Abstract
Deficits in proprioception, the ability to discriminate the relative position and movement of our limbs, affect ~50% of stroke patients and reduce functional outcomes. Our lack of knowledge of the anatomical correlates of proprioceptive processing limits our understanding of the impact that such deficits have on recovery. This research investigated the relationship between functional impairment in brain activity and proprioception post-stroke. We developed a novel device and task for arm position matching during functional MRI (fMRI), and investigated 16 subjects with recent stroke and nine healthy age-matched controls. The stroke-affected arm was moved by an experimenter (passive arm), and subjects were required to match the position of this limb with the opposite arm (active arm). Brain activity during passive and active arm movements was determined, as well as activity in association with performance error. Passive arm movement in healthy controls was associated with activity in contralateral primary somatosensory (SI) and motor cortices (MI), bilateral parietal cortex, supplementary (SMA) and premotor cortices, secondary somatosensory cortices (SII), and putamen. Active arm matching was associated with activity in contralateral SI, MI, bilateral SMA, premotor cortex, putamen, and ipsilateral cerebellum. In subjects with stroke, similar patterns of activity were observed. However, in stroke subjects, greater proprioceptive error was associated with less activity in ipsilesional supramarginal and superior temporal gyri, and lateral thalamus. During active arm movement, greater proprioceptive error was associated with less activity in bilateral SMA and ipsilesional premotor cortex. Our results enhance our understanding of the correlates of proprioception within the temporal parietal cortex and supplementary/premotor cortices. These findings also offer potential targets for therapeutic intervention to improve proprioception in recovering stroke patients and thus improve functional outcome.
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Acknowledgements
The present work was supported by a Canadian Institutes of Health Research (MOP 106662) operating grant, a Heart and Stroke Foundation of Canada Grant-in-Aid (G-13-0003029), an Alberta Innovates–Health Solutions Team Grant (201500788), and an Ontario Research Fund Grant (ORF-RE 04-47). JK was supported by an Alberta Innovates–Health Solutions MD/PhD Studentship. Special thanks to Janice Yajure and Mark Piitz for subject recruitment and assessment.
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Supplementary Figure 1
Images of mean brain activity for the control tasks (n = 8) (event related designs). Each of the following stimuli were modeled independently using a general linear model, with each movement/trial (20 per run) representing a single event A. Visual cues only. B. Active right arm movements without matching position of the left arm. C. Active left arm movements without matching position of the right arm. D. Motor imagery of the right arm matching the left arm position. E. Motor imagery of the left arm matching the right arm position. All statistical images were thresholded using an initial cluster forming threshold of z > 2.3 and a (corrected) cluster significance threshold of p = 0.01. Reduced activity during a task is presented in blue-green. MNI coordinates are presented above each axial slice. Surface rendered whole brain images are presented in the right three columns. (PNG 2510 kb)
Supplementary Figure 2
Images of the difference in brain activity between the control tasks and the position-matching task in control subjects (n = 8). Contrasts were calculated using paired t-tests to determine whether there was greater brain activation during one stimulus over another A. Active right arm matching > active right arm movement without matching (control task 2). B. Active left arm matching > active left arm movement without matching (control task 2). C. Active right arm matching > motor imagery of right arm matching (control task 3). D. Active left arm matching > motor imagery of left arm matching (control task 3). All statistical images were thresholded using an initial cluster forming threshold of z > 2.3 and a (corrected) cluster significance threshold of p = 0.01. X > Y indicates areas where X had significantly greater BOLD activation than Y. MNI coordinates are presented above each axial slice. Surface rendered whole brain images are presented in the right three columns. (PNG 1861 kb)
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Kenzie, J.M., Findlater, S.E., Pittman, D.J. et al. Errors in proprioceptive matching post-stroke are associated with impaired recruitment of parietal, supplementary motor, and temporal cortices. Brain Imaging and Behavior 13, 1635–1649 (2019). https://doi.org/10.1007/s11682-019-00149-w
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DOI: https://doi.org/10.1007/s11682-019-00149-w