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, 141 (3), 837-847

Evidence for a Subcortical Origin of Mirror Movements After Stroke: A Longitudinal Study

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Evidence for a Subcortical Origin of Mirror Movements After Stroke: A Longitudinal Study

Naveed Ejaz et al. Brain.

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.

Figures

Figure 1
Figure 1
Assessment of mirror movements. (A) Both hands were strapped onto an ergonomic hand device capable of measuring isometric forces generated at the fingertips. Controls and patients were instructed to generate isometric forces by making individuated presses to bring the cursor (short white horizontal bars) into the target zone shown in green. During each measurement session, individuated finger presses were made at 20%, 40%, 60% and 80% of the maximum voluntary force (MVF) on that finger. (B) Sample of force traces produced in active and passive hand. Force presses with the instructed finger (thumb in right hand shown in red) resulted in involuntary forces on the passive fingers of the same hand (black), and subtle mirrored forces on the fingers of the passive hand (right). (C) Mirrored force trajectories were similar to that for the instructed finger, especially at higher target force levels. (D) Mirroring was quantified as the linear slope between the peak forces produced by the instructed finger and the peak averaged forces on the passive hand. The linear slope was log-transformed to allow the use of parametric statistical test, but for the purpose of clarity the raw values of the linear slope are reported in all subsequent figures.
Figure 2
Figure 2
Longitudinal changes in mirror movements and fine-finger control after stroke. (A) Changes in mirroring for controls and patients measured in the first year after stroke. Line plots are labelled by the active hand. For patients, mirroring was primarily measured in the fingers of the non-paretic hand, during active finger presses with the paretic hand. Mirroring in the paretic hand during non-paretic finger presses is also shown. (B) Associated changes in fine-finger control on the active hand across groups. Individuated finger presses in patients and controls resulted in undesired force contractions on the uninstructed fingers of the active hand. The larger these so-called enslaved movements, the worse the degree of fine-finger control. For clarity, the raw values of the linear-slope estimates for mirroring and enslaving are plotted in A and B. Group differences within each week are indicated by **P < 0.001 and *P < 0.01.
Figure 3
Figure 3
Evoked BOLD activities for finger presses in the primary somatosensory (S1) and motor (M1) cortices. (A) During the functional MRI task, patients and controls were required to produce either 1.8 N or 8% of the maximum voluntary force (MVF) on the instructed finger. Forces are expressed as a percentage of maximum voluntary force. Controls produced forces at ∼40% of maximum voluntary force. From Week 4 onwards, forces produced by patients and controls were not significantly different (Week ≥ 4; χ2 = 0.02, P = 0.887). (B) Measurements of mirroring on the non-paretic hand were highly correlated inside and outside the scanner environments. (C) Similarly, enslaving in the paretic hand was highly correlated for measurements inside and outside the scanner environments. Each dot in B and C represents the session measurement of a single patient. For clarity, the raw values of the linear-slope estimates for mirroring are plotted in B and C. (D) Evoked BOLD activities in contra- and ipsilateral S1 and M1 cortices due to paretic finger presses. Corresponding contra and ipsilateral activities in controls are depicted by the shaded green regions (mean ± SEM).
Figure 4
Figure 4
Relative contributions of homologous and non-homologous components to mirror movements on the non-paretic hand. (A) Mirroring across all possible active/passive finger pairs for controls and patients (on non-paretic hand only). Rows and columns denote which finger was pressed on the active hand, and the finger on the passive hand that mirroring was estimated on, respectively. Diagonal and off-diagonal matrix entries represent mirroring across homologous and non-homologous finger pairs. (B) Individuated finger presses by controls resulted in enslaved forces on the passive fingers of the same hand and mirrored forces across homologous and non-homologous finger pairs. The ratio between instructed/enslaved forces within the active hand is shown in green, while the ratio between homologous and non-homologous mirroring components is shown in white. Shown here are data for controls averaged across all five measurement sessions. (C) Changes in homologous and non-homologous mirroring components on the non-paretic hand in the year following stroke. For clarity, the raw values of the linear-slope estimates for mirroring are plotted. (D) For patients, the ratios between instructed/enslaved forces on the paretic hand, and the ratio between homologous/non-homologous mirroring patterns are shown in the left and right panels, respectively.
Figure 5
Figure 5
Stability of mirroring pattern during stroke recovery. (A) The average mirroring patterns across all active/passive finger pairs are shown for patients (Week 2) and controls. For clarity, the raw values of the linear-slope estimates for mirroring are plotted in A. Similarity between the patterns for patients and controls was high, even in the early period after stroke (Week 2, r = 0.88, P ≪ 0.0001). (B) Correlations between mirroring patterns for patients and controls remained unchanged throughout recovery (χ2 = 1.87, P = 0.760). The pattern correlations for patients and controls were also close to noise ceilings; i.e. the maximum possible pattern correlations possible given the measurement noise on mirroring patterns for each control (see ‘Materials and methods’ section).

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