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      The Anatomical Basis for Dystonia: The Motor Network Model

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          Abstract

          Background

          The dystonias include a clinically and etiologically very diverse group of disorders. There are both degenerative and non-degenerative subtypes resulting from genetic or acquired causes. Traditionally, all dystonias have been viewed as disorders of the basal ganglia. However, there has been increasing appreciation for involvement of other brain regions including the cerebellum, thalamus, midbrain, and cortex. Much of the early evidence for these other brain regions has come from studies of animals, but multiple recent studies have been done with humans, in an effort to confirm or refute involvement of these other regions. The purpose of this article is to review the new evidence from animals and humans regarding the motor network model, and to address the issues important to translational neuroscience.

          Methods

          The English literature was reviewed for articles relating to the neuroanatomical basis for various types of dystonia in both animals and humans.

          Results

          There is evidence from both animals and humans that multiple brain regions play an important role in various types of dystonia. The most direct evidence for specific brain regions comes from animal studies using pharmacological, lesion, or genetic methods. In these studies, experimental manipulations of specific brain regions provide direct evidence for involvement of the basal ganglia, cerebellum, thalamus and other regions. Additional evidence also comes from human studies using neuropathological, neuroimaging, non-invasive brain stimulation, and surgical interventions. In these studies, the evidence is less conclusive, because discriminating the regions that cause dystonia from those that reflect secondary responses to abnormal movements is more challenging.

          Discussion

          Overall, the evidence from both animals and humans suggests that different regions may play important roles in different subtypes of dystonia. The evidence so far provides strong support for the motor network model. There are obvious challenges, but also advantages, of attempting to translate knowledge gained from animals into a more complete understanding of human dystonia and novel therapeutic strategies.

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          Most cited references154

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          The functional neuroanatomy of dystonia.

          Dystonia is a neurological disorder characterized by involuntary twisting movements and postures. There are many different clinical manifestations, and many different causes. The neuroanatomical substrates for dystonia are only partly understood. Although the traditional view localizes dystonia to basal ganglia circuits, there is increasing recognition that this view is inadequate for accommodating a substantial portion of available clinical and experimental evidence. A model in which several brain regions play a role in a network better accommodates the evidence. This network model accommodates neuropathological and neuroimaging evidence that dystonia may be associated with abnormalities in multiple different brain regions. It also accommodates animal studies showing that dystonic movements arise with manipulations of different brain regions. It is consistent with neurophysiological evidence suggesting defects in neural inhibitory processes, sensorimotor integration, and maladaptive plasticity. Finally, it may explain neurosurgical experience showing that targeting the basal ganglia is effective only for certain subpopulations of dystonia. Most importantly, the network model provides many new and testable hypotheses with direct relevance for new treatment strategies that go beyond the basal ganglia. This article is part of a Special Issue entitled "Advances in dystonia". Copyright © 2011 Elsevier Inc. All rights reserved.
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            Training-induced structural changes in the adult human brain.

            Structural and functional brain reorganisation can occur beyond the developmental maturation period and this was recently recognised as an intrinsic property of the human central nervous system. Brain injury or altered afferent input due to environmental changes, novel experience and learning new skills are known as modulators of brain function and underlying neuroanatomic circuitry. During the past decade invasive animal studies and in vivo imaging techniques have delineated the correlates of experience dependent reorganisation. The major future challenge is to understand the behavioural consequences and cellular mechanisms underlying training-induced neuroanatomic plasticity in order to adapt treatment strategies for patients with brain injury or neurodegenerative disorders.
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              Short latency cerebellar modulation of the basal ganglia

              The graceful, purposeful motion of our body is an engineering feat which remains unparalleled in robotic devices using advanced artificial intelligence. Much of the information required for complex movements is generated by the cerebellum and the basal ganglia in conjunction with the cortex. Cerebellum and basal ganglia have been thought to communicate with each other only through slow multi-synaptic cortical loops, begging the question as to how they coordinate their outputs in real time. Here we show in mice that the cerebellum rapidly modulates the activity of the striatum via a disynaptic pathway. Under physiological conditions this short latency pathway is capable of facilitating optimal motor control by allowing the basal ganglia to incorporate time-sensitive cerebellar information and by guiding the sign of cortico-striatal plasticity. Conversely, under pathological condition this pathway relays aberrant cerebellar activity to the basal ganglia to cause dystonia.
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                Author and article information

                Journal
                Tremor Other Hyperkinet Mov (N Y)
                Tremor Other Hyperkinet Mov (N Y)
                TOHM
                Tremor and Other Hyperkinetic Movements
                Columbia University Libraries/Information Services
                2160-8288
                2017
                23 October 2017
                : 7
                : 506
                Affiliations
                [1 ]Departments of Neurology, Human Genetics and Pediatrics, Emory University, Atlanta, GA, USA
                [2 ]Department of Surgery, University Multiprofile Hospital for Active Treatment “Alexandrovska”, Medical University of Sofia, Sofia, Bulgaria
                [3 ]Departments of Pharmacology and Neurology, Emory University, Atlanta, GA, USA
                Yale University, USA
                Author notes
                *To whom correspondence should be addressed. E-mail: hjinnah@ 123456emory.edu
                Article
                10.7916/D8V69X3S
                5673689
                29123945
                3e07561e-5116-4888-9777-092f7056dc62
                © 2017 Jinnah et al.

                This is an open-access article distributed under the terms of the Creative Commons Attribution–Noncommerical–No Derivatives License, which permits the user to copy, distribute, and transmit the work provided that the original author and source are credited; that no commercial use is made of the work; and that the work is not altered or transformed.

                History
                : 21 August 2017
                : 25 September 2017
                Page count
                Pages: 15
                Categories
                Reviews

                dystonia,cervical dystonia,torticollis,blepharospasm,focal hand dystonia,laryngeal dystonia,spasmodic dysphonia,neuroanatomy,neuroimaging

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