Elsevier

Behavioural Brain Research

Volume 417, 24 January 2022, 113563
Behavioural Brain Research

Research report
Increased intensity of unintended mirror muscle contractions after cervical spinal cord injury is associated with changes in interhemispheric and corticomuscular coherences

https://doi.org/10.1016/j.bbr.2021.113563Get rights and content

Highlights

  • Spinal cord injury (SCI) patients present increased unintended mirror muscle activity.

  • SCI patients present increased β corticomuscular coherence contralateral to the unintended mirror muscle activity.

  • SCI patients present decreased β interhemispheric coherence between sensorimotor regions.

Abstract

Mirror contractions refer to unintended contractions of the contralateral homologous muscles during voluntary unilateral contractions or movements. Exaggerated mirror contractions have been found in several neurological diseases and indicate dysfunction or lesion of the cortico-spinal pathway. The present study investigates mirror contractions and the associated interhemispheric and corticomuscular interactions in adults with spinal cord injury (SCI) – who present a lesion of the cortico-spinal tract – compared to able-bodied participants (AB). Eight right-handed adults with chronic cervical SCI and ten age-matched right-handed able-bodied volunteers performed sets of right elbow extensions at 20% of maximal voluntary contraction. Electromyographic activity (EMG) of the right and left elbow extensors, interhemispheric coherence over cerebral sensorimotor regions evaluated by electroencephalography (EEG) and corticomuscular coherence between signals over the cerebral sensorimotor regions and each extensor were quantified. Overall, results revealed that participants with SCI exhibited (1) increased EMG activity of both active and unintended active limbs, suggesting more mirror contractions, (2) reduced corticomuscular coherence between signals over the left sensorimotor region and the right active limb and increased corticomuscular coherence between the right sensorimotor region and the left unintended active limb, (3) decreased interhemispheric coherence between signals over the two sensorimotor regions. The increased corticomuscular communication and decreased interhemispheric communication may reflect a reduced inhibition leading to increased communication with the unintended active limb, possibly resulting to exacerbated mirror contractions in SCI. Finally, mirror contractions could represent changes of neural and neuromuscular communication after SCI.

Introduction

Mirror movements refer to the unintended movements involving the contralateral homologous muscles during voluntary unilateral movements and are particularly visible in distal upper limb muscles [1]. Mirror movements are normally present during childhood and disappear gradually as the central nervous system matures [2], [3]. However, mirror muscle contractions, also described as mirror activity [4], can still be recorded with electromyography (EMG) in healthy adults during tasks requiring to perform low or high force levels [5], [6]. Mirror movements are even increased in neurological populations [7], especially in brain-injured patients [8], [9], [10]. Two theories are proposed in the literature to explain the presence of mirror contractions, but the neurological correlates are still debated. On the one hand, the “ipsilateral activation theory” postulates that mirror contractions could be the result, at least in part, of ipsilateral hemispheric projections through the cortico-spinal tract [1], [7], [11]. This theory is particularly relevant to explain mirror contractions in children with cerebral lesions or congenital syndromes who do not present the progressive inhibition of the ipsilateral projections found in typical child development [12], [13]. On the other hand, the “bilateral activation theory” postulates that the activation of the motor area in one hemisphere during voluntary movement facilitates the activation of the same motor area in the opposite hemisphere leading to mirror contractions [14]. Hence, one motor cortex inhibits the activity of the opposite motor cortex to prevent mirror contractions during unilateral motor tasks [15], [16]. This theory is supported by studies using transcranial magnetic stimulation (TMS) suggesting that mirror contractions during the production of unimanual movements may be the result of altered interhemispheric communication between motor areas [17]. Although there is a small ipsilateral corticospinal tract component in healthy adults [11], there is currently little electrophysiological [18] and anatomical [19] evidences for direct connections onto ipsilateral muscles. Mirror contractions in healthy adults may thus originate in the hemisphere contralateral to the unintended movement [1]. Furthermore, using both functional magnetic resonance imaging (fMRI) and TMS, Chiou et al. [20] showed that ipsilateral motor cortex was activated during unilateral muscle contractions suggesting that motor cortices work together to perform voluntary unilateral movements. On this basis, mirror contractions may also result from corticomuscular interactions between both contralateral and ipsilateral motor cortices and muscles involved in unintended contractions.

Because mirror contractions can suggest dysfunction or lesion of the cortico-spinal pathway [13], [21], we propose to investigate whether a spinal cord injury (SCI), that may involve a lesion of the corticospinal tract (but also other descending and ascending pathways), modulates unintended mirror contractions. This question has never been addressed as such, even if previous studies using electroencephalography (EEG) and/or EMG recordings have found changes at cortical and muscular levels and also in corticomuscular communication in participants with SCI [22], [23], [24], [25]. Although no study has specifically investigated mirror contractions in people with SCI, several findings suggest that unintended muscle activations in the contralateral limb may be exacerbated. In particular, increased unintended activation of the antagonist muscles during voluntary unilateral contractions has been reported in participants with SCI [22] and associated with changes in communication between cortical and spinal structures inhibiting antagonist muscles [26], [27], [28]. In addition, important changes in the cortical motor network have also been documented in SCI patients [25]. Therefore, we could hypothesise that the changes of the communication between central and peripheral structures could exacerbate unintended muscle activations in the contralateral limb during voluntary unilateral contractions. This communication can be investigated through corticomuscular coherence (CMC) which can be defined as a measure of the functional coupling between sensorimotor cortex and muscular activity [29], [30] and which is thought to reflect the interactions between descending (motor command) and ascending (sensory input) pathways [31], [32]. Therefore, based on concomitant analysis of corticocortical and corticomuscular coherences, the present study aims to evaluate the production of unintended mirror muscle activity in SCI compared to able-bodied participants and the associated interhemispheric and corticomuscular interactions. We hypothesised that the level of unintended mirror contractions would be increased in the SCI group compared to able-bodied participants. We also expected to find differences in both interhemispheric coherence and corticomuscular coherence between signals over the contralateral sensorimotor region and the limb producing unintended mirror muscle activations.

Section snippets

Participants

The current study is based on the same sample as in Cremoux et al. [22]. Eight right-handed adults with chronic cervical spinal cord injury located between C5 and C7 spinal nerves (SCI group; 1 female, age: 32.50 ± 6.16 years, time since injury: 9.63 ± 4.14 years) and ten age-matched right-handed able-bodied volunteers (AB group; 1 female, age: 27.44 ± 4.03 years) participated in the study. The individual performance of right elbow extensors and the grade of completeness of the lesion were

Results

Summary of descriptive and estimation statistics for all two-sample independent comparisons is presented in Table 2.

Discussion

The main purpose of this study was to explore the intensity of mirror contractions and the associated interhemispheric and corticomuscular correlates in AB and SCI participants who produced submaximal right elbow extensions. Our main result is that, for a similar normalised force production at 20% of MVC in AB and SCI participants, participants with SCI presented greater EMG activation of extensor muscles in both the right active and the left unintended active limbs. This result suggests that

Conclusion

Due to the small sample size and high heterogeneity especially in the SCI group, the results of this study should be treated with caution and would need to be replicated on an ideal sample size of fifteen or more SCI patients. In addition, an interesting perspective could be to perform subgroup analyses on a larger sample of SCI patients in order to extend the current findings. Furthermore, in this study we have chosen to consider the unintended contralateral muscular activations as mirror

Funding

This research did not receive any specific grant from funding agencies in the public, commercial, or not-for-profit sectors.

CRediT authorship contribution statement

Joseph Tisseyre: Conceptualization, Methodology, Validation, Formal analysis, Writing – original draft, Writing – review & editing, Visualization. Sylvain Cremoux: Conceptualization, Methodology, Writing – review & editing, Validation, Investigation, Visualization, Supervision. David Amarantini: Conceptualization, Methodology, Writing – review & editing, Software, Validation, Supervision. Jessica Tallet: Conceptualization, Methodology, Writing – review & editing, Validation, Supervision.

References (79)

  • S. Cremoux et al.

    Does the force level modulate the cortical activity during isometric contractions after a cervical spinal cord injury?

    Clin. Neurophysiol.

    (2013)
  • G.I. Boorman et al.

    Impaired “natural reciprocal inhibition” in patients with spasticity due to incomplete spinal cord injury

    Electroencephalogr. Clin. Neurophysiol.

    (1996)
  • M. Knikou et al.

    Reduced reciprocal inhibition during assisted stepping in human spinal cord injury

    Exp. Neurol.

    (2011)
  • D.M. Halliday et al.

    Using electroencephalography to study functional coupling between cortical activity and electromyograms during voluntary contractions in humans

    Neurosci. Lett.

    (1998)
  • H.J. Hermens et al.

    Development of recommendations for SEMG sensors and sensor placement procedures

    J. Electromyogr. Kinesiol.

    (2000)
  • D. Amarantini et al.

    A method to combine numerical optimization and EMG data for the estimation of joint moments under dynamic conditions

    J. Biomech.

    (2004)
  • F. Perrin et al.

    Spherical splines for scalp potential and current density mapping

    Electroencephalogr. Clin. Neurophysiol.

    (1989)
  • J. Bigot et al.

    A new statistical test based on the wavelet cross-spectrum to detect time–frequency dependence between non-stationary signals: Application to the analysis of cortico-muscular interactions

    NeuroImage

    (2011)
  • C. Charissou et al.

    Fatigue- and training-related changes in ‘beta’ intermuscular interactions between agonist muscles

    J. Electromyogr. Kinesiol.

    (2016)
  • V. Morash et al.

    Classifying EEG signals preceding right hand, left hand, tongue, and right foot movements and motor imageries

    Clin. Neurophysiol.

    (2008)
  • Z. Bayraktaroglu et al.

    Optimal imaging of cortico-muscular coherence through a novel regression technique based on multi-channel EEG and un-rectified EMG

    NeuroImage

    (2011)
  • V.M. McClelland et al.

    Rectification of the EMG is an unnecessary and inappropriate step in the calculation of Corticomuscular coherence

    J. Neurosci. Methods

    (2012)
  • R. Kristeva et al.

    Beta-range cortical motor spectral power and corticomuscular coherence as a mechanism for effective corticospinal interaction during steady-state motor output

    NeuroImage

    (2007)
  • C.K. Thomas et al.

    Muscle weakness, paralysis, and atrophy after human cervical spinal cord injury

    Exp. Neurol.

    (1997)
  • N. Alexeeva et al.

    Central cord syndrome of cervical spinal cord injury: widespread changes in muscle recruitment studied by voluntary contractions and transcranial magnetic stimulation

    Exp. Neurol.

    (1997)
  • R.G. Carson et al.

    Electromyographic activity, H-reflex modulation and corticospinal input to forearm motoneurones during active and passive rhythmic movements

    Hum. Mov. Sci.

    (1999)
  • M. Pohja et al.

    Cortico–muscular coupling in a human subject with mirror movements – a magnetoencephalographic study

    Neurosci. Lett.

    (2002)
  • F.D. Roy et al.

    Short-interval intracortical inhibition with incomplete spinal cord injury

    Clin. Neurophysiol.

    (2011)
  • M.J. Mayston et al.

    A neurophysiological study of mirror movements in adults and children

    Ann. Neurol.

    (1999)
  • T. Maudrich et al.

    Structural neural correlates of physiological mirror activity during isometric contractions of non-dominant hand muscles

    Sci. Rep.

    (2018)
  • Z. Arányi et al.

    Effort-induced mirror movements: a study of transcallosal inhibition in humans

    Exp. Brain Res.

    (2002)
  • S.-H. Chang et al.

    Interlimb interactions during bilateral voluntary elbow flexion tasks in chronic hemiparetic stroke

    Physiol. Rep.

    (2013)
  • G. Nelles et al.

    Quantitative assessment of mirror movements after stroke

    Stroke

    (1998)
  • H.-C. Kuo et al.

    Neurophysiological mechanisms and functional impact of mirror movements in children with unilateral spastic cerebral palsy

    Dev. Med. Child Neurol.

    (2018)
  • M. Riddell et al.

    Mirror movements in children with unilateral cerebral palsy due to perinatal stroke: clinical correlates of plasticity reorganization

    Dev. Med. Child Neurol.

    (2019)
  • J. Cernacek

    Contralateral motor irradiation-cerebral dominance: its changes in hemiparesis

    Arch. Neurol.

    (1961)
  • M.R. Hinder et al.

    Unilateral contractions modulate interhemispheric inhibition most strongly and most adaptively in the homologous muscle of the contralateral limb

    Exp. Brain Res.

    (2010)
  • A. Hübers et al.

    Interhemispheric motor inhibition: its role in controlling electromyographic mirror activity

    Eur. J. Neurosci.

    (2008)
  • D.S. Soteropoulos et al.

    Lack of evidence for direct corticospinal contributions to control of the ipsilateral forelimb in monkey

    J. Neurosci.

    (2011)
  • View full text