Elsevier

Brain Research

Volume 1739, 15 July 2020, 146833
Brain Research

Research report
Differential corticomotor mechanisms of ankle motor control in post stroke individuals with and without motor evoked potentials

https://doi.org/10.1016/j.brainres.2020.146833Get rights and content

Highlights

  • Relationship between corticomotor symmetry and ankle motor control is conflicting.

  • Presence or absence of MEP does not affect motor control.

  • Strategies for ankle motor control are different in those with and without MEPs.

Abstract

Objective

Deficits in ankle motor control has been identified as a significant contributor to impaired walking after stroke. Corticomotor excitability has been related to impaired upper limb motor control and poor recovery in stroke, however contributions to lower limb function are still unclear. This study used transcranial magnetic stimulation (TMS) to determine the influence of corticomotor characteristics on lower limb motor control in chronic stroke survivors.

Methods

This retrospective study assessed 28 individuals with post stroke hemiparesis. Motor evoked potentials (MEP) measured from the paretic and non-paretic tibialis anterior (TA) muscles were used to calculate corticomotor excitability symmetry (CMEsym) and relative ipsilateral corticomotor excitability (ICE). Participants were assigned to MEP+ and MEP− groups depending on the presence (+) or absence (−) of MEPs. Ankle motor control was quantified by the ability of participants to track a sinusoidal target using dorsiflexion-plantarflexion movements of the paretic ankle and tracking error was calculated using root mean square error (RMSE).

Results

Multiple linear regression model for all participants revealed only CMEsym and FMLE (p < 0.01) to significantly predict RMSE. In the MEP+ group, CMEsym significantly predicted RMSE (p = 0.03) while FMLE (p = 0.02) was a significant predictor for the MEP−.

Conclusion

Our results indicate that CMEsym between the ipsilesional and contralesional hemispheres does not necessarily translate to better paretic ankle motor control in chronic stroke. Presence or absence of a MEP in the TA muscle did not affect the ankle tracking performance, however, it was noted that different strategies maybe used by those with and without a MEP.

Introduction

Approximately two-thirds of stroke survivors experience limitations in independent walking (Jorgensen et al., 1995). Impairments in ankle motor control following stroke is a significant contributor to reduced walking speed and increased walking asymmetry (Lin et al., 2006). Since voluntary control of the ankle plays a key role in restoration of functional ambulation post stroke, it is important to fully understand neural mechanisms contributing to impaired motor control to facilitate effective gait retraining and neuromodulation programs.

Numerous studies using transcranial magnetic stimulation (TMS), a non-invasive neurophysiological tool to quantify neural excitability of descending corticomotor pathways, have demonstrated that the primary motor cortex (M1) plays a crucial role in goal-directed movement (Beaulieu et al., 2014, Carey et al., 2004). Previously, upper limb TMS studies have demonstrated that an imbalance in interhemispheric corticomotor excitability symmetry (CMEsym), resulting due to increased excitability of the contralesional hemisphere and concurrent decrease in excitability of the ipsilesional hemisphere, interferes with motor recovery after stroke and is related to poor upper limb movement control (Koski et al., 2004, Murase et al., 2004, Ward and Cohen, 2004). However, the theory of interhemispheric imbalance has been challenged by recent studies which have demonstrated no causal relationship between imbalanced interhemispheric inhibition and upper limb motor control (McDonnell and Stinear, 2017, Xu et al., 2019). Due to the limited number of TMS studies focused on lower limb motor recovery and interhemispheric imbalance, it is still unclear if the interhemispheric competition model is valid in predicting lower limb recovery following stroke. Stroke survivors demonstrate asymmetry in between-hemisphere lower limb M1 corticomotor excitability (CME) (Palmer et al., 2016a, Sivaramakrishnan and Madhavan, 2018); however, there is no consensus on how this affects lower limb motor control. Some studies have observed that the absence of a motor evoked potential (MEP) and lesser corticomotor drive from the ipsilesional M1 in stroke participants affects walking recovery while others have found no associations (Cho et al., 2012, Hendricks et al., 2003, Palmer et al., 2016a, Palmer et al., 2016b, Sivaramakrishnan and Madhavan, 2018, Smith et al., 2017). The neural mechanisms of lower limb motor control may not be fully elucidated by these gait studies as walking requires complex and compensatory interactions. Studying a skilled voluntary goal-directed movement may provide a deeper insight into the role of descending neural drive and interhemispheric interactions after stroke. Hence, the purpose of this study was to examine the role of corticomotor contributions to lower limb motor performance in chronic stroke using a skilled ankle motor task. We hypothesized that post stroke individuals with greater interhemispheric balance and lesser ipsilateral drive from the contralesional M1 of the tibialis anterior (TA) muscle representations will demonstrate better ankle motor control.

Section snippets

Results

All variables were normally distributed. Descriptive statistics for all the participants, participants with MEPs (MEP+) and without MEPs (MEP−) are summarized in Table 1. Slope of the ipsilesional M1 (0.0027 ± 0.0024) was 67% lesser than the contralesional M1 (0.0083 ± 0.0047) resulting in CMEsym of 0.58 ± 0.31 (value close to 0 indicates greater symmetry while close to 1 indicates greater asymmetry). The MEP+ group demonstrated significantly greater ipsilesional CME, Fugl Meyer lower extremity

Discussion

Our study aimed to better understand corticomotor control of lower limb using a skilled goal-directed ankle task. In a previous study, we explored the relationship between corticomotor connectivity and walking outcomes and concluded that functional connectivity measured as the presence or absence of a TMS-induced MEP does not predict walking speed (Sivaramakrishnan and Madhavan, 2018). In this study, we specifically chose a goal-directed movement which requires precise isolated control of the

Study design

This was a retrospective study design, where measurements were collected as a part of a larger randomized control trial (RCT) in the Brain Plasticity Laboratory at the University of Illinois at Chicago (clinical trial registration: NCT03492229). We included baseline TMS, ankle motor control measurements, and clinical outcomes which were collected on consecutive days.

Participants

Twenty-eight individuals with chronic stroke who performed the visuomotor ankle tracking as a part of their baseline assessments

Funding

This work was supported by the National Institute of Health (NIH) [grant numbers R01HD075777 (SM)].

Declaration of Competing Interest

None.

CRediT authorship contribution statement

Hyosok Lim: Conceptualization, Formal analysis, Investigation, Writing - original draft, Visualization, Project administration. Sangeetha Madhavan: Conceptualization, Methodology, Writing - review & editing, Supervision, Funding acquisition.

Acknowledgements

We would like to thank all Brain Plasticity Laboratory participants and research assistants for their time and effort.

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