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