The impact of lesion side on bilateral upper limb coordination after stroke

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The impact of lesion side on bilateral upper limb coordination after stroke

• Pei-Cheng Shih,
• Christopher J. Steele,
• Dennis Hoepfel,
• Toni Muffel,
• Arno Villringer &
• Bernhard Sehm 

Journal of NeuroEngineering and Rehabilitation volume 20, Article number: 166 (2023) Cite this article

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Abstract

Background

A stroke frequently results in impaired performance of activities of daily life. Many of these are highly dependent on effective coordination between the two arms. In the context of bimanual movements, cyclic rhythmical bilateral arm coordination patterns can be classified into two fundamental modes: in-phase (bilateral homologous muscles contract simultaneously) and anti-phase (bilateral muscles contract alternately) movements. We aimed to investigate how patients with left (LHS) and right (RHS) hemispheric stroke are differentially affected in both individual-limb control and inter-limb coordination during bilateral movements.

Methods

We used kinematic measurements to assess bilateral coordination abilities of 18 chronic hemiparetic stroke patients (9 LHS; 9 RHS) and 18 age- and sex-matched controls. Using KINARM upper-limb exoskeleton system, we examined individual-limb control by quantifying trajectory variability in each hand and inter-limb coordination by computing the phase synchronization between hands during anti- and in-phase movements.

Results

RHS patients exhibited greater impairment in individual- and inter-limb control during anti-phase movements, whilst LHS patients showed greater impairment in individual-limb control during in-phase movements alone. However, LHS patients further showed a swap in hand dominance during in-phase movements.

Conclusions

The current study used individual-limb and inter-limb kinematic profiles and showed that bilateral movements are differently impaired in patients with left vs. right hemispheric strokes. Our results demonstrate that both fundamental bilateral coordination modes are differently controlled in both hemispheres using a lesion model approach. From a clinical perspective, we suggest that lesion side should be taken into account for more individually targeted bilateral coordination training strategies.

Trial registration: the current experiment is not a health care intervention study.

Background

Although various effective rehabilitation programs have been developed over the past decades, over half of chronic stroke patients still experience difficulty in achieving daily activities with their upper limbs [1]. Upper limb impairments can be characterized by impaired control of movement of the contralesional arm and difficulty in coordinating the limbs, both of which impact on quality of life [2, 3]. Rehabilitation after stroke focuses predominantly on treating the contralesional arm. However, our daily activities are highly dependent on the coordination between the two arms, and this has received far less attention [4]. Understanding the characteristics and mechanisms of bilateral coordination impairments after hemiparesis is therefore crucially needed to develop effective rehabilitation strategies.

Among the broad repertoire of human upper-limb bilateral coordination patterns, cyclic rhythmical bilateral movements can be classified into two fundamental modes: in-phase (i.e., bilateral homologous muscles contract simultaneously) and anti-phase (i.e., homologous muscles contract alternately) movements [5]. Research in healthy young adults has established that anti-phase movements are more complex and unstable [6, 7]. During anti-phase movements, participants display higher spatial and temporal variability and worse inter-limb synchronization compared to in-phase movements [8,9,10]. Though both in-phase and anti-phase movements require bilateral coordination, research in healthy adults suggests that they are associated with different control mechanisms. During bilateral in-phase finger movements, previous research has found increased activation of the left (dominant) hemisphere compared to the right [11, 12], as well as causal information flow of the BOLD signal from the left to the right motor cortex [13]. These suggest the dominant role of the left hemisphere in bilateral in-phase movement execution. In contrast, no significant laterality effects were observed during bilateral anti-phase finger movements, which suggest a similar contribution from the two hemispheres [14, 15].

After stroke affecting the motor system, patients generally exhibit greater movement variability [16] and unsteady force control [17] during bilateral movements, regardless of the coordination patterns. Also, the interhemispheric balance between the two hemispheres as well as the laterality in ascending pathways showed changes during bilateral movements after stroke [18, 19], indicating neural reorganization in bilateral movement execution [20, 21]. Moreover, like healthy adults, stroke patients experience more difficulty performing anti-phase than in-phase movements [22, 23]. However, considering that the two hemispheres are differentially involved in in- and anti-phase movements in healthy adults, we would expect distinct characteristics in bilateral coordination impairments after left and right hemispheric stroke. Consistent with this, one previous study found that left hemispheric stroke (LHS) compared to right hemispheric stroke (RHS) patients showed better inter-limb synchronization during in-phase elbow pronation-supination movements [24]. However, given that bilateral coordination is controlled by a complex system comprising both individual-limb and inter-limb components [25], a successful bilateral movement requires not only a good inter-limb coordination but also an accurate individual-limb control. Therefore, it is still unclear from the literature how individual limb performance during bilateral movements is affected after left and right hemispheric stroke.

To examine whether the lesion hemisphere influences bilateral movements after stroke, we compared inter- and individual-limb performance between stroke survivors with left and right hemispheric lesions. Inter-limb performance was examined using inter-limb synchronization index, and individual-limb by movement trajectory variability of the contralesional and ipsilesional hands. We expected that patients in general exhibit deficits in bilateral movement performance. However, we hypothesized to find differences between both groups (left vs. right hemispheric lesions). Specifically, we hypothesized firstly, that left hemispheric stroke patients exhibit stronger impairments in bilateral in-phase coordination compared to right hemispheric stroke patients. This is based on the observed left hemispheric dominance during bilateral in-phase movements in the healthy population [11]. Secondly, since right hemispheric stroke leads to a larger imbalance in interhemispheric inhibition (IHI) compared to left hemispheric stroke [26], we hypothesized that bilateral anti-phase movements, which require balanced activity in bilateral hemispheres, would exhibit stronger impairments in patients with right hemispheric stroke. Also, we furthermore assessed the individual contributions of the two hands to inter-limb synchronization. Specifically, we examined whether it is possible to use the individual-limb performance from both arms to predict the inter-limb coordination control in patients with left- and right-hemispheric stroke. This enabled us to use hand performance to infer how motor stroke affects the differential roles of the two hemispheres in bilateral coordination.

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