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      Motor recovery and microstructural change in rubro-spinal tract in subcortical stroke ☆

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          Abstract

          The mechanism of motor recovery after stroke may involve reorganization of the surviving networks. However, details of adaptive changes in structural connectivity are not well understood. Here, we show long-term changes in white matter microstructure that relate to motor recovery in stroke patients. We studied ten subcortical ischemic stroke patients who showed motor hemiparesis at the initial clinical examination and an infarcted lesion centered in the posterior limb of internal capsule of the unilateral hemisphere at the initial diffusion-weighted magnetic resonance imaging scan. The participants underwent serial diffusion tensor imaging and motor function assessments at three consecutive time points; within 2 weeks, and at 1 and 3 months after the onset. Fractional anisotropy (FA) was analyzed for regional differences between hemispheres and time points, as well as for correlation with motor recovery using a tract-based spatial statistics analysis. The results showed significantly increased FA in the red nucleus and dorsal pons in the ipsi-lesional side at 3 months, and significantly decreased FA in the ipsi-lesional internal capsule at all time points, and in the cerebral peduncle, corona radiata, and corpus callosum at 3 months. In the correlation analysis, FA values of clusters in the red nucleus, dorsal pons, midbody of corpus callosum, and cingulum were positively correlated with recovery of motor function. Our study suggests that changes in white matter microstructure in alternative descending motor tracts including the rubro-spinal pathway, and interhemispheric callosal connections may play a key role in compensating for motor impairment after subcortical stroke.

          Highlights

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            Subcortical stroke patients showed motor hemiparesis followed by gradual recovery.

          • •

            Lesion overlap was located with its center in the posterior limb of internal capsule.

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            Fractional anisotropy (FA) gradually increased in the red nucleus in three months.

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            FA in the red nucleus was positively correlated with recovery of motor paresis.

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            FA in the middle part of corpus callosum was also correlated with motor recovery.

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          Most cited references35

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          The role of ipsilateral premotor cortex in hand movement after stroke.

          S Wimalaratna, Heidi Johansen-Berg, Udo Kischka … (2002)
          Movement of an affected hand after stroke is associated with increased activation of ipsilateral motor cortical areas, suggesting that these motor areas in the undamaged hemisphere may adaptively compensate for damaged or disconnected regions. However, this adaptive compensation has not yet been demonstrated directly. Here we used transcranial magnetic stimulation (TMS) to interfere transiently with processing in the ipsilateral primary motor or dorsal premotor cortex (PMd) during finger movements. TMS had a greater effect on patients than controls in a manner that depended on the site, hemisphere, and time of stimulation. In patients with right hemiparesis (but not in healthy controls), TMS applied to PMd early (100 ms) after the cue to move slowed simple reaction-time finger movements by 12% compared with controls. The relative slowing of movements with ipsilateral PMd stimulation in patients correlated with the degree of motor impairment, suggesting that functional recruitment of ipsilateral motor areas was greatest in the more impaired patients. We also used functional magnetic resonance imaging to monitor brain activity in these subjects as they performed the same movements. Slowing of reaction time after premotor cortex TMS in the patients correlated inversely with the relative hemispheric lateralization of functional magnetic resonance imaging activation in PMd. This inverse correlation suggests that the increased activation in ipsilateral cortical motor areas during movements of a paretic hand, shown in this and previous functional imaging studies, represents a functionally relevant, adaptive response to the associated brain injury.
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            Early prediction of outcome of activities of daily living after stroke: a systematic review.

            J M Veerbeek, Martijn W. Heymans, Erik Limbergen … (2011)
            Knowledge about robust and unbiased factors that predict outcome of activities of daily living (ADL) is paramount in stroke management. This review investigates the methodological quality of prognostic studies in the early poststroke phase for final ADL to identify variables that are predictive or not predictive for outcome of ADL after stroke. PubMed, Ebsco/Cinahl and Embase were systematically searched for prognostic studies in which stroke patients were included ≤2 weeks after onset and final outcome of ADL was determined ≥3 months poststroke. Risk of bias scores were used to distinguish high- and low-quality studies and a qualitative synthesis was performed. Forty-eight of 8425 identified citations were included. The median risk of bias score was 17 out of 27 (range, 6-22) points. Most studies failed to report medical treatment applied, management of missing data, rationale for candidate determinants and outcome cut-offs, results of univariable analysis, and validation and performance of the model, making the predictive value of most determinants indistinct. Six high-quality studies showed strong evidence for baseline neurological status, upper limb paresis, and age as predictors for outcome of ADL. Gender and risk factors such as atrial fibrillation were unrelated to this outcome. Because of insufficient methodological quality of most prognostic studies, the predictive value of many clinical determinants for outcome of ADL remains unclear. Future cohort studies should focus on early prediction using simple models with good clinical performance to enhance application in stroke management and research.
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              Activation likelihood estimation meta-analysis of motor-related neural activity after stroke.

              Anne K. Rehme, Simon B. Eickhoff, Claudia Rottschy … (2012)
              Over the past two decades, several functional neuroimaging experiments demonstrated changes in neural activity in stroke patients with motor deficits. Conclusions from single experiments are usually constrained by small sample sizes and high variability across studies. Here, we used coordinate-based activation likelihood estimation meta-analyses to provide a quantitative synthesis of the current literature on motor-related neural activity after stroke. Of over 1000 PubMed search results through January 2011, 36 studies reported standardized whole-brain group coordinates. Meta-analyses were performed on 54 experimental contrasts for movements of the paretic upper limb (472 patients, 452 activation foci) and on 20 experiments comparing activation between patients and healthy controls (177 patients, 113 activation foci). We computed voxelwise correlations between activation likelihood and motor impairment, time post-stroke, and task difficulty across samples. Patients showed higher activation likelihood in contralesional primary motor cortex (M1), bilateral ventral premotor cortex and supplementary motor area (SMA) relative to healthy subjects. Activity in contralesional areas was more likely found for active than for passive tasks. Better motor performance was associated with greater activation likelihood in ipsilesional M1, pre-SMA, contralesional premotor cortex and cerebellum. Over time post-stroke, activation likelihood in bilateral premotor areas and medial M1 hand knob decreased. This meta-analysis shows that increased activation in contralesional M1 and bilateral premotor areas is a highly consistent finding after stroke despite high inter-study variance resulting from different fMRI tasks and motor impairment levels. However, a good functional outcome relies on the recruitment of the original functional network rather than on contralesional activity. Copyright © 2011 Elsevier Inc. All rights reserved.
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                Author and article information

                Journal
                Journal ID (nlm-ta): Neuroimage Clin
                Journal ID (iso-abbrev): Neuroimage Clin
                Title: NeuroImage : Clinical
                Publisher: Elsevier
                ISSN (Electronic): 2213-1582
                Publication date PMC-release: 13 December 2013
                Publication date (Electronic): 13 December 2013
                Publication date Collection: 2014
                Volume: 4
                Pages: 201-208
                Affiliations
                [a ]Division of Neurology, Department of Stroke and Cerebrovascular Diseases, National Cerebral and Cardiovascular Center, Osaka, Japan
                [b ]Human Brain Research Center, Kyoto University Graduate School of Medicine, Kyoto, Japan
                [c ]Functional Architecture Imaging Unit, RIKEN Center for Life Science Technologies, Kobe, Japan
                [d ]Department of Neurology, Kansai Rosai Hospital, Hyogo, Japan
                Author notes
                [* ]Corresponding author at: Functional Architecture Imaging Unit, RIKEN Center for Life Science Technologies, 6-7-3 Minatojima-minamimachi, Chuo-ku, Kobe, Hyogo 650-0047, Japan. Tel.: + 81 78 304 7140; fax: + 81 78 304 7141. takuya.hayashi@ 123456riken.jp
                [1]

                Present addresses: Department of Neurology, Senri Chuo Hospital, Osaka, Japan.

                Article
                Publisher ID: S2213-1582(13)00162-9
                DOI: 10.1016/j.nicl.2013.12.003
                PMC ID: 3891492
                PubMed ID: 24432247
                SO-VID: 23d5a816-1a49-45b3-860f-4e03b4431961
                Copyright © © 2013 The Authors
                License:

                This is an open-access article distributed under the terms of the Creative Commons Attribution-NonCommercial-No Derivative Works License, which permits non-commercial use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                Date received : 18 October 2013
                Date revision received : 2 December 2013
                Date accepted : 5 December 2013
                Categories
                Subject: Article

                Keywords: cr, corona radiata,ept, extrapyramidal tract,fa, fractional anisotropy,pt, pyramidal tract,tbss, tract-based spatial statistics,motor recovery,subcortical stroke,cc, corpus callosum,cp, cerebral peduncle,dti, diffusion tensor imaging,fmms, fugl-meyer motor scale,plic, posterior limb of internal capsule,reorganization,diffusion tensor image,tract-based spatial statistics
                Data availability:
                Keywords: cr, corona radiata, ept, extrapyramidal tract, fa, fractional anisotropy, pt, pyramidal tract, tbss, tract-based spatial statistics, motor recovery, subcortical stroke, cc, corpus callosum, cp, cerebral peduncle, dti, diffusion tensor imaging, fmms, fugl-meyer motor scale, plic, posterior limb of internal capsule, reorganization, diffusion tensor image, tract-based spatial statistics

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