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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Veröffentlicht in:Nature (London) 2014-06, Vol.510 (7504), p.263-267
Hauptverfasser: Peters, Andrew J., Chen, Simon X., Komiyama, Takaki
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Chen, Simon X.
Komiyama, Takaki
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
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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.</abstract><cop>London</cop><pub>Nature Publishing Group UK</pub><pmid>24805237</pmid><doi>10.1038/nature13235</doi><tpages>5</tpages></addata></record>
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language eng
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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
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