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Muscle Activation Patterns During Movement Attempts in Children With Acquired Spinal Cord Injury: Neurophysiological Assessment of Residual Motor Function Below the Level of Lesion

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Muscle Activation Patterns During Movement Attempts in Children With Acquired Spinal Cord Injury: Neurophysiological Assessment of Residual Motor Function Below the Level of Lesion

Darryn A Atkinson et al. Front Neurol.

Abstract

Introduction: Characterization of residual neuromotor capacity after spinal cord injury (SCI) is challenging. The current gold standard for measurement of sensorimotor function after SCI, the International Society for Neurological Classification of Spinal Cord Injury (ISNCSCI) exam, seeks to determine isolated intentional muscle activation, however many individuals with SCI exhibit intentional movements and muscle activation patterns which are not confined to specific joint or muscle. Further, isolated muscle activation is a feature of the neuromuscular system that emerges during development, and thus may not be an appropriate measurement standard for children younger than 6. Methods: We utilized neurophysiological assessment methodology, long studied in adult SCI populations, to evaluate residual neuromotor capacity in 24 children with SCI, as well as 19 typically developing (TD) children. Surface electromyography (EMG) signals were recorded from 11 muscles bilaterally, representing spinal motor output from all regions (i.e., cervical, thoracic, and lumbosacral), during standardized movement attempts. EMG records were subjectively analyzed based on spatiotemporal muscle activation characteristics, while the voluntary response index (VRI) was utilized for objective analysis of unilateral leg movement tasks. Results: Evidence of intentional leg muscle activation below the level of lesion was found in 11/24 children with SCI, and was classified based on activation pattern. Trace activation, bilateral (generalized) activation, and unilateral or isolated activation occurred in 32, 49, and 8% of movement tasks, respectively. Similarly, VRI analyses objectively identified significant differences between TD and SCI children in both magnitude (p < 0.01) and similarity index (p < 0.05) for all unilateral leg movement tasks. Activation of the erector spinae muscles, recorded at the T10-T12 vertebral level, was observed in all children with SCI, regardless of injury level or severity. Conclusions: Residual descending influence on spinal motor circuits may be present after SCI in children. Assessment of multi-muscle activation patterns during intentional movement attempts can provide objective evidence of the presence and extent of such residual muscle activation, and may provide an indicator of motor recovery potential following injury. The presence of residual intentional muscle activation has important implications for rehabilitation following pediatric-onset SCI.

Keywords: electromyography; motor assessment; neurophysiology; pediatric spinal cord injury; rehabilitation.

Figures

Figure 1
Figure 1
Pediatric functional neurophysiologic assessment summary. (A) Muscles from which EMG is recorded during the assessment, and their respective spinal root innervation. The right-hand column lists the movements used to assess intentional activation for the applicable muscles. (B) Example of electrode placements. Rectus Abdominus electrodes were placed para-umbilically, while erector spinae electrodes were placed with the superior aspect of the electrode at the level of the T10 spinous process. Written informed consent was obtained from the child's parent for the use of this image.
Figure 2
Figure 2
Pediatric functional neurophysiologic assessment: evaluation of typically developing motor patterns. (A) EMG recordings from 3 different TD children (aged 3, 7, and 11 years old, left to right) during performance of the left ankle dorsiflexion task, demonstrating the three muscle activation patterns observed during development of isolated muscle activation in these children: bilateral muscle activation, unilateral muscle activation, and isolated muscle activation. RA, rectus abdominus; ES, erector spinae; ADD, adductor magnus; RF, rectus femoris; VL, vastus lateralis; MH, medial hamstrings (semitendinosus); TA, tibialis anterior; MG, medial gastrocnemius. SI and magnitude values corresponding to each example. (B) Relationship between age and muscle activation pattern, where N, no activation; T, trace activation; B, bilateral activation; U, unilateral activation; and I, isolated activation. RADF, right ankle dorsiflexion; LKE, left knee extension; RKE, right knee extension.
Figure 3
Figure 3
Pediatric functional neurophysiologic assessment: Qualitative and quantitative evaluation of residual motor patterns in children with SCI. (A) EMG recordings from 5 different children with SCI during performance of the left ankle dorsiflexion task, demonstrating the 5 muscle activation patterns observed during development of isolated muscle activation in these children: no muscle activation, trace muscle activation, bilateral muscle activation, unilateral muscle activation, and isolated muscle activation. RA, rectus abdominus; ES, erector spinae; ADD, adductor magnus; RF, rectus femoris; VL, vastus lateralis; MH, medial hamstrings (semitendinosus); TA, tibialis anterior; MG, medial gastrocnemius. SI and magnitude values corresponding to each example. (B) Relationship between group (NMA, IMA, and TD) and muscle activation pattern for each unilateral movement task, N, no activation; T, trace activation; B, bilateral activation; U, unilateral activation; and I, isolated activation; IMA, intentional muscle activation; NMA, no muscle activation; TD, typically developing.
Figure 4
Figure 4
Summary of quantitative evaluation of unilateral movement tasks in TD children and children with SCI. (A) SI and Magnitude values are plotted against each other for comparison of group results for each unilateral movement task. Circles represent individual participants; diamonds represent group averages. (B) average magnitude values by group (C) average SI values by group (D) Comparison of SI values and qualitative score. Black bars indicate statistically significant differences between groups (p < 0.05). SI, similarity index; LADF, left ankle dorsiflexion; RADF, right ankle dorsiflexion; LKE, left knee extension; RKE, right knee extension; IMA, intentional muscle activation; NMA, no muscle activation; TD, typically developing.
Figure 5
Figure 5
Delayed-onset muscle activation in children with SCI. EMG recordings from 3 different children with SCI during performance of the sit up task, demonstrating delayed onset bilateral muscle activation in all leg muscles. The hashed red lines indicate the timing of onset of muscle activation. UT, upper trapezius; DELT, anterior deltoid; RA, rectus abdominus; ES, erector spinae; ADD, adductor magnus; RF, rectus femoris; VL, vastus lateralis; MH, medial hamstrings (semitendinosus); TA, tibialis anterior; MG, medial gastrocnemius.
Figure 6
Figure 6
Trunk muscle activation during intentional movement attempts in children with cervical SCI. EMG recordings from three different children with SCI during two different leg movement attempts: left ankle dorsiflexion (A) and left knee extension (B). (C–E) Average RMS values for left ankle dorsiflexion, left knee extension, and grand average across all movement tasks for all children with cervical SCI. EMG, electromyography; RMS, root mean square; UT, Upper Trapezius; DELT, Deltoid; RA, Rectus Abdominus; ES, Erector Spinae; ADD, Adductor Magnus; RF, Rectus Femoris; VL, Vastus Lateralis; MH, Medial Hamstrings; TA, Tibialis Anterior; MG, Medial Gastrocnemius.

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