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.

Differential involvement of cortical and cerebellar areas using dominant and nondominant hands: An FMRI study

“…Dynamic power grip designs, similar to the one used in this study, have previously been shown to be a powerful way to investigate motor functions in healthy controls, aging, and stroke disease [Boudrias et al, 2012; Talelli et al, 2008; Ward et al, 2006]. In the current study, task performance was consistent using either hand for all subjects, both in terms of reaching the required GF target and maintaining the grip force for the specified duration.…”

“…Previous fMRI GF studies focused on the effect of different forces applied using the DH [Keisker et al, 2009; Kuhtz‐Buschbeck et al, 2008; Spraker et al, 2012; Talelli et al, 2008; Ward et al, 2006, 2007, 2008]. In these studies, the regions responded in a linear fashion and were mainly localised with the CL M1 and IL cerebellum.…”

Secondary Degeneration Detected by Combining Voxel-Based Morphometry and Tract-Based Spatial Statistics in Subcortical Strokes with Different Outcomes in Hand Function

“…9,22 The impaired functional integrity of the corticospinal system may recruit secondary motor networks in both hemispheres to generate motor output to spinal cord motor neurons, but the secondary motor networks are less efficient at generating motor output, so this type of reorganization can be only partly successful in reducing motor deficits after stroke. 10 Therefore, the outcome of motor function is likely to be attributed to the degree of damage of the primary motor system. Our findings suggest that the degree of secondary degeneration above the primary lesion correlates with the outcomes in hand function.…”

“…9 Cerebral reorganization has been consistently demonstrated in patients with stroke by use of functional MR imaging, which depends on the integrity of the corticospinal system. 10 However, regions where secondary degeneration contributes to differences of cerebral reorganization have not been completely identified. Moreover, the relationships between outcomes in hand function and secondary degeneration of the motor system are not clearly understood.…”

Structural Plasticity of Remote Cortical Brain Regions is Determined by Connectivity to the Primary Lesion in Subcortical Stroke

“…In the neuroimaging literature, reorganization within wide-spread functional brain networks have been described. [5][6][7][8] In addition, changes of white-matter properties were observed in areas both adjacent to and remote from ischemic lesions reflecting secondary degeneration. [9][10][11] Only few studies have focused on changes of cortical gray matter after stroke using conventional volumetric measurements, 12 voxel-based morphometry, 13,14 or CT measurements.…”