection</collection><collection>Health & Medical Collection</collection><collection>ProQuest Central (purchase pre-March 2016)</collection><collection>Biology Database (Alumni Edition)</collection><collection>Medical Database (Alumni Edition)</collection><collection>Psychology Database (Alumni)</collection><collection>Science Database (Alumni Edition)</collection><collection>STEM Database</collection><collection>ProQuest Pharma Collection</collection><collection>Public Health Database</collection><collection>Technology Research Database</collection><collection>ProQuest SciTech Collection</collection><collection>ProQuest Technology Collection</collection><collection>ProQuest Natural Science Collection</collection><collection>Hospital Premium Collection</collection><collection>Hospital Premium Collection (Alumni Edition)</collection><collection>ProQuest Central (Alumni) (purchase pre-March 2016)</collection><collection>Research Library (Alumni Edition)</collection><collection>Materials Science & Engineering Collection</collection><collection>ProQuest Central (Alumni Edition)</collection><collection>ProQuest One Sustainability</collection><collection>ProQuest Central UK/Ireland</collection><collection>Advanced Technologies & Aerospace Collection</collection><collection>Agricultural & Environmental Science Collection</collection><collection>ProQuest Central Essentials</collection><collection>Biological Science Collection</collection><collection>eLibrary</collection><collection>ProQuest Central</collection><collection>Technology Collection</collection><collection>Natural Science Collection</collection><collection>Earth, Atmospheric & Aquatic Science Collection</collection><collection>Environmental Sciences and Pollution Management</collection><collection>ProQuest One Community College</collection><collection>ProQuest Materials Science Collection</collection><collection>ProQuest Central Korea</collection><collection>Engineering Research Database</collection><collection>Health Research Premium Collection</collection><collection>Health Research Premium Collection (Alumni)</collection><collection>ProQuest Central Student</collection><collection>Research Library Prep</collection><collection>AIDS and Cancer Research Abstracts</collection><collection>SciTech Premium Collection</collection><collection>ProQuest Health & Medical Complete (Alumni)</collection><collection>Materials Science Database</collection><collection>Nursing & Allied Health Database (Alumni Edition)</collection><collection>Meteorological & Geoastrophysical Abstracts - 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Academic</collection><jtitle>Nature (London)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Peters, Andrew J.</au><au>Chen, Simon X.</au><au>Komiyama, Takaki</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Emergence of reproducible spatiotemporal activity during motor learning</atitle><jtitle>Nature (London)</jtitle><stitle>Nature</stitle><addtitle>Nature</addtitle><date>2014-06-12</date><risdate>2014</risdate><volume>510</volume><issue>7504</issue><spage>263</spage><epage>267</epage><pages>263-267</pages><issn>0028-0836</issn><eissn>1476-4687</eissn><coden>NATUAS</coden><abstract>Inhibitory neuron activity is found to be relatively stable during motor learning whereas excitatory neuron activity is much more dynamic — the results indicate that a large number of neurons exhibit activity changes early on during motor learning, but this population is refined with subsequent practice.
Motor cortex change during learning
How the brain learns to make adaptive body movements is a central question in systems neuroscience. Motor learning is thought to drive dramatic plasticity in motor circuits, but the extent of this plasticity in large neuronal populations is unclear. Takaki Komiyama and colleagues used techniques including a genetically encoded calcium indicator and chronic
in vivo
two-photon imaging in the motor cortex during a two-week forelimb motor learning task in mice, and found that inhibitory neuron activity is relatively stable during motor learning while excitatory neuron plasticity is much more dynamic. The results indicate that a large number of neurons exhibit activity level changes early on during motor learning, but this population is refined with subsequent practice.
The motor cortex is capable of reliably driving complex movements
1
,
2
yet exhibits considerable plasticity during motor learning
3
,
4
,
5
,
6
,
7
,
8
,
9
,
10
. These observations suggest that the fundamental relationship between motor cortex activity and movement may not be fixed but is instead shaped by learning; however, to what extent and how motor learning shapes this relationship are not fully understood. Here we addressed this issue by using
in vivo
two-photon calcium imaging
11
to monitor the activity of the same population of hundreds of layer 2/3 neurons while mice learned a forelimb lever-press task over two weeks. Excitatory and inhibitory neurons were identified by transgenic labelling
12
,
13
. Inhibitory neuron activity was relatively stable and balanced local excitatory neuron activity on a movement-by-movement basis, whereas excitatory neuron activity showed higher dynamism during the initial phase of learning. The dynamics of excitatory neurons during the initial phase involved the expansion of the movement-related population which explored various activity patterns even during similar movements. This was followed by a refinement into a smaller population exhibiting reproducible spatiotemporal sequences of activity. This pattern of activity associated with the learned movement was unique to expert animals and not observed during similar movements made during the naive phase, and the relationship between neuronal activity and individual movements became more consistent with learning. These changes in population activity coincided with a transient increase in dendritic spine turnover in these neurons. Our results indicate that a novel and reproducible activity–movement relationship develops as a result of motor learning, and we speculate that synaptic plasticity within the motor cortex underlies the emergence of reproducible spatiotemporal activity patterns for learned movements. These results underscore the profound influence of learning on the way that the cortex produces movements.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>24805237</pmid><doi>10.1038/nature13235</doi><tpages>5</tpages></addata></record> |
fulltext | fulltext |
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ispartof | Nature (London), 2014-06, Vol.510 (7504), p.263-267 |
issn | 0028-0836 1476-4687 |
language | eng |
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source | MEDLINE; Nature; SpringerLink Journals - AutoHoldings |
subjects | 14 14/35 14/69 631/378/1595/2618 631/378/2597/2599 631/378/2632/1663 64/60 9/74 Animals Brain Calcium - metabolism Dendritic Spines - physiology Female Forelimb - physiology Humanities and Social Sciences Learning Learning - physiology letter Male Mice Models, Neurological Motor ability Motor cortex Motor Cortex - physiology Motor learning Motor Skills - physiology multidisciplinary Neural Inhibition Neuronal Plasticity - physiology Neurons Physiological aspects Physiological research Plasticity Reproducibility of Results Science Spatio-Temporal Analysis Spine |
title | Emergence of reproducible spatiotemporal activity during motor learning |
url | https://sfx.bib-bvb.de/sfx_tum?ctx_ver=Z39.88-2004&ctx_enc=info:ofi/enc:UTF-8&ctx_tim=2025-02-04T19%3A49%3A23IST&url_ver=Z39.88-2004&url_ctx_fmt=infofi/fmt:kev:mtx:ctx&rfr_id=info:sid/primo.exlibrisgroup.com:primo3-Article-gale_proqu&rft_val_fmt=info:ofi/fmt:kev:mtx:journal&rft.genre=article&rft.atitle=Emergence%20of%20reproducible%20spatiotemporal%20activity%20during%20motor%20learning&rft.jtitle=Nature%20(London)&rft.au=Peters,%20Andrew%20J.&rft.date=2014-06-12&rft.volume=510&rft.issue=7504&rft.spage=263&rft.epage=267&rft.pages=263-267&rft.issn=0028-0836&rft.eissn=1476-4687&rft.coden=NATUAS&rft_id=info:doi/10.1038/nature13235&rft_dat=%3Cgale_proqu%3EA372554145%3C/gale_proqu%3E%3Curl%3E%3C/url%3E&disable_directlink=true&sfx.directlink=off&sfx.report_link=0&rft_id=info:oai/&rft_pqid=1539434911&rft_id=info:pmid/24805237&rft_galeid=A372554145&rfr_iscdi=true |