Kinematics of individual muscle units in natural contractions measured in vivo using ultrafast ultrasound

Abstract

The study of human neuromechanical control at the motor unit (MU) level has predominantly focussed on electrical activity and force generation, whilst the link between these, the muscle deformation, has not been widely studied. Here, we describe a methodology utilising ultrafast ultrasound (US), allowing imaging of up to tens of thousands of frames per second, to measure the deformation of the muscular tissue due to individual MU twitches for a population of active MUs during voluntary contractions. We used the spiking activity of MUs decomposed from high-density surface electromyography recordings of the tibialis anterior muscle to guide the analysis of simultaneously recorded ultrafast US. With a novel analysis on the US images we identified, with high spatio-temporal precision, the velocity maps associated with single MU movements. From the individual MU profiles obtained from the velocity maps, the region of movement, the duration of the mechanical twitch, the total and active contraction times, and the activation time were computed. The latter features, the temporal features, showed high repeatability across different force levels. The former feature, the spatial feature, showed high consistency across force levels, however the complicated dynamics of the muscle motion resulted in morphing and translation of these regions. Furthermore, the experimental measures provided the first evidence of muscle unit twisting during voluntary contractions. The proposed approach allows, for the first time, non-invasive recordings of muscle deformation due to individual MU activations during voluntary contractions.Key pointsWe identified the activity of single motor units (MUs) from high-density surface electromyography (HDsEMG) and used this information in combination with ultrafast ultrasound to extract local muscle motion due to the contraction of individual muscle unitsMultiple MUs, including those with fibres overlapping in space, can be simultaneously and individually detected using this techniqueThe proposed method allows us to measure both the spiking activity of motor units and their movement within the muscles concomitantlyThe technique allows for populations of MUs to be tracked and monitored in the electrical and mechanical domains simultaneously and non-invasively during natural contractions, thus achieving a high spatio-temporal resolution in the characterization of MU behaviour

A fast blind source separation algorithm for decomposing ultrafast ultrasound images into spatiotemporal muscle unit kinematics

“…The nEMG recordings consisted of weaker force levels (less active motor units, MUs). Thus, this confirms the observations of a negative correlation between spike-triggered average twitch amplitude and force level made in Lubel et al [31]. The impact of computational time on the parameter values in the proposed velocity blind source separation (velBSS) algorithm for two different recordings (nEMG and sEMG).…”

“…The nEMG recordings consisted of weaker force levels (less active motor units, MUs). Thus, this confirms the observations of a negative correlation between spike-triggered average twitch amplitude and force level made in Lubel et al[31].…”

“…However, a MU with split territories may become two separate components. In addition, many active MUs complicate the displacement field at higher force levels due to the heterogenic composition of linear and non-linear elastic constituents [31]. Thus, we expect non-linear mechanics where this algorithm may still detect the largest and strongest MUs with possibly distorted mechanical signals and small amplitude spike-triggered averaged twitches.…”

Spatially repeatable components from ultrafast ultrasound are associated with motor unit activity in human isometric contractions *

“…Moreover, we assume that MU activities can be linearly summed together in the velocity field. However, recent findings have observed non-linear summations [46]. Nevertheless, it should only affect the estimated temporal signals and not the spatial location of the MU during stable isometric contractions.…”