Neuromuscular Control before and after Independent Walking Onset in Children with Cerebral Palsy

Bekius, Annike; Zandvoort, Coen S.; Kerkman, Jennifer N.; Pol, Laura A. van de; Vermeulen, R. Jeroen; Harlaar, Jaap; Daffertshofer, Andreas; Buizer, Annemieke I.; Dominici, Nadia

doi:10.3390/s21082714

Cited by 7 publications

(14 citation statements)

References 56 publications

(44 reference statements)

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“…To support the hypothesis, it is noteworthy to consider that different treatment approaches have shown minimal changes in synergies, even if gait pattern, movement quality and speed improved significantly after treatment ( Table 2 ). These results are coherent with the fact that CP results from a cortical and/or subcortical brain lesions in the perinatal period, causing impairments in motor controls since the very beginning ( Cappellini et al, 2016 ; Cappellini et al, 2020 ; Short et al, 2020 ; Bekius et al, 2021 ).…”

Section: Resultssupporting

confidence: 84%

“…The most affected synergies are those related to the knee-foot and the knee-hip couples, which result to be impaired in most patients ( Thelen et al, 2003 ; Czupryna and Nowotny, 2012 ). In addition, children affected by CP show a higher stride-to-stride variability, which is not observed in healthy controls ( Kim et al, 2018 ; Yu et al, 2019 ; Bekius et al, 2021 ). Bekius and others have recently summarized the evolution in the use of muscle synergies as biomarkers for evaluating locomotion in children affected by CP ( Bekius et al, 2020 ).…”

Section: Introductionmentioning

confidence: 79%

“…The previously mentioned results are visible as early as a child starts walking, as demonstrated by Dominici et al (2011) who found that neonates already show patterns of stepping that are retained later ( Dominici et al 2011 ). Bekius et al investigated specifically muscle synergies variation before and after the onset of independent walking in both TD and CP children ( Bekius et al, 2021 ). They showed that children with CP recruit less synergies already in supported walking as well as in the first years of independent walking, underlining the need of an early rehabilitation program which might promote an early motor recovery as proposed by Cappellini et al (2020) .…”

Section: Discussionmentioning

confidence: 99%

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Recent developments in muscle synergy analysis in young people with neurodevelopmental diseases: A Systematic Review

Beltrame

Scano

Marino

et al. 2023

Front. Bioeng. Biotechnol.

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The central nervous system simplifies motor control by sending motor commands activating groups of muscles, known as synergies. Physiological locomotion can be described as a coordinated recruitment of four to five muscle synergies. The first studies on muscle synergies in patients affected by neurological diseases were on stroke survivors. They showed that synergies can be used as biomarkers for motor impairment as they vary in patients with respect to healthy people. Likewise, muscle synergy analysis has been applied to developmental diseases (DD). The need for a comprehensive view of the present findings is crucial for comparing results achieved so far and promote future directions in the field. In the present review, we screened three scientific databases and selected thirty-six papers investigating muscle synergies extracted from locomotion in children affected by DD. Thirty-one articles investigate how cerebral palsy (CP) influences motor control, the currently exploited method in studying motor control in CP and finally the effects of treatments in these patients in terms of synergies and biomechanics; two articles investigate how muscle synergies vary in Duchenne muscular dystrophy (DMD), and three other articles assess other developmental pathologies, such as chronic and acute neuropathic pain. For CP, most of the studies demonstrate that the number of synergies is lower and that the synergy composition varies in the affected children with respect to normal controls. Still, the predictability of treatment’s effects and the etiology of muscle synergy variation are open questions, as it has been reported that treatments minimally modify synergies, even if they improve biomechanics. The application of different algorithms in extracting synergies might bring about more subtle differences. Considering DMD, no correlation was found between non-neural muscle weakness and muscle modules’ variation, while in chronic pain a decreased number of synergies was observed as a possible consequence of plastic adaptations. Even if the potential of the synergistic approach for clinical and rehabilitation practices is recognized, there is not full consensus on protocols nor widely accepted guidelines for the systematic clinical adoption of the method in DD. We critically commented on the current findings, on the methodological issues and the relative open points, and on the clinical impact of muscle synergies in neurodevelopmental diseases to fill the gap for applying the method in clinical practice.

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Section: Resultssupporting

confidence: 84%

Section: Introductionmentioning

confidence: 79%

Section: Discussionmentioning

confidence: 99%

See 1 more Smart Citation

Recent developments in muscle synergy analysis in young people with neurodevelopmental diseases: A Systematic Review

Beltrame

Scano

Marino

et al. 2023

Front. Bioeng. Biotechnol.

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show abstract

“…Comparing groups based on the VAF added by each synergy also distinguished between CON and LFH individuals, as well as HFH and LFH individuals without relying on investigator-made decisions regarding a critical threshold. A similar approach was used by Bekius et al, who found that children with cerebral palsy exhibit greater VAF in the first synergy in their more-affected side 52 . Alternatively, Ballarini et al described an algorithm for choosing the optimal NumSyn, which may also serve to decrease the impact of investigator choice on the results 53 .…”

Section: Discussionmentioning

confidence: 97%

Evidence for shared neural information between muscle synergies and corticospinal efficacy

Young

Banks

McGuirk

et al. 2022

Sci Rep

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Stroke survivors often exhibit gait dysfunction which compromises self-efficacy and quality of life. Muscle Synergy Analysis (MSA), derived from electromyography (EMG), has been argued as a method to quantify the complexity of descending motor commands and serve as a direct correlate of neural function. However, controversy remains regarding this interpretation, specifically attribution of MSA as a neuromarker. Here we sought to determine the relationship between MSA and accepted neurophysiological parameters of motor efficacy in healthy controls, high (HFH), and low (LFH) functioning stroke survivors. Surface EMG was collected from twenty-four participants while walking at their self-selected speed. Concurrently, transcranial magnetic stimulation (TMS) was administered, during walking, to elicit motor evoked potentials (MEPs) in the plantarflexor muscles during the pre-swing phase of gait. MSA was able to differentiate control and LFH individuals. Conversely, motor neurophysiological parameters, including soleus MEP area, revealed that MEP latency differentiated control and HFH individuals. Significant correlations were revealed between MSA and motor neurophysiological parameters adding evidence to our understanding of MSA as a correlate of neural function and highlighting the utility of combining MSA with other relevant outcomes to aid interpretation of this analysis technique.

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“…Another limitation of this study is that only healthy individuals were recruited into the experiment, the obtained results cannot be extrapolated to patients with motor impaired patients directly. Because the group of disabled individuals with stroke, cerebral palsy, traumatic brain injury, and so on often display spasticity and abnormal synergy during strength training, yielding distinctly different muscle coordination patterns from that of the healthy subjects ( Kong et al, 2019 ; Bekius et al, 2021 ; Li et al, 2021 ). Therefore, in our future for subjects with specific motor impairment, the modulation of muscle synergies needs to be analyzed independently.…”

Section: Discussionmentioning

confidence: 99%

Applying muscle synergy analysis to forearm high-density electromyography of healthy people

et al. 2022

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IntroductionMuscle synergy is regarded as a motor control strategy deployed by the central nervous system (CNS). Clarifying the modulation of muscle synergies under different strength training modes is important for the rehabilitation of motor-impaired patients.MethodsTo represent the subtle variation of neuromuscular activities from the smaller forearm muscles during wrist motion, we proposed to apply muscle synergy analysis to preprocessed high-density electromyographic data (HDEMG). Here, modulation of muscle synergies within and across the isometric and isotonic training modes for strengthening muscles across the wrist were investigated. Surface HDEMGs were recorded from healthy subjects (N = 10). Three different HDEMG electrode configurations were used for comparison and validation of the extracted muscle synergies. The cosine of principal angles (CPA) and the Euclidian distance (ED) between synergy vectors were used to evaluate the intra- and inter-mode similarity of muscle synergies. Then, how the activation coefficients modulate the excitation of specific synergy under each mode was examined by pattern recognition. Next, for a closer look at the mode-specific synergies and the synergies shared by the two training modes, k-means clustering was applied.ResultsWe observed high similarity of muscle synergies across different tasks within each training mode, but decreased similarity of muscle synergies across different training modes. Both intra- and intermode similarity of muscle synergies were consistently robust to electrode configurations regardless of the similarity metric used.DiscussionOverall, our findings suggest that applying muscle synergy analysis to HDEMG is feasible, and that the traditional muscle synergies defined by whole-muscle components may be broadened to include sub-muscle components represented by the HDEMG channels. This work may lead to an appropriate neuromuscular analysis method for motor function evaluation in clinical settings and provide valuable insights for the prescription of rehabilitation training therapies.

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Neuromuscular Control before and after Independent Walking Onset in Children with Cerebral Palsy

Cited by 7 publications

References 56 publications

Recent developments in muscle synergy analysis in young people with neurodevelopmental diseases: A Systematic Review

Recent developments in muscle synergy analysis in young people with neurodevelopmental diseases: A Systematic Review

Evidence for shared neural information between muscle synergies and corticospinal efficacy

Applying muscle synergy analysis to forearm high-density electromyography of healthy people

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