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Synergistic but independent: The role of corticospinal and alternate motor fibers for residual motor output after stroke.

ABSTRACT: BACKGROUND:Brain imaging has shown that not only the cortico-spinal tract (CST), but also alternate corticofugal motor fibers (aMF), such as the cortico-rubro-spinal and cortico-reticulo-spinal tract, influence residual motor output after stroke. So far, studies mainly have investigated each tract separately. A combined analysis of CST and aMF with assessment of their interactive role, i.e., that structural integrity of one tract influences the functional role of the structural integrity of the other, is pending. METHODS:39 late subacute stroke patients (aged 59.4 ± 12.0 years, 100 ± 11 days after stroke) were included. Probabilistic tractography was used to reconstruct CST and aMF. Fractional anisotropy (FA) was calculated as a measure of microstructural integrity. Multiple-linear-regression analysis was used to associate tract-related FA with residual motor output and to determine interactions between CST and aMF. RESULTS:Both CST (coefficient = 3.93, p < 0.0001) and aMF (coefficient = - 4.43, p = 0.003) of the affected hemisphere significantly contributed to residual motor output. An interaction of their impacts with a consecutive influence on motor output was not detected (p = 0.882). Thus, these data suggest that aMF and CST explain residual motor output in stroke patients in a synergistic, but mainly independent manner. CONCLUSIONS:The structural states of the CST and also - to a smaller degree - of the aMF correlate with residual motor output in late subacute stroke patients. Based on this statistical modeling with all inherent limitations, the novel finding of an absence of a significant interaction between both tracts in regard of their functional role, suggests that both corticofugal pathways act synergistically but largely independently. These findings add to the understanding of the functional role of different corticofugal motor fibers and their interactions for motor output after stroke.

SUBMITTER: Schulz R

PROVIDER: S-EPMC5426012 | biostudies-literature | 2017

REPOSITORIES: biostudies-literature

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Synergistic but independent: The role of corticospinal and alternate motor fibers for residual motor output after stroke.

Schulz Robert R Park Eunhee E Lee Jungsoo J Chang Won Hyuk WH Lee Ahee A Kim Yun-Hee YH Hummel Friedhelm C FC

NeuroImage. Clinical 20170419

<h4>Background</h4>Brain imaging has shown that not only the cortico-spinal tract (CST), but also alternate corticofugal motor fibers (aMF), such as the cortico-rubro-spinal and cortico-reticulo-spinal tract, influence residual motor output after stroke. So far, studies mainly have investigated each tract separately. A combined analysis of CST and aMF with assessment of their interactive role, i.e., that structural integrity of one tract influences the functional role of the structural integrity ...[more]

PMID: 28516034

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Project description:Anisotropy of descending motor pathways has repeatedly been linked to the severity of motor impairment following stroke-related damage to the corticospinal tract. Despite promising findings consistently tying anisotropy of the ipsilesional corticospinal tract to motor outcome, anisotropy is not yet utilized as a biomarker for motor recovery in clinical practice as several methodological constraints hinder a conclusive understanding of degenerative processes in the ipsilesional corticospinal tract and compensatory roles of other descending motor pathways. These constraints include estimating anisotropy in voxels with multiple fibre directions, sampling biases and confounds due to ageing-related atrophy. The present study addressed these issues by combining diffusion spectrum imaging with a novel compartmentwise analysis approach differentiating voxels with one dominant fibre direction (one-directional voxels) from voxels with multiple fibre directions. Compartmentwise anisotropy for bihemispheric corticospinal and extrapyramidal tracts was compared between 25 chronic stroke patients, 22 healthy age-matched controls, and 24 healthy young controls and its associations with motor performance of the upper and lower limbs were assessed. Our results provide direct evidence for Wallerian degeneration along the entire length of the ipsilesional corticospinal tract reflected by decreased anisotropy in descending fibres compared with age-matched controls, while ageing-related atrophy was observed more ubiquitously across compartments. Anisotropy of descending ipsilesional corticospinal tract voxels showed highly robust correlations with various aspects of upper and lower limb motor impairment, highlighting the behavioural relevance of Wallerian degeneration. Moreover, anisotropy measures of two-directional voxels within bihemispheric rubrospinal and reticulospinal tracts were linked to lower limb deficits, while anisotropy of two-directional contralesional rubrospinal voxels explained gross motor performance of the affected hand. Of note, the relevant extrapyramidal structures contained fibres crossing the midline, fibres potentially mitigating output from brain stem nuclei, and fibres transferring signals between the extrapyramidal system and the cerebellum. Thus, specific parts of extrapyramidal pathways seem to compensate for impaired gross arm and leg movements incurred through stroke-related corticospinal tract lesions, while fine motor control of the paretic hand critically relies on ipsilesional corticospinal tract integrity. Importantly, our findings suggest that the extrapyramidal system may serve as a compensatory structural reserve independent of post-stroke reorganization of extrapyramidal tracts. In summary, compartment-specific anisotropy of ipsilesional corticospinal tract and extrapyramidal tracts explained distinct aspects of motor impairment, with both systems representing different pathophysiological mechanisms contributing to motor control post-stroke. Considering both systems in concert may help to develop diffusion imaging biomarkers for specific motor functions after stroke.

Project description:BackgroundMotor outcome after stroke is associated with reorganisation of cortical networks and corticospinal tract (CST) integrity. However, the relationships between motor severity, CST damage, and functional brain connectivity are not well understood. Here, the main objective was to study the effect of CST damage on the relationship between functional motor network connectivity and hand motor function in two groups of stroke patients: the severely (n=8) and the mildly impaired (n=14).MethodsTwenty-two carotid stroke patients with motor deficits were studied with magnetic resonance imaging (MRI) at 3 weeks, at 3 and 6 months. Healthy subjects (n=28) were scanned once. The CST injury was assessed by fractional anisotropy values. Functional connectivity was studied from a whole-hand grip task fMRI in a cortical and cerebellar motor network. Functional connectivity indexes were computed between these regions at each time point. The relationship between hand motor strength, ipsilesional CST damage and functional connectivity from the primary motor cortex (M1) was investigated using global and partial correlations.FindingsIn mildly impaired patients, cortico-cortical connectivity was disturbed at three weeks but returned to a normal pattern after 3 months. Cortico-cerebellar connectivity was still decreased at 6 months. In severely impaired patients, the cortico-cortical connectivity tended to return to a normal pattern, but the cortico-cerebellar connectivity was totally abolished during the follow-up. In the entire group of patients, the hand motor strength was correlated to the ipsilesional functional connectivity from M1. Partial correlations revealed that these associations were not anymore significant when the impact of CST damage was removed, except for the ipsilesional M1-contralateral cerebellum connectivity.ConclusionFunctional brain connectivity changes can be observed, even in severely impaired patients with no recovery. Upper limb function is mainly explained by the CST damage and by the ipsilesional cortico-cerebellar connectivity.

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Synergistic but independent: The role of corticospinal and alternate motor fibers for residual motor output after stroke.

Publications

Synergistic but independent: The role of corticospinal and alternate motor fibers for residual motor output after stroke.

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