Evidence for a subcortical origin of mirror movements after stroke: a longitudinal study

Abstract

Following a stroke, mirror movements are unintended movements that appear in the non-paretic hand when the paretic hand voluntarily moves. Mirror movements have previously been linked to overactivation of sensorimotor areas in the non-lesioned hemisphere. In this study, we hypothesized that mirror movements might instead have a subcortical origin, and are the by-product of subcortical motor pathways upregulating their contributions to the paretic hand. To test this idea, we first characterized the time course of mirroring in 53 first-time stroke patients, and compared it to the time course of activities in sensorimotor areas of the lesioned and non-lesioned hemispheres (measured using functional MRI). Mirroring in the non-paretic hand was exaggerated early after stroke (Week 2), but progressively diminished over the year with a time course that parallelled individuation deficits in the paretic hand. We found no evidence of cortical overactivation that could explain the time course changes in behaviour, contrary to the cortical model of mirroring. Consistent with a subcortical origin of mirroring, we predicted that subcortical contributions should broadly recruit fingers in the non-paretic hand, reflecting the limited capacity of subcortical pathways in providing individuated finger control. We therefore characterized finger recruitment patterns in the non-paretic hand during mirroring. During mirroring, non-paretic fingers were broadly recruited, with mirrored forces in homologous fingers being only slightly larger (1.76 times) than those in non-homologous fingers. Throughout recovery, the pattern of finger recruitment during mirroring for patients looked like a scaled version of the corresponding control mirroring pattern, suggesting that the system that is responsible for mirroring in controls is upregulated after stroke. Together, our results suggest that post-stroke mirror movements in the non-paretic hand, like enslaved movements in the paretic hand, are caused by the upregulation of a bilaterally organized subcortical system.

Motor Overflow and Spasticity in Chronic Stroke Share a Common Pathophysiological Process: Analysis of Within-Limb and Between-Limb EMG-EMG Coherence

“…As such, the alpha-band coherence in this study is most likely a release from cortical control, and is consistent with a reticulospinal drive ( 21 ). This view is supported by the findings from a recent longitudinal study ( 41 ).…”

Further evidence for a non-cortical origin of mirror movements after stroke

“…The lack of correlation with time since stroke differs from Ejaz et al, who used a longitudinal, as opposed to our study's cross-sectional design. That the CCC AH and fMRI activation maps acquired while patients carried out the same task did not correlate agrees with Ejaz et al (Ejaz et al, 2018), and also with Gerloff et al (Gerloff et al, 2006) who reported significant contralesional M1 overactivation in stroke patients without significant MMs, as determined by EMG coherence. Earlier literature reviews had F o r P e e r R e v i e w already underlined the frequent dissociation between clinically overt MMs and cSM1 overactivations (Calautti et al, 2003).…”

“…In their article, Ejaz et al (Ejaz et al, 2018) interpret the lack of cSM1 overactivation despite MMs, and the observed pattern of MMs with individuated finger presses, as consistent with a brainstem involvement in post-stroke MMs, more specifically the rubrospinal and/or reticulospinal pathways.…”

“…Ejaz et al (Ejaz et al, 2018) are to be commended for showing no evidence for a cortical origin of post-stroke mirror movements (MMs). Using functional MRI (fMRI) during affected-finger presses in recovering adult-onset stroke patients, they found no consistent relationship between contralesional sensorimotor cortex (cSM1) activation and quantitative indices of MMs; specifically, MMs were not linked to the presence of cSM1 overactivation, arguing against the 'transcallosal' mechanism classically believed to cause MMs (Di Pino et al, 2014).…”

Brain–Machine Interface Induced Morpho-Functional Remodeling of the Neural Motor System in Severe Chronic Stroke

“…In addition, the cerebellum can also influence the inhibitory motor network at the cortical level [105]. On the other hand, it has been suggested that after stroke, mirror movements might be mediated by subcortical instead of cortical networks, suggesting involvement of rubrospinal and reticulospinal pathways [106,107].…”