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Rapid formation and selective stabilization of synapses for enduring motor memories

Novel motor skills are learned through repetitive practice and, once acquired, persist long after training stops. Earlier studies have shown that such learning induces an increase in the efficacy of synapses in the primary motor cortex, the persistence of which is associated with retention of the ta... Full description

Journal Title: Nature (London) 2009-12-17, Vol.462 (7275), p.915-919
Main Author: Xu, Tonghui
Other Authors: Yu, Xinzhu , Perlik, Andrew J , Tobin, Willie F , Zweig, Jonathan A , Tennant, Kelly , Jones, Theresa , Zuo, Yi
Format: Electronic Article Electronic Article
Language: English
Subjects:
Publisher: England: Nature Publishing Group
ID: ISSN: 0028-0836
Link: https://www.ncbi.nlm.nih.gov/pubmed/19946267
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recordid: cdi_pubmedcentral_primary_oai_pubmedcentral_nih_gov_2844762
title: Rapid formation and selective stabilization of synapses for enduring motor memories
format: Article
creator:
  • Xu, Tonghui
  • Yu, Xinzhu
  • Perlik, Andrew J
  • Tobin, Willie F
  • Zweig, Jonathan A
  • Tennant, Kelly
  • Jones, Theresa
  • Zuo, Yi
subjects:
  • Aging - physiology
  • Animals
  • Article
  • Dendrites - physiology
  • education
  • Forelimb - physiology
  • Memory - physiology
  • Mice
  • Motor cortex
  • Motor Cortex - cytology
  • Motor Cortex - physiology
  • Motor learning
  • Motor Skills - physiology
  • Neural transmission
  • Neuronal Plasticity - physiology
  • Physiological aspects
  • Psychomotor Performance
  • Pyramidal Cells - metabolism
  • Seeds
  • Synapses - metabolism
  • Time Factors
ispartof: Nature (London), 2009-12-17, Vol.462 (7275), p.915-919
description: Novel motor skills are learned through repetitive practice and, once acquired, persist long after training stops. Earlier studies have shown that such learning induces an increase in the efficacy of synapses in the primary motor cortex, the persistence of which is associated with retention of the task. However, how motor learning affects neuronal circuitry at the level of individual synapses and how long-lasting memory is structurally encoded in the intact brain remain unknown. Here we show that synaptic connections in the living mouse brain rapidly respond to motor-skill learning and permanently rewire. Training in a forelimb reaching task leads to rapid (within an hour) formation of postsynaptic dendritic spines on the output pyramidal neurons in the contralateral motor cortex. Although selective elimination of spines that existed before training gradually returns the overall spine density back to the original level, the new spines induced during learning are preferentially stabilized during subsequent training and endure long after training stops. Furthermore, we show that different motor skills are encoded by different sets of synapses. Practice of novel, but not previously learned, tasks further promotes dendritic spine formation in adulthood. Our findings reveal that rapid, but long-lasting, synaptic reorganization is closely associated with motor learning. The data also suggest that stabilized neuronal connections are the foundation of durable motor memory.
language: eng
source:
identifier: ISSN: 0028-0836
fulltext: no_fulltext
issn:
  • 0028-0836
  • 1476-4687
url: Link


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subjectAging - physiology ; Animals ; Article ; Dendrites - physiology ; education ; Forelimb - physiology ; Memory - physiology ; Mice ; Motor cortex ; Motor Cortex - cytology ; Motor Cortex - physiology ; Motor learning ; Motor Skills - physiology ; Neural transmission ; Neuronal Plasticity - physiology ; Physiological aspects ; Psychomotor Performance ; Pyramidal Cells - metabolism ; Seeds ; Synapses - metabolism ; Time Factors
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abstractNovel motor skills are learned through repetitive practice and, once acquired, persist long after training stops. Earlier studies have shown that such learning induces an increase in the efficacy of synapses in the primary motor cortex, the persistence of which is associated with retention of the task. However, how motor learning affects neuronal circuitry at the level of individual synapses and how long-lasting memory is structurally encoded in the intact brain remain unknown. Here we show that synaptic connections in the living mouse brain rapidly respond to motor-skill learning and permanently rewire. Training in a forelimb reaching task leads to rapid (within an hour) formation of postsynaptic dendritic spines on the output pyramidal neurons in the contralateral motor cortex. Although selective elimination of spines that existed before training gradually returns the overall spine density back to the original level, the new spines induced during learning are preferentially stabilized during subsequent training and endure long after training stops. Furthermore, we show that different motor skills are encoded by different sets of synapses. Practice of novel, but not previously learned, tasks further promotes dendritic spine formation in adulthood. Our findings reveal that rapid, but long-lasting, synaptic reorganization is closely associated with motor learning. The data also suggest that stabilized neuronal connections are the foundation of durable motor memory.
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