Cortical Synaptic AMPA Receptor Plasticity during Motor Learning
Modulation of synaptic strength through trafficking of AMPA receptors (AMPARs) is a fundamental mechanism underlying synaptic plasticity, learning, and memory. However, the dynamics of AMPAR trafficking in vivo and its correlation with learning have not been resolved. Here, we used in vivo two-photo...
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Veröffentlicht in: | Neuron (Cambridge, Mass.) Mass.), 2020-03, Vol.105 (5), p.895-908.e5 |
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description | Modulation of synaptic strength through trafficking of AMPA receptors (AMPARs) is a fundamental mechanism underlying synaptic plasticity, learning, and memory. However, the dynamics of AMPAR trafficking in vivo and its correlation with learning have not been resolved. Here, we used in vivo two-photon microscopy to visualize surface AMPARs in mouse cortex during the acquisition of a forelimb reaching task. Daily training leads to an increase in AMPAR levels at a subset of spatially clustered dendritic spines in the motor cortex. Surprisingly, we also observed increases in spine AMPAR levels in the visual cortex. There, synaptic potentiation depends on the availability of visual input during motor training, and optogenetic inhibition of visual cortex activity impairs task performance. These results indicate that motor learning induces widespread cortical synaptic potentiation by increasing the net trafficking of AMPARs into spines, including in non-motor brain regions.
•In vivo imaging of AMPA receptors reveals high dynamics at individual synapses•Motor learning induces potentiation of a clustered subset of dendritic spines•Motor learning increases AMPA receptor levels in motor and visual cortex•Plasticity of visual cortex during learning depends on visual input
Through in vivo imaging of synaptic AMPA receptors in mice, Roth et al. show that motor learning potentiates synapses in both motor and visual cortex. Recruitment and potentiation of the visual cortex require visual stimuli during motor training. |
doi_str_mv | 10.1016/j.neuron.2019.12.005 |
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•In vivo imaging of AMPA receptors reveals high dynamics at individual synapses•Motor learning induces potentiation of a clustered subset of dendritic spines•Motor learning increases AMPA receptor levels in motor and visual cortex•Plasticity of visual cortex during learning depends on visual input
Through in vivo imaging of synaptic AMPA receptors in mice, Roth et al. show that motor learning potentiates synapses in both motor and visual cortex. Recruitment and potentiation of the visual cortex require visual stimuli during motor training.</description><identifier>ISSN: 0896-6273</identifier><identifier>EISSN: 1097-4199</identifier><identifier>DOI: 10.1016/j.neuron.2019.12.005</identifier><identifier>PMID: 31901303</identifier><language>eng</language><publisher>United States: Elsevier Inc</publisher><subject>AMPA receptors ; Animals ; Cortex (motor) ; Dendritic spines ; Dendritic Spines - metabolism ; Food ; Forelimb ; Intravital Microscopy ; Learning ; long-term potentiation ; Mice ; Microscopy, Fluorescence ; Motor Activity ; motor cortex ; Motor Cortex - metabolism ; motor learning ; Motor skill learning ; Neuronal Plasticity ; Neurons - metabolism ; Neuroplasticity ; Optogenetics ; Potentiation ; Protein Transport ; Psychomotor Performance ; Receptors, AMPA - metabolism ; Sensorimotor integration ; Spatio-Temporal Analysis ; synaptic clustering ; Synaptic plasticity ; Synaptic strength ; two-photon imaging ; Visual cortex ; Visual Cortex - metabolism ; α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid ; α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors</subject><ispartof>Neuron (Cambridge, Mass.), 2020-03, Vol.105 (5), p.895-908.e5</ispartof><rights>2019 Elsevier Inc.</rights><rights>Copyright © 2019 Elsevier Inc. All rights reserved.</rights><rights>2019. Elsevier Inc.</rights><lds50>peer_reviewed</lds50><oa>free_for_read</oa><woscitedreferencessubscribed>false</woscitedreferencessubscribed><citedby>FETCH-LOGICAL-c491t-c40cac282df8f90db3de6283df4680669cf018b2794388fb6a2fed4c75a0e2a63</citedby><cites>FETCH-LOGICAL-c491t-c40cac282df8f90db3de6283df4680669cf018b2794388fb6a2fed4c75a0e2a63</cites></display><links><openurl>$$Topenurl_article</openurl><openurlfulltext>$$Topenurlfull_article</openurlfulltext><thumbnail>$$Tsyndetics_thumb_exl</thumbnail><linktohtml>$$Uhttps://www.sciencedirect.com/science/article/pii/S0896627319310475$$EHTML$$P50$$Gelsevier$$H</linktohtml><link.rule.ids>230,314,776,780,881,3537,27901,27902,65306</link.rule.ids><backlink>$$Uhttps://www.ncbi.nlm.nih.gov/pubmed/31901303$$D View this record in MEDLINE/PubMed$$Hfree_for_read</backlink></links><search><creatorcontrib>Roth, Richard H.</creatorcontrib><creatorcontrib>Cudmore, Robert H.</creatorcontrib><creatorcontrib>Tan, Han L.</creatorcontrib><creatorcontrib>Hong, Ingie</creatorcontrib><creatorcontrib>Zhang, Yong</creatorcontrib><creatorcontrib>Huganir, Richard L.</creatorcontrib><title>Cortical Synaptic AMPA Receptor Plasticity during Motor Learning</title><title>Neuron (Cambridge, Mass.)</title><addtitle>Neuron</addtitle><description>Modulation of synaptic strength through trafficking of AMPA receptors (AMPARs) is a fundamental mechanism underlying synaptic plasticity, learning, and memory. However, the dynamics of AMPAR trafficking in vivo and its correlation with learning have not been resolved. Here, we used in vivo two-photon microscopy to visualize surface AMPARs in mouse cortex during the acquisition of a forelimb reaching task. Daily training leads to an increase in AMPAR levels at a subset of spatially clustered dendritic spines in the motor cortex. Surprisingly, we also observed increases in spine AMPAR levels in the visual cortex. There, synaptic potentiation depends on the availability of visual input during motor training, and optogenetic inhibition of visual cortex activity impairs task performance. These results indicate that motor learning induces widespread cortical synaptic potentiation by increasing the net trafficking of AMPARs into spines, including in non-motor brain regions.
•In vivo imaging of AMPA receptors reveals high dynamics at individual synapses•Motor learning induces potentiation of a clustered subset of dendritic spines•Motor learning increases AMPA receptor levels in motor and visual cortex•Plasticity of visual cortex during learning depends on visual input
Through in vivo imaging of synaptic AMPA receptors in mice, Roth et al. show that motor learning potentiates synapses in both motor and visual cortex. Recruitment and potentiation of the visual cortex require visual stimuli during motor training.</description><subject>AMPA receptors</subject><subject>Animals</subject><subject>Cortex (motor)</subject><subject>Dendritic spines</subject><subject>Dendritic Spines - metabolism</subject><subject>Food</subject><subject>Forelimb</subject><subject>Intravital Microscopy</subject><subject>Learning</subject><subject>long-term potentiation</subject><subject>Mice</subject><subject>Microscopy, Fluorescence</subject><subject>Motor Activity</subject><subject>motor cortex</subject><subject>Motor Cortex - metabolism</subject><subject>motor learning</subject><subject>Motor skill learning</subject><subject>Neuronal Plasticity</subject><subject>Neurons - metabolism</subject><subject>Neuroplasticity</subject><subject>Optogenetics</subject><subject>Potentiation</subject><subject>Protein Transport</subject><subject>Psychomotor Performance</subject><subject>Receptors, AMPA - metabolism</subject><subject>Sensorimotor integration</subject><subject>Spatio-Temporal Analysis</subject><subject>synaptic clustering</subject><subject>Synaptic plasticity</subject><subject>Synaptic strength</subject><subject>two-photon imaging</subject><subject>Visual cortex</subject><subject>Visual Cortex - metabolism</subject><subject>α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid</subject><subject>α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors</subject><issn>0896-6273</issn><issn>1097-4199</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2020</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><recordid>eNp9kUtvGyEUhVHUKHGT_oOoGqmbbDy5wAwzbKJaVptWctQobdcIw50UawwOzETyvy-W8-yiGx6Xcw8cPkLOKJQUqLhYlR7HGHzJgMqSshKgPiATCrKZVlTKd2QCrRRTwRp-TN6ntAKgVS3pETnmVALlwCfk8zzEwRndFz-3Xm_ysphd38yKWzS4GUIsbnqdctUN28KO0fm74jrs6gvU0eftKTnsdJ_ww-N8Qn5__fJr_m26-HH1fT5bTE0l6ZBHMNqwltmu7STYJbcoWMttV4kWhJCmA9ouWSMr3rbdUmjWoa1MU2tApgU_IZd73824XKM16Ieoe7WJbq3jVgXt1NsT7_6ou_CgGhBAockG548GMdyPmAa1dslg32uPYUyKcc4lk5LVWfrpH-kqjNHneIpVrBaCCs6yqtqrTAwpReyeH0NB7RCpldojUjtEijKVEeW2j6-DPDc9MXlJivk7HxxGlYxDb9C6iGZQNrj_3_AX98CkfA</recordid><startdate>20200304</startdate><enddate>20200304</enddate><creator>Roth, Richard H.</creator><creator>Cudmore, Robert H.</creator><creator>Tan, Han L.</creator><creator>Hong, Ingie</creator><creator>Zhang, Yong</creator><creator>Huganir, Richard L.</creator><general>Elsevier Inc</general><general>Elsevier Limited</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>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>5PM</scope></search><sort><creationdate>20200304</creationdate><title>Cortical Synaptic AMPA Receptor Plasticity during Motor Learning</title><author>Roth, Richard H. ; Cudmore, Robert H. ; Tan, Han L. ; Hong, Ingie ; Zhang, Yong ; Huganir, Richard L.</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c491t-c40cac282df8f90db3de6283df4680669cf018b2794388fb6a2fed4c75a0e2a63</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2020</creationdate><topic>AMPA receptors</topic><topic>Animals</topic><topic>Cortex (motor)</topic><topic>Dendritic spines</topic><topic>Dendritic Spines - metabolism</topic><topic>Food</topic><topic>Forelimb</topic><topic>Intravital Microscopy</topic><topic>Learning</topic><topic>long-term potentiation</topic><topic>Mice</topic><topic>Microscopy, Fluorescence</topic><topic>Motor Activity</topic><topic>motor cortex</topic><topic>Motor Cortex - metabolism</topic><topic>motor learning</topic><topic>Motor skill learning</topic><topic>Neuronal Plasticity</topic><topic>Neurons - metabolism</topic><topic>Neuroplasticity</topic><topic>Optogenetics</topic><topic>Potentiation</topic><topic>Protein Transport</topic><topic>Psychomotor Performance</topic><topic>Receptors, AMPA - metabolism</topic><topic>Sensorimotor integration</topic><topic>Spatio-Temporal Analysis</topic><topic>synaptic clustering</topic><topic>Synaptic plasticity</topic><topic>Synaptic strength</topic><topic>two-photon imaging</topic><topic>Visual cortex</topic><topic>Visual Cortex - metabolism</topic><topic>α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid</topic><topic>α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Roth, Richard H.</creatorcontrib><creatorcontrib>Cudmore, Robert H.</creatorcontrib><creatorcontrib>Tan, Han L.</creatorcontrib><creatorcontrib>Hong, Ingie</creatorcontrib><creatorcontrib>Zhang, Yong</creatorcontrib><creatorcontrib>Huganir, Richard L.</creatorcontrib><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>PubMed Central (Full Participant titles)</collection><jtitle>Neuron (Cambridge, Mass.)</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Roth, Richard H.</au><au>Cudmore, Robert H.</au><au>Tan, Han L.</au><au>Hong, Ingie</au><au>Zhang, Yong</au><au>Huganir, Richard L.</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Cortical Synaptic AMPA Receptor Plasticity during Motor Learning</atitle><jtitle>Neuron (Cambridge, Mass.)</jtitle><addtitle>Neuron</addtitle><date>2020-03-04</date><risdate>2020</risdate><volume>105</volume><issue>5</issue><spage>895</spage><epage>908.e5</epage><pages>895-908.e5</pages><issn>0896-6273</issn><eissn>1097-4199</eissn><abstract>Modulation of synaptic strength through trafficking of AMPA receptors (AMPARs) is a fundamental mechanism underlying synaptic plasticity, learning, and memory. However, the dynamics of AMPAR trafficking in vivo and its correlation with learning have not been resolved. Here, we used in vivo two-photon microscopy to visualize surface AMPARs in mouse cortex during the acquisition of a forelimb reaching task. Daily training leads to an increase in AMPAR levels at a subset of spatially clustered dendritic spines in the motor cortex. Surprisingly, we also observed increases in spine AMPAR levels in the visual cortex. There, synaptic potentiation depends on the availability of visual input during motor training, and optogenetic inhibition of visual cortex activity impairs task performance. These results indicate that motor learning induces widespread cortical synaptic potentiation by increasing the net trafficking of AMPARs into spines, including in non-motor brain regions.
•In vivo imaging of AMPA receptors reveals high dynamics at individual synapses•Motor learning induces potentiation of a clustered subset of dendritic spines•Motor learning increases AMPA receptor levels in motor and visual cortex•Plasticity of visual cortex during learning depends on visual input
Through in vivo imaging of synaptic AMPA receptors in mice, Roth et al. show that motor learning potentiates synapses in both motor and visual cortex. Recruitment and potentiation of the visual cortex require visual stimuli during motor training.</abstract><cop>United States</cop><pub>Elsevier Inc</pub><pmid>31901303</pmid><doi>10.1016/j.neuron.2019.12.005</doi><oa>free_for_read</oa></addata></record> |
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subjects | AMPA receptors Animals Cortex (motor) Dendritic spines Dendritic Spines - metabolism Food Forelimb Intravital Microscopy Learning long-term potentiation Mice Microscopy, Fluorescence Motor Activity motor cortex Motor Cortex - metabolism motor learning Motor skill learning Neuronal Plasticity Neurons - metabolism Neuroplasticity Optogenetics Potentiation Protein Transport Psychomotor Performance Receptors, AMPA - metabolism Sensorimotor integration Spatio-Temporal Analysis synaptic clustering Synaptic plasticity Synaptic strength two-photon imaging Visual cortex Visual Cortex - metabolism α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid α-Amino-3-hydroxy-5-methyl-4-isoxazole propionic acid receptors |
title | Cortical Synaptic AMPA Receptor Plasticity during Motor Learning |
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