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.

How many motor units is enough? An assessment of the influence of the number of motor units on firing rate calculations.

The number of motor units included in calculations of mean firing rates varies widely in the literature. It is unknown how the number of decomposed motor units included in the calculation of firing rate per participant compares to the total number of active motor units in the muscle, and if this is different for males and females. Bootstrapped distributions and confidence intervals (CI) of mean motor unit firing rates decomposed from the tibialis anterior were used to represent the total number of active motor units for individual participants in trials from 20 to 100 % of maximal voluntary contraction. Bootstrapped distributions of mean firing rates were constructed using different numbers of motor units, from one to the maximum number for each participant, and compared to the CIs. A probability measure for each number of motor units involved in firing rate was calculated and then averaged across all individuals. Motor unit numbers required for similar levels of probability increased as contraction intensity increased (p < 0.001). Increased levels of probability also required higher numbers of motor units (p < 0.001). There was no effect of sex (p ≥ 0.97) for any comparison. This methodology should be repeated in other muscles, and aged populations.

The effects of periodic and noisy tendon vibration on a kinesthetic targeting task.

Tendon vibration is used extensively to assess the role of peripheral mechanoreceptors in motor control, specifically, the muscle spindles. Periodic tendon vibration is known to activate muscle spindles and induce a kinesthetic illusion that the vibrated muscle is longer than it actually is. Noisy tendon vibration has been used to assess the frequency characteristics of proprioceptive reflex pathways during standing; however, it is unknown if it induces the same kinesthetic illusions as periodic vibration. The purpose of the current study was to assess the effects of both periodic and noisy tendon vibration in a kinesthetic targeting task. Participants (N = 15) made wrist extension movements to a series of visual targets without vision of the limb, while their wrist flexors were either vibrated with periodic vibration (20, 40, 60, 80, and 100 Hz), or with noisy vibration which consisted of filtered white noise with power between ~ 20 and 100 Hz. Overall, our results indicate that both periodic and noisy vibration can induce robust targeting errors during a wrist targeting task. Specifically, the vibration resulted in an undershooting error when moving to the target. The findings from this study have important implications for the use of noisy tendon vibration to assess proprioceptive reflex pathways and should be considered when designing future studies using noisy vibration.

Effects of postural threat on perceptions of lower leg somatosensory stimuli during standing.

Height-induced postural threat affects emotional state and standing balance behaviour during static, voluntary, and dynamic tasks. Facing a threat to balance also affects sensory and cortical processes during balance tasks. As sensory and cognitive functions are crucial in forming perceptions of movement, balance-related changes during threatening conditions might be associated with changes in conscious perceptions. Therefore, the purpose of this study was to examine the changes and potential mechanisms underlying conscious perceptions of balance-relevant information during height-induced postural threat. A combination of three experimental procedures utilized height-induced postural threat to manipulate emotional state, balance behavior, and/or conscious perceptions of balance-related stimuli. Experiment 1 assessed conscious perception of foot position during stance. During continuous antero-posterior pseudorandom support surface rotations, perceived foot movement was larger while actual foot movement did not change in the High (3.2 m, at the edge) compared to Low (1.1 m, away from edge) height conditions. Experiment 2 and 3 assessed somatosensory perceptual thresholds during upright stance. Perceptual thresholds for ankle rotations were elevated while foot sole vibrations thresholds remained unchanged in the High compared to Low condition. This study furthers our understanding of the relationship between emotional state, sensory perception, and balance performance. While threat can influence the perceived amplitude of above threshold ankle rotations, there is a reduction in the sensitivity of an ankle rotation without any change to foot sole sensitivity. These results highlight the effect of postural threat on neurophysiological and cognitive components of balance control and provide insight into balance assessment and intervention.

The role of torque feedback in standing balance.

It has been proposed that sensory force/pressure cues are integrated within a positive feedback mechanism, which accounts for the slow dynamics of human standing behavior and helps align the body with gravity. However, experimental evidence of this mechanism remains scarce. This study tested predictions of a positive torque feedback mechanism for standing balance, specifically that differences between a "reference" torque and actual torque are self-amplified, causing the system to generate additional torque. Seventeen healthy young adults were positioned in an apparatus that permitted normal sway at the ankle until a brake on the apparatus was applied, discreetly "locking" body movement during stance. Once locked, a platform positioned under the apparatus remained in place (0 mm) or slowly translated backward (3 mm or 6 mm), tilting subjects forward. Postural behavior was characterized by two distinct responses: the center of pressure (COP) offset (i.e., change in COP elicited by the surface translation) and the COP drift (i.e., change in COP during the sustained tilt). Model simulations were performed using a linear balance control model containing torque feedback to provide a conceptual basis for the interpretation of experimental results. Holding the body in sustained tilt positions resulted in COP drifting behavior, reflecting attempts of the balance control system to restore an upright position through increases in plantar flexor torque. In line with predictions of positive torque feedback, larger COP offsets led to faster increases in COP over time. These findings provide experimental support for a positive torque feedback mechanism involved in the control of standing balance.NEW & NOTEWORTHY Using model simulations and a novel experimental approach, we tested behavioral predictions of a sensory torque feedback mechanism involved in the control of upright standing. Torque feedback is thought to reduce the effort required to stand and play a functional role in slowly aligning the body with gravity. Our results provide experimental evidence of a torque feedback mechanism and offer new and valuable insights into the sensorimotor control of human balance.

Cortical potentials time-locked to discrete postural events during quiet standing are facilitated during postural threat exposure.

During unperturbed bipedal standing, postural control is governed primarily by subcortical and spinal networks. However, it is unclear if cortical networks begin to play a greater role when stability is threatened. This study investigated how initial and repeated exposure to a height-related postural threat modulates cortical potentials time-locked to discrete centre of pressure (COP) events during standing. Twenty-seven young adults completed a series of 90-s standing trials at LOW (0.8 m above the ground, away from edge) and HIGH (3.2 m above the ground, at edge) threat conditions. Three LOW trials were completed before and after 15 consecutive HIGH trials. Participants stood on a force plate while electroencephalographic (EEG) activity was recorded. To examine changes in cortical activity in response to discrete postural events, prominent forward and backward peaks in the anterior-posterior COP time series were identified. EEG data were waveform-averaged to these events and the amplitude of event-related cortical activity was calculated. At the LOW condition, event-related potentials (ERPs) were scarcely detectable. However, once individuals stood at the HIGH condition, clear ERPs were observed, with more prominent potentials being observed for forward (edge-directed), compared to backward, COP events. Since forward COP peaks accelerate the centre of mass away from the platform edge, these results suggest there is intermittent recruitment of cortical networks that may be involved in the detection and minimization of postural sway toward a perceived threat. This altered cortical engagement appears resistant to habituation and may contribute to threat-related balance changes that persist following repeated threat exposure. KEY POINTS: While standing balance control is regulated primarily by subcortical and spinal processes, it is unclear if cortical networks play a greater role when stability is threatened. This study examined how cortical potentials time-locked to prominent peaks in the anterior-posterior centre of pressure (COP) time series were modulated by exposure to a height-related postural threat. While cortical potentials recorded over the primary sensorimotor cortices were scarcely detectable under non-threatening conditions, clear cortical potentials were observed when individuals stood under conditions of height-related threat. Cortical potentials were larger in response to COP peaks directed toward, compared to away from, the platform edge, and showed limited habituation with repeated threat exposure. Since forward COP peaks accelerate the centre of mass away from the platform edge, these findings suggest that when balance is threatened, there is intermittent recruitment of cortical networks, which may minimize the likelihood of falling in the direction of a perceived threat.

Sex differences in motor unit behaviour: A review.

The lack of systematic investigations on sex-related differences in motor unit behaviour poses a challenge in understanding and optimizing health and performance in males and females. Limited investigations revealed that sex differences in motor unit behaviour might be present in human muscles. This review summarizes the current knowledge on sex differences in motor unit behaviour and potential factors that may contribute to these differences. We show significant under-representation of female participants in motor unit studies and a limited number of studies investigating sex differences in motor unit behaviour. We place the current insights within the context of methodological limitations and outline several recommendations and future directions to improve female representation in this research area. We conclude that there is an urgent need to gather more data in females and investigate sex differences in motor unit behaviour. The knowledge gained could be used to develop sex-specific approaches to improve neuromuscular performance and rehabilitation.

The effects of eccentric exercise-induced fatigue on position sense during goal-directed movement.

We investigated the impairment of position sense associated with muscle fatigue. In Experiment 1, participants performed learned eccentric extension (22°/s) movements of the elbow as the arm was pulled through the horizontal plane without vision of the arm. They opened their closed right hand when they judged it to be passing through a target. Dynamic position sense was assessed via accuracy of limb position to the target at the time of hand opening. Eccentric movements were performed against a flexion load [10% of flexion maximum voluntary contractions (MVCs)]. We investigated performance under conditions with and without biceps vibration, as well as before and after eccentric exercise. In Experiment 2, a motor was used to extend the participant's limb passively. We compared conditions with and without vibration of the lengthening but passive biceps, before and after exercise. In Experiment 1, vibration of the active biceps resulted in participants opening their hands earlier [mean, [Formula: see text] (95% confidence interval, CI) -5.52° (-7.40, -3.63)] compared with without vibration. Exercise reduced flexion MVCs by ∼44%, and participants undershot the target more [-5.51° (-9.31, -1.70)] in the post-exercise block during control trials. Exercise did not influence the persistence of the vibratory illusion. In Experiment 2, vibration resulted in greater undershooting [-2.99° (-3.99, -1.98)] compared with without vibration, before and after exercise. Although exercise reduced MVCs by ∼50%, the passive task showed no effects of exercise. We suggest that the central nervous system continues to rely on muscle spindles for limb position sense, even when they reside in a muscle exposed to fatiguing eccentric contractions.NEW & NOTEWORTHY Dynamic position errors were examined in an eccentric and a passive elbow extension proprioceptive-targeting task, before and after eccentric exercise, with and without muscle vibration. Participants actively undershot the target more when fatigued while fatigue did not exacerbate task accuracy during passive movement. Vibration caused undershoots regardless of fatigue state during active and passive movements. We propose that the central nervous system continues to rely on muscle spindles for kinesthesia, even when they reside in a fatigued muscle.

Facilitation and Habituation of Cortical and Subcortical Control of Standing Balance Following Repeated Exposure to a Height-related Postural Threat.

Threats to stability elicit context-specific changes in balance control; however, the underlying neural mechanisms are not fully understood. Previous work has speculated that a shift toward greater supraspinal control may contribute to threat-related balance changes. This study investigated how neural correlates of cortical and subcortical control of balance were affected by initial and repeated exposure to a height-related postural threat. Corticomuscular coherence (CMC) between EEG recorded over the sensorimotor cortex and EMG recorded from the soleus (SOL) provided an estimate of cortical control, while intermuscular coherence (IMC) between bilateral SOL provided estimates of both cortical and subcortical control. These outcomes, along with measures of psychological and arousal state and standing balance control, were examined in 28 healthy young adults during a series of 90-s quiet standing trials completed at LOW (0.8 m above ground; away from edge) and HIGH (3.2 m above ground, at edge) threat conditions. Initial exposure to threat significantly increased gamma-band CMC (31-40 Hz) and IMC at frequencies thought to be mediated by cortical (21-40 Hz) and subcortical (5-20 Hz) substrates. Following repeated threat exposure, only estimates of cortical control (gamma CMC and 21-40 Hz IMC) demonstrated significant habituation. Estimates of cortical control changed in parallel with high-frequency centre of pressure power (>0.5 Hz) and plantar-dorsiflexor coactivation, but not other threat-related balance changes which did not habituate. These results support the hypothesis that postural threat induces a shift toward more supraspinal control of balance, and suggests this altered neural control may contribute to specific threat-related balance changes.

The acute effects of periodic and noisy tendon vibration on wrist muscle stretch responses.

Mechanical muscle tendon vibration activates multiple sensory receptors in the muscle and tendon. In particular, tendon vibration tends to activate the Ia afferents the strongest, but also will activate group II and Ib afferents. This activation can cause three main effects in the central nervous system: proprioceptive illusions, tonic vibration reflexes, and suppression of the stretch response. Noisy tendon vibration has been used to assess the frequency characteristics of proprioceptive reflexes and, interestingly there appeared to be no evidence for proprioceptive illusions or tonic vibration reflexes during standing [9]. However, it remains unknown if noisy vibration induces a suppression of the muscle stretch response. Therefore, the purpose of this study was to investigate the effects of noisy and periodic tendon vibration on the stretch response in the flexor carpi radialis muscle (FCR). We examined FCR stretch responses with and without periodic (20 and 100 Hz) and noisy (∼10-100 Hz) tendon vibration. We additionally had participants perform the task under the instruction set to either not respond to the perturbation or to respond as fast as possible. The key finding from this study was that both periodic and noisy vibration resulted in a reduced stretch response amplitude. Additionally, it was found that a participant's intent to respond did not modulate the amount of suppression observed. The findings from this study provide a more detailed understanding of the effects of tendon vibration on the muscle stretch response.

Does height-induced threat modulate shortening of reaction times induced by a loud stimulus in a lateral stepping and a wrist extension task?

INTRODUCTION: The StartReact (SR) effect is the accelerated release of a prepared movement when a startling acoustic stimulus is presented at the time of the imperative stimulus (IS). SR paradigms have been used to study defective control of balance and gait in people with neurological conditions, but differences in emotional state (e.g. fear of failure) may be a potential confounder when comparing patients to healthy subjects. In this study, we aimed to gain insight in the effects of postural threat on the SR effect by manipulating surface height during a postural (lateral step) task and a non-postural (wrist extension) task. METHODS: Eleven healthy participants performed a lateral step perpendicular to the platform edge, and 19 participants performed a wrist extension task while standing at the platform edge. Participants initiated the movement as fast as possible in response to an IS that varied in intensity across trials (80 dB to 121 dB) at both low and high platform height (3.2 m). For the lateral step task, we determined anticipatory postural adjustments (APA) and step onset latencies. For the wrist extension task, muscle onset latencies were determined. We used Wilcoxon signed-rank tests on the relative onset latencies between both heights, to identify whether the effect of height was different for IS intensities between 103 and 118 dB compared to 121 dB. RESULTS: For both tasks, onset latencies were significantly shortened at 121 dB compared to 80 dB, regardless of height. In the lateral step task, the effect of height was larger at 112 dB compared to 121 dB. The absolute onset latencies showed that at 112 dB there was no such stimulus intensity effect at high as seen at low surface height. In the wrist extension task, no differential effects of height could be demonstrated across IS intensities. CONCLUSIONS: Postural threat had a significant, yet modest effect on shortening of RTs induced by a loud IS, with a mere 3 dB difference between standing on high versus low surface height. Interestingly, this effect of height was specific to the postural (i.e. lateral stepping) task, as no such differences could be demonstrated in the wrist extension task. This presumably reflects more cautious execution of the lateral step task when standing on height. The present findings suggest that applying stimuli of sufficiently high intensity (≥115 dB) appears to neutralize potential differences in emotional state when studying SR effects.

Learning to stand with unexpected sensorimotor delays.

Human standing balance relies on self-motion estimates that are used by the nervous system to detect unexpected movements and enable corrective responses and adaptations in control. These estimates must accommodate for inherent delays in sensory and motor pathways. Here, we used a robotic system to simulate human standing about the ankles in the anteroposterior direction and impose sensorimotor delays into the control of balance. Imposed delays destabilized standing, but through training, participants adapted and re-learned to balance with the delays. Before training, imposed delays attenuated vestibular contributions to balance and triggered perceptions of unexpected standing motion, suggesting increased uncertainty in the internal self-motion estimates. After training, vestibular contributions partially returned to baseline levels and larger delays were needed to evoke perceptions of unexpected standing motion. Through learning, the nervous system accommodates balance sensorimotor delays by causally linking whole-body sensory feedback (initially interpreted as imposed motion) to self-generated balance motor commands.

When standing, neurons in the brain send signals to skeletal muscles so we can adjust our movements to stay upright based on the requirements from the surrounding environment. The long nerves needed to connect our brain, muscles and sensors lead to considerable time delays (up to 160 milliseconds) between sensing the environment and the generation of balance-correcting motor signals. Such delays must be accounted for by the brain so it can adjust how it regulates balance and compensates for unexpected movements. Aging and neurological disorders can lead to lengthened neural delays, which may result in poorer balance. Computer modeling suggests that we cannot maintain upright balance if delays are longer than 300-340 milliseconds. Directly assessing the destabilizing effects of increased delays in human volunteers can reveal how capable the brain is at adapting to this neurological change. Using a custom-designed robotic balance simulator, Rasman et al. tested whether healthy volunteers could learn to balance with delays longer than the predicted 300-340 millisecond limit. In a series of experiments, 46 healthy participants stood on the balance simulator which recreates the physical sensations and neural signals for balancing upright based on a computer-driven virtual reality. This unique device enabled Rasman et al. to artificially impose delays by increasing the time between the generation of motor signals and resulting whole-body motion. The experiments showed that lengthening the delay between motor signals and whole-body motion destabilized upright standing, decreased sensory contributions to balance and led to perceptions of unexpected movements. Over five days of training on the robotic balance simulator, participants regained their ability to balance, which was accompanied by recovered sensory contributions and perceptions of expected standing, despite the imposed delays. When a subset of participants was tested three months later, they were still able to compensate for the increased delay. The experiments show that the human brain can learn to overcome delays up to 560 milliseconds in the control of balance. This discovery may have important implications for people who develop balance problems because of older age or neurologic diseases like multiple sclerosis. It is possible that robot-assisted training therapies, like the one in this study, could help people overcome their balance impairments.

Brain connectivity during simulated balance in older adults with and without Parkinson's disease.

Individuals with Parkinson's disease often experience postural instability, a debilitating and largely treatment-resistant symptom. A better understanding of the neural substrates contributing to postural instability could lead to more effective treatments. Constraints of current functional neuroimaging techniques, such as the horizontal orientation of most MRI scanners (forcing participants to lie supine), complicates investigating cortical and subcortical activation patterns and connectivity networks involved in healthy and parkinsonian balance control. In this cross-sectional study, we utilized a newly-validated MRI-compatible balance simulator (based on an inverted pendulum) that enabled participants to perform balance-relevant tasks while supine in the scanner. We utilized functional MRI to explore effective connectivity underlying static and dynamic balance control in healthy older adults (n = 17) and individuals with Parkinson's disease while on medication (n = 17). Participants performed four tasks within the scanner with eyes closed: resting, proprioceptive tracking of passive ankle movement, static balancing of the simulator, and dynamic responses to random perturbations of the simulator. All analyses were done in the participant's native space without spatial transformation to a common template. Effective connectivity between 57 regions of interest was computed using a Bayesian Network learning approach with false discovery rate set to 5%. The first 12 principal components of the connection weights, binomial logistic regression, and cross-validation were used to create 4 separate models: contrasting static balancing vs {rest, proprioception} and dynamic balancing vs {rest, proprioception} for both controls and individuals with Parkinson's disease. In order to directly compare relevant connections between controls and individuals with Parkinson's disease, we used connections relevant for predicting a task in either controls or individuals with Parkinson's disease in logistic regression with Least Absolute Shrinkage and Selection Operator regularization. During dynamic balancing, we observed decreased connectivity between different motor areas and increased connectivity from the brainstem to several cortical and subcortical areas in controls, while individuals with Parkinson's disease showed increased connectivity associated with motor and parietal areas, and decreased connectivity from brainstem to other subcortical areas. No significant models were found for static balancing in either group. Our results support the notion that dynamic balance control in individuals with Parkinson's disease relies more on cortical motor areas compared to healthy older adults, who show a preference of subcortical control during dynamic balancing.

Soleus responses to Achilles tendon stimuli are suppressed by heel and enhanced by metatarsal cutaneous stimuli during standing.

KEY POINTS: We examined the influence of cutaneous feedback from the heel and metatarsal regions of the foot sole on the soleus stretch reflex pathway during standing. We found that heel electrical stimuli suppressed and metatarsal stimuli enhanced the soleus vibration response. Follow-up experiments indicated that the interaction between foot sole cutaneous feedback and the soleus vibration response was likely not mediated by presynaptic inhibition and was contingent upon a modulation at the ⍺-motoneuron pool level. The spatially organized interaction between cutaneous feedback from the foot sole and the soleus vibration response provides information about how somatosensory information is combined to appropriately respond to perturbations during standing. ABSTRACT: Cutaneous feedback from the foot sole provides balance-relevant information and has the potential to interact with spinal reflex pathways. In this study, we examined how cutaneous feedback from the foot sole (heel and metatarsals) influenced the soleus response to proprioceptive stimuli during standing. We delivered noisy vibration (10-115 Hz) to the right Achilles tendon while we intermittently applied electrical pulse trains (five 1-ms pulses at 200 Hz, every 0.8-1.0 s) to the skin under either the heel or the metatarsals of the ipsilateral foot sole. We analysed time-dependent (referenced to cutaneous stimuli) coherence and cross-correlations between the vibration acceleration and rectified soleus EMG. Vibration-EMG coherence was observed across a bandwidth of ∼10-80 Hz, and coherence was suppressed by heel but enhanced by metatarsal cutaneous stimuli. Cross-correlations showed soleus EMG was correlated with the vibration (∼40 ms lag) and cross-correlations were also suppressed by heel (from 104-155 ms) but enhanced by metatarsal (from 76-128 ms) stimuli. To examine the neural mechanisms mediating this reflex interaction, we conducted two further experiments to probe potential contributions from (1) presynaptic inhibition, and (2) modulations at the ⍺- and γ-motoneuron pools. Results suggest the cutaneous interactions with the stretch reflex pathway required a modulation at the ⍺-motoneuron pool and were likely not mediated by presynaptic inhibition. These findings demonstrate that foot sole cutaneous information functionally tunes the stretch reflex pathway during the control of upright posture and balance.

Sex differences in the modulation of the motor unit discharge rate leads to reduced force steadiness.

The purpose of this study was to evaluate the relationship between the variability in the motor unit inter-pulse interval and force steadiness at submaximal and maximal force outputs between the sexes. Twenty-four male and 24 female participants were recruited to perform isometric dorsiflexion contractions at 20, 40, 60, 80, and 100% maximum voluntary contraction. Tibialis anterior myoelectric signal was recorded by an intramuscular electrode. Females had lower force steadiness (coefficient of variation of force (CoV-Force), 27.3%, p < 0.01) and a greater coefficient of variation of motor unit action potential inter-pulse interval (CoV-IPI), compared with males (9.6%, p < 0.01). There was no significant correlation between the normalized CoV-IPI and CoV-Force (r = 0.19, p > 0.01), but there was a significant repeated measures correlation between the raw scores for root-mean-square force error and the standard deviation of motor unit discharge rate (r = 0.65, p < 0.01). Females also had a greater incidence of doublet discharges on average across force levels (p < 0.01). The sex differences may result from motor unit behaviours (i.e., doublet and rapid discharges, synchronization, rate coding or recruitment), leading to lower force steadiness and greater CoV-IPI in females. Novelty: Sex differences in force steadiness may be due to neural strategies. Females have lower force steadiness compared with males. Greater incidence of doublet discharges in females may result in lesser force steadiness.

Is the 'reverse onion skin' phenomenon more prevalent than we thought during intramuscular myoelectric recordings from low to maximal force outputs?

There are isolated instances in the literature that suggest the 'onion skin' phenomenon is not always present. That is, newly recruited high threshold motor units (MU) have higher discharge rates than previously recruited low threshold MUs. Therefore, the purpose of this paper was to investigate the presence of the 'onion skin' phenomenon in a large sample of intramuscular myoelectric recordings from low to maximal force outputs. Forty-eight participants performed rapid isometric dorsiflexion contractions at 20, 40, 60, 80 and 100 % MVC while intramuscular electrical activity was recorded. A bivariate frequency-distribution of the motor unit discharge rate and motor unit action potential peak-to-peak (P-P) amplitude was assessed. There was a significant difference in bivariate frequency-distribution across force levels (D's = 0.1083-0.3094, p's < 0.001). Newly recruited high threshold MUs did have lower discharge rates, but there was an increase in the presence of high threshold, large P-P amplitude MUs with higher discharge rates than lower threshold MUs (reverse onion skin) during the stable portion of the force output. The recruitment of high threshold MUs with higher discharge rates decreased the level of common drive from the cross-correlation (Rxy) = 0.79 at 20 % MVC to Rxy = 0.68 at 100 % MVC (p < 0.01), but it remained high. As the interference pattern becomes more complex with the recruitment of more motor units at higher force outputs, intramuscular electrodes may be more discriminating while recording motor unit activity leading to the identification of both the 'reverse onion skin' and 'onion skin' phenomenon being present.

Influence of age on the frequency characteristics of the soleus muscle response to Achilles tendon vibration during standing.

KEY POINTS: Proprioceptive sensory information from the ankle joint is critical for the control of upright posture and balance. We examined the influence of age (n = 54 healthy adults, 20-82 years old) on lower limb muscle responses to proprioceptive perturbations evoked by Achilles tendon vibration during standing. The frequency bandwidth of the muscle response became narrower, and the gain (the muscle response relative to the stimulus) and scaling (increases in response amplitude with increases in stimulus amplitude) decreased with age. Mechanics of the muscle-tendon unit (mechanical admittance) did not differ with age during standing, and thus probably did not mediate the age-related changes observed in soleus muscle responses to vibration. These findings add to our understanding of how altered proprioceptive responses may contribute to impaired mobility and falls with ageing. ABSTRACT: Proprioceptive information from the ankle joint plays an important role in the control of upright posture and balance. Ageing influences many components of the sensorimotor system, which leads to poor mobility and falls. However, little is known about the influence of age on the characteristics of short latency muscle responses to proprioceptive stimuli during standing across frequencies that are encoded by muscle spindles. We examined the frequency characteristics of the soleus muscle response to noisy (10-115 Hz) Achilles tendon vibration during standing in 54 healthy adults across a broad age range (20-82 years). The results showed the frequency bandwidth of the soleus response (vibration-electromyography coherence) became progressively narrower with ageing. Coherence was significantly lower in middle-aged relative to young adults between ∼7-11 and 28-62 Hz, lower in older relative to middle-aged adults between ∼30-50 Hz and lower in older relative to young adults between ∼7-64 Hz. Muscle response gain was similar between age groups at low frequencies, although gain was lower in older relative to young adults between ∼28-54 Hz. Across the age range, the response amplitude (peak-to-peak cross-covariance) and the scaling of the response with stimulus amplitude were both negatively correlated with age. Muscle-tendon mechanics (admittance) did not differ with age, suggesting this did not mediate differences in soleus responses. Our findings suggest there is a progressive change in the soleus response to proprioceptive stimuli with ageing during standing, which could contribute to poorer mobility and falls.

Lower-limb muscle responses evoked with noisy vibrotactile foot sole stimulation.

AIM: Cutaneous feedback from the foot sole contributes to the control of standing balance in two ways: it provides perceptual awareness of tactile perturbations at the interface with the ground (e.g., shifts in the pressure distribution, slips, etc.) and it reflexively activates lower-motor neurons to trigger stabilizing postural responses. Here we focus on the latter, cutaneous (or cutaneomotor) reflex coupling in the lower limb. These reflexes have been studied most-frequently with electrical pulse trains that bypass natural cutaneous mechanotransduction, stimulating cutaneous afferents in a largely non-physiological manner. Harnessing the mechanical filtering properties of cutaneous afferents, we take a novel mechanical approach by applying supra-threshold continuous noisy vibrotactile stimulation (NVS) to the medial forefoot. METHODS: Using NVS, we characterized the time and frequency domain properties of cutaneomotor reflexes in the Tibialis Anterior. We additionally measured stimulus-triggered average muscle responses to repeated discrete sinusoidal pulses for comparison. To investigate cutaneomotor reflex gain scaling, stimuli were delivered at 3- or 10-times perceptual threshold (PT), while participants held 12.5% or 25% of maximum voluntary contraction (MVC). RESULTS: Peak responses in the time domain were observed at lags reflecting transmission delay through a polysynaptic reflex pathway (~90-100 ms). Increasing the stimulus amplitude enhanced cutaneomotor coupling, likely by increasing afferent firing rates. Although greater background muscle contraction increased the overall amplitude of the evoked responses, it did not increase the proportion of the muscle response attributable to cutaneous input. CONCLUSION: Taken together, our findings support the use of NVS as a novel tool for probing the physiological properties of cutaneomotor reflex pathways.

Frequency characteristics of heteronymous responses evoked by Achilles tendon vibration during quiet stance.

Primary (Ia) sensory afferents that innervate muscle spindles provide strong synaptic input to homonymous motoneurons and are thought to play a role in balance control. In addition, Ia afferents have broad heteronymous connections; i.e., projections to motoneurons that innervate other muscles that act at the same joint as well as at different joints. The purpose of the current study was to investigate heteronymous Ia afferent connections from the triceps surae muscles to lower limb and back muscles during quiet standing in humans. We applied supra-threshold noisy vibration (10-115 Hz) to the right Achilles tendon of 12 participants maintaining quiet stance and recorded EMG activity bilaterally from homonymous (Soleus) and heteronymous muscles (Semitendinosus, Vastus Lateralis, Erector Spinae). We estimated coherence, phase, and gain between the tendon probe acceleration and rectified EMG from each muscle. We found significant coherence between the probe acceleration and EMG in ipsilateral Soleus (5-100 Hz), Semitendinosus (10-75 Hz), Vastus Lateralis (5-70 Hz), and bilateral Erector Spinae muscles (10-70 Hz). These results provide evidence that triceps surae muscle spindle afferents can influence the activity of muscles proximal to the ankle joint across a broad frequency band during quiet standing.

Sex differences in motor unit discharge rates at maximal and submaximal levels of force output.

This study evaluated potential sex differences in motor unit (MU) behaviour at maximal and submaximal force outputs. Forty-eight participants, 24 females and 24 males, performed isometric dorsiflexion contractions at 20%, 40%, 60%, 80%, and 100% of a maximum voluntary contraction (MVC). Tibialis anterior electromyography was recorded both by surface and intramuscular electrodes. Compared with males, females had a greater MU discharge rate (MUDR) averaged across all submaximal intensities (Δ 0.45 pps, 2.56%). Males exhibited greater increases in MUDR above 40% MVC, surpassing females at 100% MVC (p's < 0.01). Averaged across all force outputs, females had a greater incidence of doublet and rapid discharges and a greater percentage of MU trains with doublet and rapid (5-10 ms) discharges (Δ 75.55% and 61.48%, respectively; p's < 0.01). A subset of males (n = 8) and females (n = 8), matched for maximum force output, revealed that females had even greater MUDR (Δ 1.38 pps, 7.47%) and percentage of MU trains with doublet and rapid discharges (Δ 51.62%, 56.68%, respectively; p's < 0.01) compared with males at each force output, including 100% MVC. Analysis of the subset of strength-matched males and females suggest that sex differences in MU behaviour may be a result of females needing to generate greater neural drive to achieve fused tetanus. Novelty Females had higher MUDRs and greater percentage of MU trains with doublets across submaximal force outputs (20%-80% MVC). Differences were even greater for a strength matched subset. Differences in motor unit behaviour may arise from musculoskeletal differences, requiring greater neural drive in females.