Network structure of the human musculoskeletal system shapes neural interactions on multiple time scales

Kerkman, Jennifer N.; Daffertshofer, Andreas; Gollo, Leonardo L.; Breakspear, Michael; Boonstra, Tjeerd W.

doi:10.1126/sciadv.aat0497

Cited by 127 publications

(114 citation statements)

References 51 publications

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“…Pioneering works have started looking at the interplay between multiple muscle activity for postural control (Kerkman et al, 2018). Building on this, future research should strive to extent such work to integrate brain, muscle and kinematic signals recorded from multiple muscles/effectors in ecological motor actions such as locomotion or skilled hand (e.g., writing, drawing, knitting) actions.…”

Section: Limitations and Perspectivesmentioning

confidence: 99%

Coupling between human brain activity and body movements: Insights from non-invasive electromagnetic recordings

et al. 2019

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Electroencephalographic and magnetoencephalographic data have characterized two types of brain-body interactions observed during various types of motor actions, "corticokinematic" and "corticomuscular" coupling. Here, we review the literature on these interactions in healthy individuals, discuss several open debates, and outline current limitations and directions for future research. Corticokinematic coupling (commonly referred to as corticokinematic coherence) probes the relationship between activity of sensorimotor network nodes and various movement-related signals (e.g., speed, velocity, acceleration). It is mainly driven by movement rhythmicity during active, passive, and observed dynamic motor actions. It typically predominates at the primary sensorimotor cortex contralateral to the moving limb, occurs at movement frequency and its harmonics, and predominantly reflects the cortical processing of proprioceptive feedback driven by movement rhythmicity in a broad range of dynamic motor actions. Corticomuscular coupling (commonly referred to as corticomuscular coherence) probes the interaction between sensorimotor cortical rhythms and electromyographic (EMG) activity that mainly occurs during steady isometric muscle contraction. We will here focus on the~20-Hz coupling that is observed during weak isometric contraction and is linked to the modulation of the descending motor command by the~20-Hz sensorimotor rhythm. This review argues that corticokinematic and corticomuscular couplings have different neural bases. Corticokinematic coupling is mainly driven by afferent signals, while corticomuscular coupling is mainly (but not solely) driven by efferent signals. This distinction should be considered when investigating interactions between brain and body movements.

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Section: Limitations and Perspectivesmentioning

confidence: 99%

Coupling between human brain activity and body movements: Insights from non-invasive electromagnetic recordings

et al. 2019

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“…; Kerkman et al . ). Indeed, when the CNS is performing a new motor act, the reduction in the number of available dimensions simplifies the size of search space and thus motor solutions.…”

Section: Introductionmentioning

confidence: 97%

“…We hypothesized that the CNS reduces the redundancies of motor control by projecting common synaptic input to distinct motor modules in a default way, as observed during synergistic actions. This hypothesis was based on the fact that the two populations of motoneurons may receive common input from both supraspinal and afferent pathways and this strategy is needed to reduce the available number of motor dimensions (Lacquaniti et al 2012;Boonstra et al 2016;Santello et al 2016;Kerkman et al 2018). Indeed, when the CNS is performing a new motor act, the reduction in the number of available dimensions simplifies the size of search space and thus motor solutions.…”

Section: Introductionmentioning

confidence: 99%

The human central nervous system transmits common synaptic inputs to distinct motor neuron pools during non‐synergistic digit actions

Vecchio

Germer

Elias

et al. 2019

The Journal of Physiology

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Key points Neural connectivity between distinct motor neuronal modules in the spinal cord is classically studied through electrical stimulation or multi‐muscle EMG recordings. We quantified the strength of correlation in the activity of two distinct populations of motor neurons innervating the thenar and first dorsal interosseous muscles during tasks that required the two hand muscles to exert matched or un‐matched forces in different directions. We show that when the two hand muscles are concurrently activated, synaptic input to the two motor neuron pools is shared across all frequency bandwidths (representing cortical and spinal input) associated with force control. The observed connectivity indicates that motor neuron pools receive common input even when digit actions do not belong to a common behavioural repertoire. Abstract Neural connectivity between distinct motor neuronal modules in the spinal cord is classically studied through electrical stimulation or multi‐muscle EMG recordings. Here we quantify the strength of correlation in the activity of two distinct populations of motor neurons innervating the thenar and first dorsal interosseous muscles in humans during voluntary contractions. To remove confounds associated with previous studies, we used a task that required the two hand muscles to exert matched or un‐matched forces in different directions. Despite the force production task consisting of uncommon digit force coordination patterns, we found that synaptic input to motor neurons is shared across all frequency bands, reflecting cortical and spinal inputs associated with force control. The coherence between discharge timings of the two pools of motor neurons was significant at the delta (0–5 Hz), alpha (5–15 Hz) and beta (15–35 Hz) bands (P < 0.05). These results suggest that correlated input to motor neurons of two hand muscles can occur even during tasks not belonging to a common behavioural repertoire and despite lack of common innervation. Moreover, we show that the extraction of activity from motor neurons during voluntary force control removes cross‐talk associated with global EMG recordings, thus allowing direct in vivo interrogation of spinal motor neuron activity.

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“…Welch's method was used here, with window length 1 s and overlap 0.75 s. Then, intermuscular coherence (IMCOH) was computed using Welch's method and the same window parameters for all pairs of the measured muscles. Coherence is commonly used to investigate coupling between neural activities (59,60).…”

Section: Data Processingmentioning

confidence: 99%

Muscular Activity Modulation During Post-operative Walking With Hybrid Assistive Limb (HAL) in a Patient With Thoracic Myelopathy Due to Ossification of Posterior Longitudinal Ligament: A Case Report

et al. 2020

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Disorders of the central nervous system sometimes cause severe sensory motor paralysis accompanied by gait impairment. Recently, there are several reports on the effectiveness of robot-assisted gait training for patients experiencing these issues. The purpose of this case report was to assess the neuromechanical effect of a wearable robot suit HAL (Hybrid Assistive Limb) during post-operative gait training in a patient with gait impairment due to compressive myelopathy caused by ossification of the posterior longitudinal ligament (OPLL). For this purpose, we compared lower limb muscular activities while the patient was walking with and without the robot through a course of treatment sessions by (i) gait phase-dependent muscle usage analysis, (ii) muscle synergy analysis, and (iii) muscle network analysis. The results show (i) enhanced activity of the extensor muscles for weight-bearing in the initial sessions by using HAL and reduced knee extensor and increased hip extensor activations for achieving larger steps and faster gait in the later sessions; (ii) involvement of a greater number of synergies during walking with HAL than without HAL; and (iii) modulated muscle network property during walking with HAL remaining until the next HAL session. The patient's gait was improved after completing HAL sessions, acquiring close to normal joint profile with greater range of joint movement, faster walking speed, and larger step length. We discuss that the muscular activity modulation during walking with HAL suggests altered control of the muscles by the central nervous system during post-operative walking. Activity-dependent sensorimotor augmentation by HAL is discussed in the context of recovery of gait control by the central nervous system. The relationship between the altered control and the achieved gait recovery requires further investigation.

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Network structure of the human musculoskeletal system shapes neural interactions on multiple time scales

Abstract: Changes in postural task result in a frequency-dependent reconfiguration of the multiplex muscle network.

Cited by 127 publications

References 51 publications

Coupling between human brain activity and body movements: Insights from non-invasive electromagnetic recordings

Coupling between human brain activity and body movements: Insights from non-invasive electromagnetic recordings

The human central nervous system transmits common synaptic inputs to distinct motor neuron pools during non‐synergistic digit actions

Muscular Activity Modulation During Post-operative Walking With Hybrid Assistive Limb (HAL) in a Patient With Thoracic Myelopathy Due to Ossification of Posterior Longitudinal Ligament: A Case Report

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