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Motor system activation after subcortical stroke depends on corticospinal system integrity.

ABSTRACT: Movement-related brain activation patterns after subcortical stroke are characterized by relative overactivations in cortical motor areas compared with controls. In patients able to perform a motor task, overactivations are greater in those with more motor impairment. We hypothesized that recruitment of motor regions would shift from primary to secondary motor networks in response to impaired functional integrity of the corticospinal system (CSS). We measured the magnitude of brain activation using functional MRI during a motor task in eight chronic subcortical stroke patients. CSS functional integrity was assessed using transcranial magnetic stimulation to obtain stimulus/response curves for the affected first dorsal interosseus muscle, with a shallower gradient representing increasing disruption of CSS functional integrity. A negative correlation between the gradient of stimulus/response curve and magnitude of task-related brain activation was found in several motor-related regions, including ipsilesional posterior primary motor cortex [Brodmann area (BA) 4p], contralesional anterior primary motor cortex (BA 4a), bilateral premotor cortex, supplementary motor area, intraparietal sulcus, dorsolateral prefrontal cortex and contralesional superior cingulate sulcus. There were no significant positive correlations in any brain region. These results suggest that impaired functional integrity of the CSS is associated with recruitment of secondary motor networks in both hemispheres in an attempt to generate motor output to spinal cord motoneurons. Secondary motor regions are less efficient at generating motor output so this reorganization can only be considered partially successful in reducing motor impairment after stroke.

SUBMITTER: Ward NS

PROVIDER: S-EPMC3717515 | biostudies-literature | 2006 Mar

REPOSITORIES: biostudies-literature

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Motor system activation after subcortical stroke depends on corticospinal system integrity.

Ward Nick S NS Newton Jennifer M JM Swayne Orlando B C OB Lee Lucy L Thompson Alan J AJ Greenwood Richard J RJ Rothwell John C JC Frackowiak Richard S J RS

Brain : a journal of neurology 20060118 Pt 3

Movement-related brain activation patterns after subcortical stroke are characterized by relative overactivations in cortical motor areas compared with controls. In patients able to perform a motor task, overactivations are greater in those with more motor impairment. We hypothesized that recruitment of motor regions would shift from primary to secondary motor networks in response to impaired functional integrity of the corticospinal system (CSS). We measured the magnitude of brain activation us ...[more]

PMID: 16421171

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Project description:BackgroundPreserved integrity of the corticospinal tract (CST) is a marker of good upper-limb behavior and recovery following stroke. However, there is less understanding of neural mechanisms that might help facilitate upper-limb motor recovery in stroke survivors with extensive CST damage.ObjectiveThe purpose of this study was to investigate resting state functional connectivity in chronic stroke survivors with different levels of CST damage and to explore neural correlates of greater upper-limb motor performance in stroke survivors with compromised ipsilesional CST integrity.MethodsThirty chronic stroke survivors (24 males, aged 64.7 ± 10.8 years) participated in this study. Three experimental sessions were conducted to: 1) obtain anatomical (T1, T2) structural (diffusion) and functional (resting state) MRI sequences, 2) determine CST integrity with transcranial magnetic stimulation (TMS) and conduct assessments of upper-limb behavior, and 3) reconfirm CST integrity status. Participants were divided into groups according to the extent of CST damage. Those in the extensive CST damage group did not show TMS evoked responses and had significantly lower ipsilesional fractional anisotropy.ResultsOf the 30 chronic stroke survivors, 12 were categorized as having extensive CST damage. Stroke survivors with extensive CST damage had weaker functional connectivity in the ipsilesional sensorimotor network and greater functional connectivity in the ipsilesional fronto-parietal network compared to those with preserved CST integrity. For participants with extensive CST damage, improved motor performance was associated with greater functional connectivity of the ipsilesional fronto-parietal network and higher fractional anisotropy of the ipsilesional rostral superior longitudinal fasciculus.ConclusionsStroke survivors with extensive CST damage have greater resting state functional connectivity of an ipsilesional fronto-parietal network that appears to be a behaviorally relevant neural mechanism that improves upper-limb motor performance.

Project description:The structural integrity of the corticospinal tract (CST) after stroke is closely linked to the degree of motor impairment. Simple and reliable methods of assessing white matter integrity within the CST would facilitate the use of this measure in routine clinical practice. Commonly, diffusion tensor imaging is used to measure voxel-wise fractional anisotropy (FA) in a variety of regions of interest (ROIs) representing the CST. Several methods are currently in use with no consensus about which approach is best. ROIs are usually either the whole CST or the posterior limb of the internal capsule (PLIC). These are created manually on brain images or with reference to an individual's CST determined by tractography. Once the ROI has been defined, the FA can be reported as an absolute measure from the ipsilesional side or as a ratio in comparison to the contralesional side. Both corticospinal tracking and manual ROI definition in individual stroke patients are time consuming and subject to bias. Here, we investigated whether using a CST template derived from healthy volunteers was a feasible method for defining the appropriate ROI within which to measure changes in FA. We reconstructed the CST connecting the primary motor cortex to the ipsilateral pons in 23 age-matched control subjects and 21 stroke patients. An average healthy CST template was created from the 23 control subjects. For each patient, FA values were then calculated for both the template CST and for their own CST. We compared patients' FA metrics between the two tracts by considering four measures (FA in the ipsilesional side, FA in the contralesional side, FA ratio of the ipsilesional side to the contralesional side and FA asymmetry between the two sides) and in two tract-based ROIs (whole tract and tract section traversing the PLIC). There were no significant differences in FA metrics for either method, except for contralesional FA. Furthermore, we found that FA metrics relating to CST damage all correlated with motor ability post-stroke equally well. These results suggest that the healthy CST template could be a surrogate structure for defining tract-based ROIs with which to measure stroke patients' FA metrics, avoiding the necessity for CST tracking in individual patients. CST template-based automated quantification of structural integrity would greatly facilitate implementation of practical clinical applications of diffusion tensor imaging.

Project description:ObjectiveStudies on upper limb recovery following stroke have highlighted the importance of the structural and functional integrity of the corticospinal tract (CST) in determining clinical outcomes. However, such relationships have not been fully explored for the lower limb. We aimed to test whether variation in walking impairment was associated with variation in the structural or functional integrity of the CST.MethodsTranscranial magnetic stimulation was used to stimulate each motor cortex while EMG recordings were taken from the vastus lateralis (VL) bilaterally; these EMG measures were used to calculate both ipsilateral and contralateral recruitment curves for each lower limb. The slope of these recruitment curves was used to examine the strength of functional connectivity from the motor cortex in each hemisphere to the lower limbs in chronic stroke patients and to calculate a ratio between ipsilateral and contralateral outputs referred to as the functional connectivity ratio (FCR). The structural integrity of the CST was assessed using diffusion tensor MRI to measure the asymmetry in fractional anisotropy (FA) of the internal capsule. Lower limb impairment and walking speed were also measured.ResultsThe FCR for the paretic leg correlated with walking impairment, such that greater relative ipsilateral connectivity was associated with slower walking speeds. Asymmetrical FA values, reflecting reduced structural integrity of the lesioned CST, were associated with greater walking impairment. FCR and FA asymmetry were strongly positively correlated with each other.ConclusionsPatients with relatively greater ipsilateral connectivity between the contralesional motor cortex and the paretic lower limb were more behaviorally impaired and had more structural damage to their ipsilesional hemisphere CST.SignificanceMeasures of structural and functional damage may be useful in the selection of therapeutic strategies, allowing for more tailored and potentially more beneficial treatments.

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Motor system activation after subcortical stroke depends on corticospinal system integrity.

Publications

Motor system activation after subcortical stroke depends on corticospinal system integrity.

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