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      Disengagement of motor cortex from movement control during long-term learning


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          Long-term training of motor skills reorganizes motor circuits to bypass primary motor cortex.


          Motor learning involves reorganization of the primary motor cortex (M1). However, it remains unclear how the involvement of M1 in movement control changes during long-term learning. To address this, we trained mice in a forelimb-based motor task over months and performed optogenetic inactivation and two-photon calcium imaging in M1 during the long-term training. We found that M1 inactivation impaired the forelimb movements in the early and middle stages, but not in the late stage, indicating that the movements that initially required M1 became independent of M1. As previously shown, M1 population activity became more consistent across trials from the early to middle stage while task performance rapidly improved. However, from the middle to late stage, M1 population activity became again variable despite consistent expert behaviors. This later decline in activity consistency suggests dissociation between M1 and movements. These findings suggest that long-term motor learning can disengage M1 from movement control.

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          Most cited references28

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          DeepLabCut: markerless pose estimation of user-defined body parts with deep learning

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            Learning-induced LTP in neocortex.

            The hypothesis that learning occurs through long-term potentiation (LTP)- and long-term depression (LTD)-like mechanisms is widely held but unproven. This hypothesis makes three assumptions: Synapses are modifiable, they modify with learning, and they strengthen through an LTP-like mechanism. We previously established the ability for synaptic modification and a synaptic strengthening with motor skill learning in horizontal connections of the rat motor cortex (MI). Here we investigated whether learning strengthened these connections through LTP. We demonstrated that synapses in the trained MI were near the ceiling of their modification range, compared with the untrained MI, but the range of synaptic modification was not affected by learning. In the trained MI, LTP was markedly reduced and LTD was enhanced. These results are consistent with the use of LTP to strengthen synapses during learning.
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              Plasticity and primary motor cortex.

              One fundamental function of primary motor cortex (MI) is to control voluntary movements. Recent evidence suggests that this role emerges from distributed networks rather than discrete representations and that in adult mammals these networks are capable of modification. Neuronal recordings and activation patterns revealed with neuroimaging methods have shown considerable plasticity of MI representations and cell properties following pathological or traumatic changes and in relation to everyday experience, including motor-skill learning and cognitive motor actions. The intrinsic horizontal neuronal connections in MI are a strong candidate substrate for map reorganization: They interconnect large regions of MI, they show activity-dependent plasticity, and they modify in association with skill learning. These findings suggest that MI cortex is not simply a static motor control structure. It also contains a dynamic substrate that participates in motor learning and possibly in cognitive events as well.

                Author and article information

                Sci Adv
                Sci Adv
                Science Advances
                American Association for the Advancement of Science
                October 2019
                30 October 2019
                : 5
                : 10
                [1]Neurobiology Section, Center for Neural Circuits and Behavior, Department of Neurosciences, and Halıcıoğlu Data Science Institute, University of California, San Diego, La Jolla, CA, USA.
                Author notes

                These authors contributed equally to this work.

                []Corresponding author. Email: tkomiyama@ 123456ucsd.edu
                Copyright © 2019 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Distributed under a Creative Commons Attribution NonCommercial License 4.0 (CC BY-NC).

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial license, which permits use, distribution, and reproduction in any medium, so long as the resultant use is not for commercial advantage and provided the original work is properly cited.

                Funded by: doi http://dx.doi.org/10.13039/100000001, National Science Foundation;
                Award ID: 1734940
                Funded by: doi http://dx.doi.org/10.13039/100000008, David and Lucile Packard Foundation;
                Funded by: doi http://dx.doi.org/10.13039/100000053, National Eye Institute;
                Award ID: R01 EY025349
                Funded by: doi http://dx.doi.org/10.13039/100000053, National Eye Institute;
                Award ID: P30EY022589
                Funded by: doi http://dx.doi.org/10.13039/100000055, National Institute on Deafness and Other Communication Disorders;
                Award ID: R01 DC014690
                Funded by: doi http://dx.doi.org/10.13039/100000065, National Institute of Neurological Disorders and Stroke;
                Award ID: R01 NS091010A
                Funded by: doi http://dx.doi.org/10.13039/100000065, National Institute of Neurological Disorders and Stroke;
                Award ID: U01 NS094342
                Funded by: doi http://dx.doi.org/10.13039/100000065, National Institute of Neurological Disorders and Stroke;
                Award ID: 1R21NS109722
                Funded by: doi http://dx.doi.org/10.13039/100000875, Pew Charitable Trusts;
                Funded by: doi http://dx.doi.org/10.13039/100003194, New York Stem Cell Foundation;
                Funded by: doi http://dx.doi.org/10.13039/100005270, McKnight Foundation;
                Funded by: doi http://dx.doi.org/10.13039/100012378, Kavli Institute for Brain and Mind, University of California, San Diego;
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