Neural filtering of physiological tremor oscillations to spinal motor neurons mediates short-term acquisition of a skill learning task.

The acquisition of a motor skill involves adaptations of spinal and supraspinal pathways to alpha motoneurons. In this study, we estimated the shared synaptic contributions of these pathways to understand the neural mechanisms underlying the short-term acquisition of a new force-matching task. High-density surface electromyography (HDsEMG) was acquired from the first dorsal interosseous (FDI; 7 males and 6 females) and tibialis anterior (TA; 7 males and 4 females) during 15 trials of an isometric force-matching task. For two selected trials (pre- and post-skill acquisition), we decomposed the HDsEMG into motor unit spike trains, tracked motor units between trials, and calculated the mean discharge rate and the coefficient of variation of inter-spike interval (CoVISI). We also quantified the post/pre ratio of motor units' coherence within delta, alpha, and beta bands. Force-matching improvements were accompanied by increased mean discharge rate and decreased CoVISI for both muscles. Moreover, the area under the curve within alpha band decreased by ∼22% (TA) and ∼13% (FDI), with no delta or beta bands changes. These reductions correlated significantly with increased coupling between force/neural drive and target oscillations. These results suggest that short-term force-matching skill acquisition is mediated by attenuation of physiological tremor oscillations in the shared synaptic inputs. Supported by simulations, a plausible mechanism for alpha band reductions may involve spinal interneurons phase-cancelling descending oscillations. Therefore, during skill learning, the central nervous system acts as a matched filter, adjusting synaptic weights of shared inputs to suppress neural components unrelated to the specific task.Significance statement Previous studies have proposed that only the low-frequency oscillations of shared synaptic inputs to motor neurons, encompassing task-related and task-unrelated oscillations, are responsible for the generated muscle force. In our study, we investigated whether the acquisition of a new motor task involving precise force generation requires specific alterations in these shared synaptic inputs. Our findings demonstrated that, for both a hand muscle and a leg muscle, the skill acquisition was mediated by a reduction in shared synaptic oscillations unrelated to the required force fluctuations (i.e., physiological tremor band oscillations). Therefore, during the force-matching task learning, the central nervous system acts like a neural filter, modulating the synaptic weights of shared inputs to attenuate neural components unrelated to the specific task.

Muscle contractile properties directly influence shared synaptic inputs to spinal motor neurons.

Alpha band oscillations in shared synaptic inputs to the alpha motor neuron pool can be considered an involuntary source of noise that hinders precise voluntary force production. This study investigated the impact of changing muscle length on the shared synaptic oscillations to spinal motor neurons, particularly in the physiological tremor band. Fourteen healthy individuals performed low-level dorsiflexion contractions at ankle joint angles of 90° and 130°, while high-density surface electromyography (HDsEMG) was recorded from the tibialis anterior (TA). We decomposed the HDsEMG into motor units spike trains and calculated the motor units' coherence within the delta (1-5 Hz), alpha (5-15 Hz), and beta (15-35 Hz) bands. Additionally, force steadiness and force spectral power within the tremor band were quantified. Results showed no significant differences in force steadiness between 90° and 130°. In contrast, alpha band oscillations in both synaptic inputs and force output decreased as the length of the TA was moved from shorter (90°) to longer (130°), with no changes in delta and beta bands. In a second set of experiments (10 participants), evoked twitches were recorded with the ankle joint at 90° and 130°, revealing longer twitch durations in the longer TA muscle length condition compared to the shorter. These experimental results, supported by a simple computational simulation, suggest that increasing muscle length enhances the muscle's low-pass filtering properties, influencing the oscillations generated by the Ia afferent feedback loop. Therefore, this study provides valuable insights into the interplay between muscle biomechanics and neural oscillations. KEY POINTS: We investigated whether changes in muscle length, achieved by changing joint position, could influence common synaptic oscillations to spinal motor neurons, particularly in the tremor band (5-15 Hz). Our results demonstrate that changing muscle length from shorter to longer induces reductions in the magnitude of alpha band oscillations in common synaptic inputs. Importantly, these reductions were reflected in the oscillations of muscle force output within the alpha band. Longer twitch durations were observed in the longer muscle length condition compared to the shorter, suggesting that increasing muscle length enhances the muscle's low-pass filtering properties. Changes in the peripheral contractile properties of motor units due to changes in muscle length significantly influence the transmission of shared synaptic inputs into muscle force output. These findings prove the interplay between muscle mechanics and neural adaptations.

Beyond Belief: Exploring the Alignment of Self-Efficacy, Self-Prediction, Self-Perception, and Actual Performance Measurement in a Squat Jump Performance-A Pilot Study.

It is widely accepted that athletic performance emerges from a complex interaction between physical and cognitive features. Several studies highlighted self-efficacy (SE) in the cognitive domain of athletic performance, but no studies have correlated SE with sport-specific tasks. According to Bandura, this study explored SE and its relationship with self-prediction (SP), self-perception (PSJ), and actual performance in a squat jump (SJ). Thirty-nine healthy collegiate students were assessed using an SE questionnaire, an SP measurement tool, and a validated optical system for actual SJ performance. An SE score and an SE esteem index (SEE) were determined. The alignment between an individual's SP of their SJ performance and their SE beliefs was also examined. The data revealed a significant correlation between SE score and both SJ (r = 0.432; p = 0.006) and SP (r = 0.441; p = 0.005). Furthermore, disparities among the actual SJ, SP, and SEE were statistically non-significant, implying a congruence between self-belief and performance. With a deeper understanding of the interaction between SE, SP, and sport-specific tasks, sports professionals could develop targeted interventions to enhance athletes' overall athletic achievements and apply SE as a feature linking physical and cognitive athletic performance.

Electrophysiological neuromuscular alterations and severe fatigue predict long-term muscle weakness in survivors of COVID-19 acute respiratory distress syndrome.

Introduction: Long-term weakness is common in survivors of COVID-19-associated acute respiratory distress syndrome (CARDS). We longitudinally assessed the predictors of muscle weakness in patients evaluated 6 and 12 months after intensive care unit discharge with in-person visits. Methods: Muscle strength was measured by isometric maximal voluntary contraction (MVC) of the tibialis anterior muscle. Candidate predictors of muscle weakness were follow-up time, sex, age, mechanical ventilation duration, use of steroids in the intensive care unit, the compound muscle action potential of the tibialis anterior muscle (CMAP-TA-S100), a 6-min walk test, severe fatigue, depression and anxiety, post-traumatic stress disorder, cognitive assessment, and body mass index. We also compared the clinical tools currently available for the evaluation of muscle strength (handgrip strength and Medical Research Council sum score) and electrical neuromuscular function (simplified peroneal nerve test [PENT]) with more objective and robust measures of force (MVC) and electrophysiological evaluation of the neuromuscular function of the tibialis anterior muscle (CMAP-TA-S100) for their essential role in ankle control. Results: MVC improved at 12 months compared with 6 months. CMAP-TA-S100 (P = 0.016) and the presence of severe fatigue (P = 0.036) were independent predictors of MVC. MVC was strongly associated with handgrip strength, whereas CMAP-TA-S100 was strongly associated with PENT. Discussion: Electrical neuromuscular abnormalities and severe fatigue are independently associated with reduced MVC and can be used to predict the risk of long-term muscle weakness in CARDS survivors.

Sex-differences in the longitudinal recovery of neuromuscular function in COVID-19 associated acute respiratory distress syndrome survivors.

Introduction: Patients admitted to the intensive care unit (ICU) following severe acute respiratory syndrome 2 (SARS-CoV-2) infection may have muscle weakness up to 1 year or more following ICU discharge. However, females show greater muscle weakness than males, indicating greater neuromuscular impairment. The objective of this work was to assess sex differences in longitudinal physical functioning following ICU discharge for SARS-CoV-2 infection. Methods: We performed longitudinal assessment of physical functioning in two groups: 14 participants (7 males, 7 females) in the 3-to-6 month and 28 participants (14 males, 14 females) in the 6-to-12 month group following ICU discharge and assessed differences between the sexes. We examined self-reported fatigue, physical functioning, compound muscle action potential (CMAP) amplitude, maximal strength, and the neural drive to the tibialis anterior muscle. Results: We found no sex differences in the assessed parameters in the 3-to-6-month follow-up, indicating significant weakness in both sexes.Sex differences emerged in the 6-to-12-month follow-up. Specifically, females exhibited greater impairments in physical functioning, including lower strength, walking lower distances, and high neural input even 1 year following ICU-discharge. Discussion: Females infected by SARS-CoV-2 display significant impairments in functional recovery up to 1 year following ICU discharge. The effects of sex should be considered in post-COVID neurorehabilitation.

Neuromuscular Fatigue Affects Calf Muscle Activation Strategies, but Not Dynamic Postural Balance Control in Healthy Young Adults.

Neuromuscular fatigue could negatively affect postural balance, but its effects on dynamic postural regulation are still debated. This study aimed to investigate whether a fatigue protocol on calf muscle could affect muscle activation strategies and dynamic balance performance. Seventeen male adults (age 24.1 ± 4.6 years; height 183.9 ± 7.2 cm; weight 80.2 ± 7.2 kg) volunteered in the study. They performed a dynamic test on an instrumented platform, which provided anterior-posterior oscillations on the sagittal plane, before and after a localized fatigue protocol. High-density surface electromyographical (EMG) signals were recorded bilaterally from the soleus and the medial gastrocnemius muscles. The fatigue protocol, consisting of two quasi-isometric tiptoe standing exercise to failure with a fixed load, did not affect the global dynamic balance performance. Conversely, the frequency value corresponding to 95% of the total power spectrum density of the angular displacement signal increased after fatigue (from 1.03 ± 0.42 to 1.31 ± 0.42 Hz; p < 0.05). The EMG analysis showed a significant difference in the PRE/POST fatigue ratio of the root-mean-square (RMS) between the soleus and the gastrocnemius medialis muscles. No differences were detected for the coefficient of variation and the barycenter coordinates of the RMS EMG values between muscles and sides. The variations in the frequency content of the angular displacement and EMG activity across muscles may be related to an increase in the calf muscles stiffness after fatigue. The role of neuromechanical calf muscle properties seems to be relevant in maintaining the dynamic postural performance after a quasi-isometric fatigue protocol until failure.

The force-generation capacity of the tibialis anterior muscle at different muscle-tendon lengths depends on its motor unit contractile properties.

PURPOSE: Muscle-tendon length can influence central and peripheral motor unit (MU) characteristics, but their interplay is unknown. This study aims to explain the effect of muscle length on MU firing and contractile properties by applying deconvolution of high-density surface EMG (HDEMG), and torque signals on the same MUs followed at different lengths during voluntary contractions. METHODS: Fourteen participants performed isometric ankle dorsiflexion at 10% and 20% of the maximal voluntary torque (MVC) at short, optimal, and long muscle lengths (90°, 110°, and 130° ankle angles, respectively). HDEMG signals were recorded from the tibialis anterior, and MUs were tracked by cross-correlation of MU action potentials across ankle angles and torques. Torque twitch profiles were estimated using model-based deconvolution of the torque signal based on composite MU spike trains. RESULTS: Mean discharge rate of matched motor units was similar across all muscle lengths (P = 0.975). Interestingly, the increase in mean discharge rate of MUs matched from 10 to 20% MVC force levels at the same ankle angle was smaller at 110° compared with the other two ankle positions (P = 0.003), and the phenomenon was explained by a greater increase in twitch torque at 110° compared to the shortened and lengthened positions (P = 0.002). This result was confirmed by the deconvolution of electrically evoked contractions at different stimulation frequencies and muscle-tendon lengths. CONCLUSION: Higher variations in MU twitch torque at optimal muscle lengths likely explain the greater force-generation capacity of muscles in this position.

Half marathon induces changes in central control and peripheral properties of individual motor units in master athletes.

Acute changes in central control and peripheral properties of motor units following a half-marathon has never been examined in master athletes. Therefore, the main purpose of this study was to estimate the firing properties and twitch characteristics of motor units after a 21-km race in a group of ten trained older adults. High-density surface EMG decomposition was used to identify motor unit activity during a submaximal contraction of the tibialis anterior muscle before and after the half marathon. The area of the estimated motor unit twitch profile was found smaller after the race (P = 0.039). This reduction in contractile efficiency was compensated by a significant increase in the initial and average discharge rate of the identified motor units (P < 0.001). By estimating the amount of shared and independent synaptic input to tibialis anterior motor neurons, we demonstrated that adaptations in the discharge properties of master athletes' motor units are the likely consequence of an increased net excitatory synaptic drive to the motor neuron pool. These findings suggest a potential role of long-distance running in ameliorating declines in muscle function of older adults by enhancing the neural drive to muscle.