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Brain plasticity in Parkinson’s disease with freezing of gait induced by action observation training

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Abstract

Gait disorders represent a therapeutic challenge in Parkinson’s disease (PD). This study investigated the efficacy of 4-week action observation training (AOT) on disease severity, freezing of gait and motor abilities in PD, and evaluated treatment-related brain functional changes. 25 PD patients with freezing of gait were randomized into two groups: AOT (action observation combined with practicing the observed actions) and “Landscape” (same physical training combined with landscape-videos observation). At baseline and 4-week, patients underwent clinical evaluation and fMRI. Clinical assessment was repeated at 8-week. At 4-week, both groups showed reduced freezing of gait severity, improved walking speed and quality of life. Moreover, AOT was associated with reduced motor disability and improved balance. AOT group showed a sustained positive effect on motor disability, walking speed, balance and quality of life at 8-week, with a trend toward a persisting reduced freezing of gait severity. At 4-week vs. baseline, AOT group showed increased recruitment of fronto-parietal areas during fMRI tasks, while the Landscape group showed a reduced fMRI activity of the left postcentral and inferior parietal gyri and right rolandic operculum and supramarginal gyrus. In AOT group, functional brain changes were associated with clinical improvements at 4-week and predicted clinical evolution at 8-week. AOT has a more lasting effect in improving motor function, gait and quality of life in PD patients relative to physical therapy alone. AOT-related performance gains are associated with an increased recruitment of motor regions and fronto-parietal mirror neuron and attentional control areas.

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Acknowledgments

We thank Dr. Elisa Pelosin for providing us with the video clips used during the training sessions. This study was partially supported by a grant from the Jacques and Gloria Gossweiler Foundation.

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    Authors and Affiliations

    1. Neuroimaging Research Unit, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Via Olgettina, 60, 20132, Milan, Italy

      Federica Agosta, Elisabetta Sarasso, Elisa Canu, Alessandro Meani, Lidia Sarro & Massimo Filippi

    2. Department of Neurology, Institute of Experimental Neurology, Division of Neuroscience, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy

      Maria Antonietta Volonté, Lidia Sarro, Giancarlo Comi & Massimo Filippi

    3. Laboratory of Movement Analysis, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy

      Roberto Gatti & Elisabetta Sarasso

    4. Department of Neuroradiology, San Raffaele Scientific Institute, Vita-Salute San Raffaele University, Milan, Italy

      Andrea Falini

    5. Biostatistics Unit, IRCCS-Ospedale Casa Sollievo Della Sofferenza, San Giovanni Rotondo, Foggia, Italy

      Massimiliano Copetti

    6. Faculty of Physical Education and Physiotherapy, Vrije Universiteit Brussel, Bruxelles, Belgium

      Erik Cattrysse & Eric Kerckhofs

    7. Physiotherapy Unit, Humanitas University and Humanitas Clinical and Research Center, Rozzano, Italy

      Roberto Gatti

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    1. Federica Agosta
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    Correspondence to Massimo Filippi.

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    Conflicts of interest

    F Agosta serves on the editorial board of the Journal of Neurology; has received speaker honoraria from EXCEMED– Excellence in Medical Education; and receives research supports from the Italian Ministry of Health, AriSLA (Fondazione Italiana di Ricerca per la SLA), and the European Research Council. R. Gatti, E. Sarasso, M.A. Volonté, E. Canu, A. Meani, L. Sarro, M. Copetti, E. Cattrysse, E. Kerckhofs, and A. Falini report no disclosures. G. Comi has received compensation for consulting services and/or speaking activities from Novartis, Teva Pharmaceutical Ind., Sanofi, Genzyme, Merck Serono, Biogen, Bayer, Actelion, Serono Symposia International Foundation, Almirall, Chugai and Receptos. M. Filippi is Editor-in-Chief of Journal of Neurology; serves on the scientific advisory board of Teva Pharmaceutical Industries; has received compensation for consulting services and/or speaking activities from Biogen Idec, Excemed, Novartis, and Teva Pharmaceutical Industries; and receives research support from Biogen Idec, Teva Pharmaceutical Industries, Novartis, Italian Ministry of Health, Fondazione Italiana Sclerosi Multipla, Cure PSP, Alzheimer’s Drug Discovery Foundation (ADDF), the Jacques and Gloria Gossweiler Foundation (Switzerland), and ARiSLA (Fondazione Italiana di Ricerca per la SLA).

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    F. Agosta and R. Gatti contributed equally to this work.

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    Agosta, F., Gatti, R., Sarasso, E. et al. Brain plasticity in Parkinson’s disease with freezing of gait induced by action observation training. J Neurol 264, 88–101 (2017). https://doi.org/10.1007/s00415-016-8309-7

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    • DOI: https://doi.org/10.1007/s00415-016-8309-7

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