The central nervous system (CNS) controls skeletal muscles by the recruitment of motor units (MUs). Understanding MU function is critical in the diagnosis of neuromuscular diseases, exercise physiology and sports, and rehabilitation medicine. Recording and analyzing the MUs’ electrical depolarization is the basis for state-of-the-art methods. Ultrafast ultrasound is a method that has the potential to study MUs because of the electrical depolarizations and consequent mechanical twitches. In this study, we evaluate if single MUs and their mechanical twitches can be identified using ultrafast ultrasound imaging of voluntary contractions. We compared decomposed spatio-temporal components of ultrasound image sequences against the gold standard needle electromyography. We found that 31% of the MUs could be successfully located and their firing pattern extracted. This method allows new non-invasive opportunities to study mechanical properties of MUs and the CNS control in neuromuscular physiology.
The central nervous system coordinates movement through forces generated by motor units (MUs) in skeletal muscles. To analyze MUs function is essential in sports, rehabilitation medicine applications, and neuromuscular diagnostics. The MUs and their function are studied using electromyography. Typically, these methods study only a small muscle volume (1 mm 3) or only a superficial (<1 cm) volume of the muscle. Here we introduce a method to identify so-called mechanical units, i.e., the mechanical response of electrically active MUs, in the whole muscle (4 × 4 cm, cross-sectional) under voluntary contractions by ultrafast ultrasound imaging and spatiotemporal decomposition. We evaluate the performance of the method by simulation of active MUs' mechanical response under weak contractions. We further test the experimental feasibility on eight healthy subjects. We show the existence of mechanical units that contribute to the tissue dynamics in the biceps brachii at low force levels and that these units are similar to MUs described by electromyography with respect to the number of units, territory sizes, and firing rates. This study introduces a new potential neuromuscular functional imaging method, which could be used to study a variety of questions on muscle physiology that previously were difficult or not possible to address.
Objective
In this study, the aim was to compare the performance of four spatiotemporal decomposition algorithms (stICA, stJADE, stSOBI, and sPCA) and parameters for identifying single motor units in human skeletal muscle under voluntary isometric contractions in ultrafast ultrasound image sequences as an extension of a previous study. The performance was quantified using two measures: (1) the similarity of components’ temporal characteristics against gold standard needle electromyography recordings and (2) the agreement of detected sets of components between the different algorithms.
Results
We found that out of these four algorithms, no algorithm significantly improved the motor unit identification success compared to stICA using spatial information, which was the best together with stSOBI using either spatial or temporal information. Moreover, there was a strong agreement of detected sets of components between the different algorithms. However, stJADE (using temporal information) provided with complementary successful detections. These results suggest that the choice of decomposition algorithm is not critical, but there may be a methodological improvement potential to detect more motor units.
Background: Human movement is generated by activating motor units (MUs), i.e., the smallest structures that can be voluntarily controlled. Recent findings have shown imaging of voluntarily activated MUs using ultrafast ultrasound based on displacement velocity images and a decomposition algorithm. Given this, estimates of trains of twitches (unfused tetanic signals) evoked by the neural discharges (spikes) of spinal motor neurons are provided. Based on these signals, a band-pass filter method (BPM) has been used to estimate its spike train. In addition, an improved spike estimation method consisting of a continuous Haar wavelet transform method (HWM) has been suggested. However, the parameters of the two methods have not been optimized, and their performance has not been compared rigorously. Method: HWM and BPM were optimized using simulations. Their performance was evaluated based on simulations and two experimental datasets with 21 unfused tetanic contractions considering their rate of agreement, spike offset, and spike offset variability with respect to the simulated or experimental spikes. Results: A range of parameter sets that resulted in the highest possible agreement with simulated spikes was provided. Both methods highly agreed with simulated and experimental spikes, but HWM was a better spike estimation method than BPM because it had a higher agreement, less bias, and less variation (p < 0.001). Conclusions: The optimized HWM will be an important contributor to further developing the identification and analysis of MUs using imaging, providing indirect access to the neural drive of the spinal cord to the muscle by the unfused tetanic signals.
Skeletal muscles are functionally regulated by populations of so-called motor units (MUs). An MU comprises a bundle of muscle fibers controlled by a neuron from the spinal cord. Current methods to diagnose neuromuscular diseases and monitor rehabilitation, and study sports sciences rely on recording and analyzing the bio-electric activity of the MUs. However, these methods provide information from a limited part of a muscle. Ultrasound imaging provides information from a large part of the muscle. It has recently been shown that ultrafast ultrasound imaging can be used to record and analyze the mechanical response of individual MUs using blind source separation. In this work, we present an alternative method-a deep learning pipeline-to identify active MUs in ultrasound image sequences, including segmentation of their territories and signal estimation of their mechanical responses (twitch train). We train and evaluate the model using simulated data mimicking the complex activation pattern of tens of activated MUs with overlapping territories and partially synchronized activation patterns. Using a slow fusion approach (based on 3D CNNs), we transform the spatiotemporal image sequence data to 2D representations and apply a deep neural network architecture for segmentation. Next, we employ a second deep neural network architecture for signal estimation. The results show that the proposed pipeline can effectively identify individual MUs, estimate their territories, and estimate their twitch train signal at low contraction forces. The framework can retain spatio-temporal consistencies and information of the mechanical response of MU activity even when the ultrasound image sequences are transformed into a 2D representation for compatibility with more traditional computer vision and image processing techniques. The proposed pipeline is potentially useful to identify simultaneously active MUs in whole muscles in ultrasound image sequences of voluntary skeletal muscle contractions at low force levels. INDEX TERMS motor unit, decomposition, ultrafast ultrasound, medical imaging, deep learning, mechanical response, neural networks, recurrent neural networks.
Background
Individual motor units have been imaged using ultrafast ultrasound based on separating ultrasound images into motor unit twitches (unfused tetanus) evoked by the motoneuronal spike train. Currently, the spike train is estimated from the unfused tetanic signal using a Haar wavelet method (HWM). Although this ultrasound technique has great potential to provide comprehensive access to the neural drive to muscles for a large population of motor units simultaneously, the method has a limited identification rate of the active motor units. The estimation of spikes partly explains the limitation. Since the HWM may be sensitive to noise and unfused tetanic signals often are noisy, we must consider alternative methods with at least similar performance and robust against noise, among other factors.
Results
This study aimed to estimate spike trains from simulated and experimental unfused tetani using a convolutive blind source separation (CBSS) algorithm and compare it against HWM. We evaluated the parameters of CBSS using simulations and compared the performance of CBSS against the HWM using simulated and experimental unfused tetanic signals from voluntary contractions of humans and evoked contraction of rats. We found that CBSS had a higher performance than HWM with respect to the simulated firings than HWM (97.5 ± 2.7 vs 96.9 ± 3.3, p < 0.001). In addition, we found that the estimated spike trains from CBSS and HWM highly agreed with the experimental spike trains (98.0% and 96.4%).
Conclusions
This result implies that CBSS can be used to estimate the spike train of an unfused tetanic signal and can be used directly within the current ultrasound-based motor unit identification pipeline. Extending this approach to decomposing ultrasound images into spike trains directly is promising. However, it remains to be investigated in future studies where spatial information is inevitable as a discriminating factor.
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