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A Neuroanatomical Framework for Upper Limb Synergies after Stroke

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      Abstract

      Muscle synergies describe common patterns of co- or reciprocal activation that occur during movement. After stroke, these synergies change, often in stereotypical ways. The mechanism underlying this change reflects damage to key motor pathways as a result of the stroke lesion, and the subsequent reorganization along the neuroaxis, which may be further detrimental or restorative to motor function. The time course of abnormal synergy formation seems to lag spontaneous recovery that occurs in the initial weeks after stroke. In healthy individuals, motor cortical activity, descending via the corticospinal tract (CST) is the predominant driver of voluntary behavior. When the CST is damaged after stroke, other descending pathways may be up-regulated to compensate. The contribution of these pathways may emerge as new synergies take shape at the chronic stage after stroke, as a result of plasticity along the neuroaxis. The location of the stroke lesion and properties of the secondary descending pathways and their regulation are then critical for shaping the synergies in the remaining motor behavior. A consideration of the integrity of remaining descending motor pathways may aid in the design of new rehabilitation therapies.

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      Most cited references 48

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      Descending pathways in motor control.

       R. N. Lemon (2007)
      Each of the descending pathways involved in motor control has a number of anatomical, molecular, pharmacological, and neuroinformatic characteristics. They are differentially involved in motor control, a process that results from operations involving the entire motor network rather than from the brain commanding the spinal cord. A given pathway can have many functional roles. This review explores to what extent descending pathways are highly conserved across species and concludes that there are actually rather widespread species differences, for example, in the transmission of information from the corticospinal tract to upper limb motoneurons. The significance of direct, cortico-motoneuronal (CM) connections, which were discovered a little more than 50 years ago, is reassessed. I conclude that although these connections operate in parallel with other less direct linkages to motoneurons, CM influence is significant and may subserve some special functions including adaptive motor behaviors involving the distal extremities.
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        Influence of interhemispheric interactions on motor function in chronic stroke.

        In patients with chronic stroke, the primary motor cortex of the intact hemisphere (M1(intact hemisphere)) may influence functional recovery, possibly through transcallosal effects exerted over M1 in the lesioned hemisphere (M1(lesioned hemisphere)). Here, we studied interhemispheric inhibition (IHI) between M1(intact hemisphere) and M1(lesioned hemisphere) in the process of generation of a voluntary movement by the paretic hand in patients with chronic subcortical stroke and in healthy volunteers. IHI was evaluated in both hands preceding the onset of unilateral voluntary index finger movements (paretic hand in patients, right hand in controls) in a simple reaction time paradigm. IHI at rest and shortly after the Go signal were comparable in patients and controls. Closer to movement onset, IHI targeting the moving index finger turned into facilitation in controls but remained deep in patients, a finding that correlated with poor motor performance. These results document an abnormally high interhemispheric inhibitory drive from M1(intact hemisphere) to M1(lesioned hemisphere) in the process of generation of a voluntary movement by the paretic hand. It is conceivable that this abnormality could adversely influence motor recovery in some patients with subcortical stroke, an interpretation consistent with models of interhemispheric competition in motor and sensory systems.
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          Functional potential in chronic stroke patients depends on corticospinal tract integrity.

          Determining whether a person with stroke has reached their full potential for recovery is difficult. While techniques such as transcranial magnetic stimulation (TMS) and MRI have some prognostic value, their role in rehabilitation is undefined. This study used TMS and MRI to determine which factors predict functional potential, defined as an individual's capacity for further functional improvement at least 6 months following stroke. We studied 21 chronic stroke patients with upper limb impairment. The functional integrity of the corticospinal tracts (CSTs) was assessed using TMS and functional MRI. The presence or absence of motor-evoked responses (MEPs) to TMS in the affected upper limb, and the lateralization of cortical activity during affected hand use were determined. The structural integrity of the CST was assessed using MRI, and diffusion tensor imaging was used to measure the asymmetry in fractional anisotropy (FA) of the internal capsules. A multiple linear regression analysis was performed, to predict both clinical score at inception and change in clinical score for 17 patients who completed a 30 day programme of motor practice with the affected upper limb. The main findings were that in patients with MEPs, meaningful gains were still possible 3 years after stroke, although the capacity for improvement declined with time. In patients without MEPs, functional potential declines with increasing CST disruption, with no meaningful gains possible if FA asymmetry exceeds a value of 0.25. This study is the first to demonstrate the complementary nature of TMS and MRI techniques in predicting functional potential in chronic stroke patients. An algorithm is proposed for the selection of individualized rehabilitation strategies, based on the prediction of functional potential. These strategies could include neuromodulation using a range of emerging techniques, to prime the motor system for a plastic response to rehabilitation.
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            Author and article information

            Affiliations
            1Movement Neuroscience Laboratory, Department of Sport and Exercise Science, Centre for Brain Research, The University of Auckland , Auckland, New Zealand
            Author notes

            Edited by: Ana Bengoetxea, Universidad del País Vasco-Euskal Herriko Unibertsitatea, Spain

            Reviewed by: Jean-Louis Thonnard, Université Catholique de Louvain, Belgium; Aaron Batista, University of Pittsburgh, USA

            *Correspondence: Winston D. Byblow, Movement Neuroscience Laboratory, Department of Sport and Exercise Science, Centre for Brain Research, The University of Auckland, Private Bag 92019, Auckland 1142, New Zealand e-mail: w.byblow@ 123456auckland.ac.nz

            This article was submitted to the journal Frontiers in Human Neuroscience.

            Contributors
            URI : http://frontiersin.org/people/u/98789
            URI : http://frontiersin.org/people/u/176954
            URI : http://frontiersin.org/people/u/31692
            Journal
            Front Hum Neurosci
            Front Hum Neurosci
            Front. Hum. Neurosci.
            Frontiers in Human Neuroscience
            Frontiers Media S.A.
            1662-5161
            16 February 2015
            2015
            : 9
            4329797
            10.3389/fnhum.2015.00082
            Copyright © 2015 McMorland, Runnalls and Byblow.

            This is an open-access article distributed under the terms of the Creative Commons Attribution License (CC BY). The use, distribution or reproduction in other forums is permitted, provided the original author(s) or licensor are credited and that the original publication in this journal is cited, in accordance with accepted academic practice. No use, distribution or reproduction is permitted which does not comply with these terms.

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            Figures: 1, Tables: 0, Equations: 0, References: 48, Pages: 6, Words: 5666
            Categories
            Neuroscience
            Perspective Article

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