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.

Effect of movement-evoked and tonic experimental pain on muscle force production.

INTRODUCTION: When performing an exercise or a functional test, pain that is evoked by movement or muscle contraction could be a stronger stimulus for changing how individuals move compared to tonic pain. We investigated whether the decrease in muscle force production is larger when experimentally-induced knee pain is directly associated to the torque produced (movement-evoked) compared to a constant painful stimulation (tonic). METHODS: Twenty-one participants performed three isometric knee extension maximal voluntary contractions without pain (baseline), during pain, and after pain. Knee pain was induced using sinusoidal electrical stimuli at 10 Hz over the infrapatellar fat pad, applied continuously or modulated proportionally to the knee extension torque. Peak torque and contraction duration were averaged across repetitions and normalized to baseline. RESULTS: During tonic pain, participants reported lower pain intensity during the contraction than at rest (p < 0.001), whereas pain intensity increased with contraction during movement-evoked pain (p < 0.001). Knee extension torque decreased during both pain conditions (p < 0.001), but a larger reduction was observed during movement-evoked compared to tonic pain (p < 0.001). Participants produced torque for longer during tonic compared to movement-evoked pain (p = 0.005). CONCLUSION: Our results indicate that movement-evoked pain was a more potent stimulus to reduce knee extension torque than tonic pain. The longer contraction time observed during tonic pain may be a result of a lower perceived pain intensity during muscle contraction. Overall, our results suggest different motor adaptation to tonic and movement-evoked pain and support the notion that motor adaptation to pain is a purposeful strategy to limit pain. This mechanistic evidence suggests that individuals experiencing prevalently tonic or movement-evoked pain may exhibit different motor adaptations, which may be important for exercise prescription.

Home-based arm cycling exercise improves trunk control in persons with incomplete spinal cord injury: an observational study.

Arm cycling is used for cardiorespiratory rehabilitation but its therapeutic effects on the neural control of the trunk after spinal cord injury (SCI) remain unclear. We investigated the effects of single session of arm cycling on corticospinal excitability, and the feasibility of home-based arm cycling exercise training on volitional control of the erector spinae (ES) in individuals with incomplete SCI. Using transcranial magnetic stimulation, we assessed motor evoked potentials (MEPs) in the ES before and after 30 min of arm cycling in 15 individuals with SCI and 15 able-bodied controls (Experiment 1). Both groups showed increased ES MEP size after the arm cycling. The participants with SCI subsequently underwent a 6-week home-based arm cycling exercise training (Experiment 2). MEP amplitudes and activity of the ES, and movements of the trunk during reaching, self-initiated rapid shoulder flexion, and predicted external perturbation tasks were measured. After the training, individuals with SCI reached further and improved trajectory of the trunk during the rapid shoulder flexion task, accompanied by increased ES activity and MEP amplitudes. Exercise adherence was excellent. We demonstrate preserved corticospinal drive after a single arm cycling session and the effects of home-based arm cycling exercise training on trunk function in individuals with SCI.

Spinal kinematic variability is increased in people with chronic low back pain during a repetitive lifting task.

Changes in spinal kinematic variability have been observed in people with chronic non-specific LBP (CNSLBP) during the performance of various repetitive functional tasks. However, the direction of these changes (i.e., less or more kinematic variability) is not consistent. This study aimed to assess differences in kinematic variability of the 3D angular displacement of thoracic and lumbar spinal segments in people with CNSLBP compared to asymptomatic individuals during a repetitive lifting task. Eleven people with CNSLBP and 11 asymptomatic volunteers performed 10 cycles of multi-planar lifting movements while spinal kinematics were recorded. For the three planes of motion, point-by-point standard deviations (SDs) were computed across all cycles of lifting and the average was calculated as a measure of kinematic variability for both segments. People with CNSLBP displayed higher thoracic (F = 8.00, p = 0.010, ηp2 = 0.286) and lumbar kinematic variability (F = 5.48, p = 0.030, ηp2 = 0.215) in the sagittal plane. Moreover, group differences were observed in the transversal plane for thoracic (F = 7.62, p = 0.012, ηp2 = 0.276) and lumbar kinematic variability (F = 5.402, p = 0.031, ηp2 = 0.213), as well as in the frontal plane for thoracic (F = 7.27, p = 0.014, ηp2 = 0.267) and lumbar kinematic variability (F = 6.11, p = 0.022, ηp2 = 0.234), all showing higher variability in those with CNSLBP. A significant main effect of group was not detected (p > 0.05) for spinal range of motion (ROM). Thus, people with CNSLBP completed the lifting task with the same ROM in all three planes of motion as observed for asymptomatic individuals, yet they performed the lifting task with higher spinal kinematic cycle-to-cycle variation.

Neuromuscular adaptations to experimentally induced pain in the lumbar region: systematic review and meta-analysis.

ABSTRACT: Experimental pain models are frequently used to understand the influence of pain on the control of human movement. In this systematic review, we assessed the effects of experimentally induced pain in the lumbar region of healthy individuals on trunk muscle activity and spine kinematics. Databases were searched from inception up to January 31, 2022. In total, 26 studies using either hypertonic saline injection (n = 19), heat thermal stimulation (n = 3), nociceptive electrical stimulation (n = 3), or capsaicin (n = 1) were included. The identified adaptations were task dependent, and their heterogeneity was partially explained by the experimental pain model adopted. Meta-analyses revealed an increase of erector spinae activity (standardized mean difference = 0.71, 95% confidence interval [CI] = 0.22-1.19) during full trunk flexion and delayed onset of transversus abdominis to postural perturbation tasks (mean difference = 25.2 ms, 95% CI = 4.09-46.30) in the presence of pain. Low quality of evidence supported an increase in the activity of the superficial lumbar muscles during locomotion and during voluntary trunk movements during painful conditions. By contrast, activity of erector spinae, deep multifidus, and transversus abdominis was reduced during postural perturbation tasks. Reduced range of motion of the lumbar spine in the presence of pain was supported by low quality of evidence. Given the agreement between our findings and the adaptations observed in clinical populations, the use of experimental pain models may help to better understand the mechanisms underlying motor adaptations to low back pain.

Non-uniform excitation of pectoralis major induced by changes in bench press inclination leads to uneven variations in the cross-sectional area measured by panoramic ultrasonography.

This study combined surface electromyography with panoramic ultrasound imaging to investigate whether non-uniform excitation could lead to acute localized variations in cross-sectional area and muscle thickness of the clavicular and sternocostal heads of pectoralis major (PM). Bipolar surface electromyograms (EMGs) were acquired from both PM heads, while 13 men performed four sets of the flat and 45° inclined bench press exercises. Before and immediately after exercise, panoramic ultrasound images were collected transversely to the fibers. Normalized root mean square (RMS) amplitude and variations in the cross-sectional area and muscle thickness were calculated separately for each PM head. For all sets of the inclined bench press, the normalized RMS amplitude was greater for the clavicular head than the sternocostal head (P < 0.001), and the opposite was observed during the flat bench press (P < 0.001). Similarly, while greater increases in cross-sectional area were observed in the clavicular than in the sternocostal head after the inclined bench press (P < 0.001), greater increases were quantified in the sternocostal than in the clavicular head after the flat bench press exercise (P = 0.046). Therefore, our results suggest that the PM regional excitation induced by changes in bench press inclination leads to acute, uneven responses of muscle architecture following the exercise.

Differences between vastus medialis and lateralis excitation onsets are dependent on the relative distance of surface electrodes placement from the innervation zone location.

Conflictual results between the onset of vastus medialis (VM) and vastus lateralis (VL) excitation may arise from methodological aspects related to the detection of surface electromyograms. In this study we used an array of surface electrodes to assess the effect of detection site, relative to the muscle innervation zone, on the difference between VM and VL excitation onsets. Ten healthy males performed moderate isometric knee extension at 40 % of their maximal voluntary isometric contraction. After the actual VM-VL onset was defined (estimated when action potentials were generated at the neuromuscular junctions of both muscles), we calculated the largest bias that the detection site may introduce in the VM-VL onset estimation. We also assessed whether the location often considered for positioning bipolar electrodes on each muscle leads to VM-VL onset estimations comparable to the actual VM-VL onset. Our main results revealed that a maximum absolute bias of 20.48 ms may be introduced in VM-VL onset estimations due to the electrodes' detection site. In addition, mean differences of âˆ¼ 12 ms in VM-VL onset estimations were attributable to largest possible discrepancies in the paired position of channels with respect to the innervation zone for VL and VM. When considering the classical location for positioning the bipolar electrodes over these muscles, differences error was subtle (∼3.4 ms) when compared with the actual VM-VL onset. Nonetheless, when accounting for the effect of relative differences in electrode position between muscles is not possible, our results suggest that a systematic absolute error of âˆ¼ 12 ms should be considered in future studies regarding VM-VL onset estimations, suggesting that onset differences lower than that might not be clinically relevant.

Non-uniform excitation of the pectoralis major muscle during flat and inclined bench press exercises.

Non-physiological sources may lead to equivocal interpretation on the degree of muscle excitation from electromyograms (EMGs) amplitude. This presumably explains the contradictory findings regarding the effect of the bench press inclination on the pectoralis major (PM) activation pattern. To contend with these issues, herein we used high-density surface EMG to investigate whether different PM regions are excited during the flat and 45° inclined bench press exercises. Single-differential EMGs were collected from 15 regions along the PM cranio-caudal axis, while 8 volunteers performed a set of the flat and 45° inclined bench press at 50% and 70% of 1 repetition maximum. The coefficient of variation, the range of motion, and the cycle duration were calculated from the barbell vertical position to assess the within-subject consistency across cycles. The number of channels detecting the largest EMGs amplitude (active channels), their interquartile range, and their barycentre coordinate were assessed to characterize the EMG amplitude distribution within PM. No significant differences in the range of motion (p > 0.11), cycle duration (p > 0.28), number of active channels (p > 0.05), and interquartile range of active channels (p > 0.39) were observed between the two bench press inclinations. Conversely, the barycentre shifted toward the PM clavicular region (p < 0.001) when the bench press changed from flat to 45°. Our results revealed that greatest EMG amplitudes were concentrated at the PM sternocostal and clavicular heads when exercising in the flat and 45° inclined bench press, respectively. Performing the bench press exercise, with different postures, seem to demand the excitation of different PM regions.

Neuromuscular adaptations to experimentally induced pain in the lumbar region: protocol for a systematic review and meta-analysis.

BACKGROUND: Numerous studies report changes in neuromuscular control in people with low back pain (LBP). However, the relationship between pain and altered neuromuscular control is challenging to unravel given the heterogeneity that exists in clinical populations. One approach commonly adopted to overcome this issue is the use of experimental pain models, but it is currently unclear if the effects of experimental pain are consistent between studies. Therefore, this planned study will systematically evaluate and summarise the effect of experimentally induced pain in the lumbar region on neuromuscular control at sites both locally and remote to the low back. METHODS: This protocol has been developed following the Preferred Reporting Items for Systematic Review and Meta-Analysis Protocols (PRISMA-P). MEDLINE, EMBASE, CINAHL, ZETOC, Web of Science, and grey literature will be searched up to August 31, 2021. Screening processes (title/abstract and full-text), data extraction, and risk of bias assessment will be conducted by two independent reviewers. Studies investigating the effects of exogenous pain models delivered to the low back region on neuromuscular control in healthy individuals will be included. Muscle activity and body kinematics will be the outcomes of interest. The comparisons of interest will be between baseline or control conditions and the experimental pain condition, as well as between the experimental pain and post-pain conditions. Randomised crossover and non-randomised studies of interventions will be included and their risk of bias will be evaluated with the Cochrane Risk-of-Bias tool or with the Risk Of Bias In Non-randomised Studies of Interventions tool, respectively. A random-effect meta-analysis will be conducted for quantitative synthesis when clinical and methodological consistency is ensured. Quality of evidence will be evaluated using the Grading of Recommendations, Assessment, Development and Evaluation guidelines. DISCUSSION: The current review will provide new insights to understand if and what neuromuscular adaptations are caused by pain experimentally induced in the lumbar region. Our findings will reveal which experimental pain model is able to better reproduce adaptations similar to those identified in people with low back pain, possibly contributing to improving our understanding of motor adaptation to low back pain in the long term. SYSTEMATIC REVIEW REGISTRATION: PROSPERO CRD42020220130.

Surface wave elastography is a reliable method to correlate muscle elasticity, torque, and electromyography activity level.

The shear elastic modulus is one of the most important parameters to characterize the mechanical behavior of soft tissues. In biomechanics, ultrasound elastography is the gold standard for measuring and mapping it locally in skeletal muscle in vivo. However, their applications are limited to the laboratory or clinic. Thus, low-frequency elastography methods have recently emerged as a novel alternative to ultrasound elastography. Avoiding the use of high frequencies, these methods allow obtaining a mean value of bulk shear elasticity. However, they are frequently susceptible to diffraction, guided waves, and near field effects, which introduces biases in the estimates. The goal of this work is to test the performance of the non-ultrasound surface wave elastography (NU-SWE), which is portable and is based on new algorithms designed to correct the incidence of such effects. Thus, we show its first application to muscle biomechanics. We performed two experiments to assess the relationships of muscle shear elasticity versus joint torque (experiment 1) and the electromyographic activity level (experiment 2). Our results were comparable regarding previous works using the reference ultrasonic methods. Thus, the NU-SWE showed its potentiality to get wide the biomechanical applications of elastography in many areas of health and sports sciences.

Changes in supramaximal M-wave amplitude at different regions of biceps brachii following eccentric exercise of the elbow flexors.

PURPOSE: Previous evidence from surface electromyograms (EMGs) suggests that exercise-induced muscle damage (EIMD) may manifest unevenly within the muscle. Here we investigated whether these regional changes were indeed associated with EIMD or if they were attributed to spurious factors often affecting EMGs. METHODS: Ten healthy male subjects performed 3 × 10 eccentric elbow flexions. Maximal voluntary contraction (MVC), muscle soreness and ultrasound images from biceps brachii distal and proximal regions were measured immediately before (baseline) and during each of the following 4 days after the exercise. Moreover, 64 monopolar surface EMGs were detected while 10 supramaximal pulses were applied to the musculocutaneous nerve. The innervation zone (IZ), the number of electrodes detecting largest M-waves and their centroid longitudinal coordinates were assessed to characterize the spatial distribution of the M-waves amplitude. RESULTS: The MVC torque decreased (~ 25%; P < 0.001) while the perceived muscle soreness scale increased (~ 4 cm; 0 cm for no soreness and 10 cm for highest imaginable soreness; P < 0.005) across days. The echo intensity of the ultrasound images increased at 48 h (71%), 72 h (95%) and 96 h (112%) for both muscle regions (P < 0.005), while no differences between regions were observed (P = 0.136). The IZ location did not change (P = 0.283). The number of channels detecting the greatest M-waves significantly decreased (up to 10.7%; P < 0.027) and the centroid longitudinal coordinate shifted distally at 24, 48 and 72 h after EIMD (P < 0.041). CONCLUSION: EIMD consistently changed supramaximal M-waves that were detected mainly proximally from the biceps brachii, suggesting that EIMD takes place locally within the biceps brachii.

Both the resistance training session and the static stretching after exercise does not affect the pectoralis major stiffness of well-trained men.

Previous evidence suggests the intense resistance training session can increase the muscle hardness, while stretching protocols with high intensity and volume can decrease it. However, it remains unknown the effects of an exercise and a less intensive stretching maneuver on muscle stiffness of well-trained men. Herein we (i) analyze the acute effects of heavy bench press exercise on the pectoralis major muscle shear modulus of well-trained men and (ii) assess the effectiveness of a 1-min stretching maneuver applied on this muscle after the exercise using shear wave elastography. Fourteen participants performed three sets of bench press from 8 to 13 repetitions maximum. Immediately after the exercise, their right shoulder was passively stretched for 1 min (stretched side) while their left arm stayed relaxed along the side of the body (control side). Elastographic images were acquired for the pectoralis major mid-region of both sides before the exercise, immediately after the intervention and after 5 min of rest. Our results revealed that both the bench press exercise and the static stretching does not affect the pectoralis major shear modulus of well-trained men. Conversely, the shear modulus significantly decreased at 5 min after intervention with respect to immediately after, for both the stretched (from 5.52 to 4.29 kPa) and the control sides (from 5.87 to 4.56 kPa). Therefore, both resistance training session and 1-min static stretching were not sufficient to significantly change the pectoralis major muscle stiffness of well-trained men.

Innervation zone locations distribute medially within the pectoralis major muscle during bench press exercise.

Changes in innervation zone (IZ) position may affect the amplitude of surface electromyograms (EMGs). If not accounted for, these changes may lead to equivocal interpretation on the degree of muscle activity from EMG amplitude. In this study we ask how much the IZ position changes within different regions of the pectoralis major (PM) during the bench press exercise. If expressive, changes in IZ position may explain the conflictual results reported on PM activation during bench press. Single-differential surface EMGs were collected from 15 regions along the PM cranial, centro-cranial, centro-caudal and caudal fibres, while 11 healthy participants gently, isometrically contracted their muscle. IZs were identified visually, from EMGs collected with the glenohumeral joint at extreme bench press positions; 20° and 110° of abduction in the horizontal plane. Except for 3 out of 88 acquisitions (4 detection sites × 2 glenohumeral angles × 11 participants), for which no phase opposition and action potential propagation were observed, IZs could be well identified. Group results revealed the IZ moved medially from 110° to 20° of glenohumeral joint abduction in the horizontal plane, regardless of the PM region from where EMGs were detected (P < 0.01). IZs were confined medially within PM, from ∼20% to ∼40% of the muscle-tendon unit length, and their position changed up to 13.3%. These results suggest that changes in the amplitude of EMGs detected mainly medially from PM may be not associated with changes in the degree of PM activity during bench press.

Is the firing rate of motor units in different vastus medialis regions modulated similarly during isometric contractions?

INTRODUCTION: Previous evidence suggests the fibers of different motor units reside within distinct vastus medialis (VM) regions. It remains unknown whether the activity of these motor units may be modulated differently. Herein we assess the discharge rate of motor units detected proximodistally from the VM to address this issue. METHODS: Surface electromyograms (EMGs) were recorded proximally and distally from the VM while 10 healthy subjects performed isometric contractions. Single motor units were decomposed from surface EMGs. The smoothed discharge rates of motor units identified from the same and from different VM regions were then cross-correlated. RESULTS: During low-level contractions, the discharge rate varied more similarly for distal (cross-correlation peak; interquartile interval: 0.27-0.40) and proximal (0.28-0.52) than for proximodistal pairs of VM motor units (0.20-0.33; P = 0.006). DISCUSSION: The discharge rates of motor units from different proximodistal VM regions show less similarity in their variations than those of pairs of units either distally or proximally. Muscle Nerve 57: 279-286, 2018.