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      Functional plasticity of the ipsilateral primary sensorimotor cortex in an elite long jumper with below-knee amputation

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          Abstract

          Functional plasticity of the sensorimotor cortex occurs following motor practice, as well as after limb amputation. However, the joint effect of limb amputation and intensive, long-term motor practice on cortical plasticity remains unclear. Here, we recorded brain activity during unilateral contraction of the hip, knee, and ankle joint muscles from a long jump Paralympic gold medalist with a unilateral below-knee amputation (Amputee Long Jumper, ALJ). He used the amputated leg with a prosthesis for take-off. Under similar conditions to the ALJ, we also recorded brain activity from healthy long jumpers (HLJ) and non-athletes with a below-knee amputation. During a rhythmic isometric contraction of knee extensor muscles with the take-off/prosthetic leg, the ALJ activated not only the contralateral primary sensorimotor cortex (M1/S1), but also the ipsilateral M1/S1. In addition, this ipsilateral M1/S1 activation was significantly greater than that seen in the HLJ. However, we did not find any significant differences between the ALJ and HLJ in M1/S1 activation during knee muscle contraction in the non-take-off/intact leg, nor during hip muscle contraction on either side. Region of interest analysis revealed that the ALJ exhibited a greater difference in M1/S1 activity and activated areas ipsilateral to the movement side between the take-off/prosthetic and non-take-off/intact legs during knee muscle contraction compared with the other two groups. However, difference in activity in M1/S1 contralateral to the movement side did not differ across groups. These results suggest that a combination of below-knee amputation and intensive, prolonged long jump training using a prosthesis (i.e. fine knee joint control) induced an expansion of the functional representation of the take-off/prosthetic leg in the ipsilateral M1/S1 in a muscle-specific manner. These results provide novel insights into the potential for substantial cortical plasticity with an extensive motor rehabilitation program.

          Highlights

          • A Paralympic gold medalist with a unilateral below-knee amputation was recruited.

          • Brain activity during hip, knee, and ankle movements was recorded.

          • Brain activity was compared with healthy athletes and non-athletes with amputation.

          • Greater ipsilateral M1/S1 activity during knee movement was observed in the medalist.

          • Intensive motor practice and limb amputation would induce drastic neural plasticity.

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          Most cited references39

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          Functional MRI evidence for adult motor cortex plasticity during motor skill learning.

          Performance of complex motor tasks, such as rapid sequences of finger movements, can be improved in terms of speed and accuracy over several weeks by daily practice sessions. This improvement does not generalize to a matched sequence of identical component movements, nor to the contralateral hand. Here we report a study of the neural changes underlying this learning using functional magnetic resonance imaging (MRI) of local blood oxygenation level-dependent (BOLD) signals evoked in primary motor cortex (M1). Before training, a comparable extent of M1 was activated by both sequences. However, two ordering effects were observed: repeating a sequence within a brief time window initially resulted in a smaller area of activation (habituation), but later in larger area of activation (enhancement), suggesting a switch in M1 processing mode within the first session (fast learning). By week 4 of training, concurrent with asymptotic performance, the extent of cortex activated by the practised sequence enlarged compared with the unpractised sequence, irrespective of order (slow learning). These changes persisted for several months. The results suggest a slowly evolving, long-term, experience-dependent reorganization of the adult M1, which may underlie the acquisition and retention of the motor skill.
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            The neural network of motor imagery: an ALE meta-analysis.

            Motor imagery (MI) or the mental simulation of action is now increasingly being studied using neuroimaging techniques such as positron emission tomography and functional magnetic resonance imaging. The booming interest in capturing the neural underpinning of MI has provided a large amount of data which until now have never been quantitatively summarized. The aim of this activation likelihood estimation (ALE) meta-analysis was to provide a map of the brain structures involved in MI. Combining the data from 75 papers revealed that MI consistently recruits a large fronto-parietal network in addition to subcortical and cerebellar regions. Although the primary motor cortex was not shown to be consistently activated, the MI network includes several regions which are known to play a role during actual motor execution. The body part involved in the movements, the modality of MI and the nature of the MI tasks used all seem to influence the consistency of activation within the general MI network. In addition to providing the first quantitative cortical map of MI, we highlight methodological issues that should be addressed in future research. Copyright © 2013 Elsevier Ltd. All rights reserved.
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              Comparing an Individual's Test Score Against Norms Derived from Small Samples

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                Author and article information

                Contributors
                Journal
                Neuroimage Clin
                Neuroimage Clin
                NeuroImage : Clinical
                Elsevier
                2213-1582
                09 May 2019
                2019
                09 May 2019
                : 23
                : 101847
                Affiliations
                [a ]Faculty of Sport Sciences, Waseda University, 2-579-15 Mikajima, Tokorozawa, Saitama 359-1192, Japan
                [b ]Faculty of Science and Technology, Keio University, 3-14-1 Hiyoshi, Kohoku-ku, Yokohama city, Kanagawa 223-8522, Japan
                [c ]The Japan Society for the Promotion of Science, 5-3-1 Kojimachi, Chiyoda-ku, Tokyo 102-0083, Japan
                [d ]Graduate School of Arts and Sciences, The University of Tokyo, 3-8-1 Komaba, Meguro-ku, Tokyo 153-8902, Japan
                Author notes
                [* ]Corresponding author at: Laboratory of Sports Sciences, Department of Life Sciences, Graduate School of Arts and Sciences, The University of Tokyo, Meguro-ku, Tokyo, Japan. nakazawa@ 123456idaten.c.u-tokyo.ac.jp
                [1]

                Equal contribution

                Article
                S2213-1582(19)30197-4 101847
                10.1016/j.nicl.2019.101847
                6525316
                31103873
                b77ac2da-4e0a-4a03-8b62-391b36c6188d
                © 2019 The Authors

                This is an open access article under the CC BY license (http://creativecommons.org/licenses/by/4.0/).

                History
                : 15 November 2018
                : 27 April 2019
                : 30 April 2019
                Categories
                Regular Article

                athlete,amputee,motor learning,rehabilitation,plasticity,prosthesis

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