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.

Calf cutaneous stimulation generates reflexes in the thigh that can be modified by subthreshold noisy vibration.

Imperceptible tactile noise applied to the skin of the feet enhances posture-correcting cutaneous reflexes. This sensory augmentation technique, stochastic resonance (SR), has not been tested in the less-sensitive hairy skin of the leg for its reflex-enhancement ability. The objectives of this study were to determine whether calf skin stimulation produces cutaneous reflexes and whether noise can modify the reflex. In 20 participants, electrotactile pulse trains were applied at the calf while participants performed submaximal isometric knee extension. To test SR, five different levels of vibrotactile noise were applied simultaneously to the test input. Muscle activity from the vastus lateralis (VL) was analyzed 60-110 ms after stimulation. Reflex ratios were calculated by dividing the reflex peak activity by the prestimulation background muscle activity. A significant reflex response was evoked in 16/20 participants (5.41 ± 2.6% of background muscle activity); these responses varied between individuals with eight being facilitatory and eight being inhibitory. In half of the participants, a new reflex appeared at some level of added noise (n = 10). The average reflex ratio of the study population was significantly higher at the "optimal" noise level (8.61 ± 4.5) than at "baseline" (4.70 ± 5.6) (P = 0.002); the optimal level varied across participants. These results suggest that cutaneous reflexes exist at the VL in response to calf skin stimulation and that SR can change cutaneous reflexes at the leg. This study provides an important first step toward SR application in clinical populations with sensory loss such as individuals with lower extremity amputation.NEW & NOTEWORTHY Our work showed that cutaneous reflexes, known to be present in response to foot sole stimulation, can also be evoked by stimulation of hairy leg skin. In addition, we demonstrated that adding tactile noise can enhance this reflex response. These findings demonstrate proof-of-concept for potential future applications where tactile stimulation, applied to the leg of an individual with amputation, can enhance postural-relevant reflexes. Improving postural control may reduce the risk of falls in this high-risk population.

Visual feedback-dependent modulation of arousal, postural control, and muscle stretch reflexes assessed in real and virtual environments.

Introduction: The mechanisms regulating neuromuscular control of standing balance can be influenced by visual sensory feedback and arousal. Virtual reality (VR) is a cutting-edge tool for probing the neural control of balance and its dependence on visual feedback, but whether VR induces neuromodulation akin to that seen in real environments (eyes open vs. closed or ground level vs. height platform) remains unclear. Methods: Here we monitored 20 healthy young adults (mean age 23.3 ± 3.2 years; 10 females) during four conditions of quiet standing. Two real world conditions (eyes open and eyes closed; REO and REC) preceded two eyes-open virtual 'low' (ground level; VRL) and 'high' (14 m height platform; VRH) conditions. We measured arousal via electrodermal activity and psychosocial questionnaires rating perceived fear and anxiety. We recorded surface electromyography over the right soleus, medial gastrocnemius, and tibialis anterior, and performed force plate posturography. As a proxy for modulations in neural control, we assessed lower limb reflexive muscle responses evoked by tendon vibration and electrical stimulation. Results: Physiological and perceptual indicators of fear and anxiety increased in the VRH condition. Background soleus muscle activation was not different across conditions; however, significant increases in muscle activity were observed for medial gastrocnemius and tibialis anterior in VRH relative to REO. The mean power frequency of postural sway also increased in the VRH condition relative to REO. Finally, with a fixed stimulus level across conditions, mechanically evoked reflexes remained constant, while H-reflex amplitudes decreased in strength within virtual reality. Discussion: Notably, H-reflexes were lower in the VRL condition than REO, suggesting that these ostensibly similar visual environments produce different states of reflexive balance control. In summary, we provide novel evidence that VR can be used to modulate upright postural control, but caution that standing balance in analogous real and virtual environments may involve different neural control states.

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.

Unperceived motor actions of the balance system interfere with the causal attribution of self-motion.

The instability of human bipedalism demands that the brain accurately senses balancing self-motion and determines whether movements originate from self-generated actions or external disturbances. Here, we challenge the longstanding notion that this process relies on a single representation of the body and world to accurately perceive postural orientation and organize motor responses to control balance self-motion. Instead, we find that the conscious sense of balance can be distorted by the corrective control of upright standing. Using psychophysics, we quantified thresholds to imposed perturbations and balance responses evoking cues of self-motion that are (in)distinguishable from corrective balance actions. When standing immobile, participants clearly perceived imposed perturbations. Conversely, when freely balancing, participants often misattributed their own corrective responses as imposed motion because their balance system had detected, integrated, and responded to the perturbation in the absence of conscious perception. Importantly, this only occurred for perturbations encoded ambiguously with balance-correcting responses and that remained below the natural variability of ongoing balancing oscillations. These findings reveal that our balance system operates on its own sensorimotor principles that can interfere with causal attribution of our actions, and that our conscious sense of balance depends critically on the source and statistics of induced and self-generated motion cues.

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.

Rapid Feedback Responses Parallel the Urgency of Voluntary Reaching Movements.

Optimal feedback control is a prominent theory used to interpret human motor behaviour. The theory posits that skilled actions emerge from control policies that link voluntary motor control (feedforward) with flexible feedback corrections (feedback control). It is clear the nervous system can generate flexible motor corrections (reflexes) when performing actions with different goals. We know little, however, about shared features of voluntary actions and feedback control in human movement. Here we reveal a link between the timing demands of voluntary actions and flexible responses to mechanical perturbations. In two experiments, 40 human participants (21 females) made reaching movements with different timing demands. We disturbed the arm with mechanical perturbations at movement onset (Experiment 1) and at locations ranging from movement onset to completion (Experiment 2). We used the resulting muscle responses and limb displacements as a proxy for the control policies that support voluntary reaching movements. We observed an increase in the sensitivity of elbow and shoulder muscle responses and a reduction in limb motion when the task imposed greater urgency to respond to the same perturbations. The results reveal a relationship between voluntary actions and feedback control as the limb was displaced less when moving faster in perturbation trials. Muscle responses scaled with changes in the displacement of the limb in perturbation trials within each timing condition. Across both experiments, human behaviour was captured by simulations based on stochastic optimal feedback control. Taken together, the results highlight flexible control that links sensory processing with features of human reaching movements.

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.

Altered Vestibular Balance Function in Combat Sport Athletes.

Combat sports pose a risk for accumulative injuries to the nervous system, yet fighters have remained an understudied population. Here, our purpose was to determine whether repetitive blows to the head have an effect on vestibular balance reflexes in combat sports athletes. We compared lower-limb muscle responses evoked with electrical vestibular stimuluation (EVS) between fighters (boxing/muay thai) and non-fighter controls. Each participant received stochastic vestibular stimulation (0-25 Hz, ±3 mA) over their mastoid processes while they stood relaxed with their head to the left or right. Surface electromyography was recorded from the medial gastrocnemius and soleus muscles bilaterally. Short and medium latency response (SLR/MLR) peaks were significantly delayed in the fighter group compared to controls. SLR and MLR peak amplitudes were also significantly lower in fighters. Fighter-estimated cumulative repetitive head impact (RHI) events demonstrated strong positive correlations with the timing of SLR and MLR peaks. Cumulative RHI events also negatively correlated with peak MLR amplitude and response gain at frequencies above 5 Hz. Our results provide evidence of a progressive vestibular impairment in combat sports athletes, potentially resulting from blows to the head accumulated in sparring practice and competitive bouts throughout their careers. Taken together, EVS-based vestibular assessments may provide a valuable clinical diagnostic tool and help better inform "return-to-play" and career-length decisions for not only combat sports athletes, but potentially other populations at risk of RHIs.

Remote Subthreshold Stimulation Enhances Skin Sensitivity in the Lower Extremity.

Foot sole skin interfaces with the ground and contributes to successful balance. In situations with reduced sensitivity in the glabrous foot skin, stochastic resonance (SR) improves skin sensitivity by adding tactile noise. Some situations, however, involve an interface comprised of hairy skin, which has higher thresholds for sensitivity. For example, in lower extremity amputation the residual limb is comprised of hairy leg skin. The main objective of this study was to determine if SR improves skin sensitivity in hairy skin, and whether a specific intensity of noise is most effective. Secondary objectives were to compare the effect between locations, ages and modalities. In 60 healthy participants a vibrotactile (test) input was delivered at the lower extremity concurrently with a second, noisy stimulus applied more proximally. The presence of a remote SR effect was tested in 15 young participants using electrotactile noise at the calf. Secondary objectives were tested in separate groups of 15 subjects and differed by substituting for one of the three variables: vibrotactile noise, heel site, and with older participants. A forced-choice protocol was used to determine detection ability of the subthreshold vibration test input with varying noise levels applied simultaneously (0, 20, 40, 60, 80, and 100% of perceptual threshold). An SR effect was identified when increased detection of the input was obtained at any level of noise versus no noise. It was found that all four test groups demonstrated evidence of SR: 33-47% of individuals showed better detection of the input with added noise. The SR effect did not appear consistently at any specific noise level for any of the groups, and none of the variables showed a superior ability to evoke SR. Interestingly, in approximately 33% of cases, threshold values fluctuated throughout testing. While this work has provided evidence that SR can enhance the perception of a vibrotactile input in hairy skin, these data suggest that the ability to repeatably show an SR effect relies on maintaining a consistent threshold.

Physiological Vibration Acceleration (Phybrata) Sensor Assessment of Multi-System Physiological Impairments and Sensory Reweighting Following Concussion.

OBJECTIVE: To assess the utility of a head-mounted wearable inertial motion unit (IMU)-based physiological vibration acceleration ("phybrata") sensor to support the clinical diagnosis of concussion, classify and quantify specific concussion-induced physiological system impairments and sensory reweighting, and track individual patient recovery trajectories. METHODS: Data were analyzed from 175 patients over a 12-month period at three clinical sites. Comprehensive clinical concussion assessments were first completed for all patients, followed by testing with the phybrata sensor. Phybrata time series data and spatial scatter plots, eyes open (Eo) and eyes closed (Ec) phybrata powers, average power (Eo+Ec)/2, Ec/Eo phybrata power ratio, time-resolved phybrata spectral density (TRPSD) distributions, and receiver operating characteristic (ROC) curves are compared for individuals with no objective impairments and those clinically diagnosed with concussions and accompanying vestibular impairment, other neurological impairment, or both vestibular and neurological impairments. Finally, pre- and post-injury phybrata case report results are presented for a participant who was diagnosed with a concussion and subsequently monitored during treatment, rehabilitation, and return-to-activity clearance. RESULTS: Phybrata data demonstrate distinct features and patterns for individuals with no discernable clinical impairments, diagnosed vestibular pathology, and diagnosed neurological pathology. ROC curves indicate that the average power (Eo+Ec)/2 may be utilized to support clinical diagnosis of concussion, while Eo and Ec/Eo may be utilized as independent measures to confirm accompanying neurological and vestibular impairments, respectively. All 3 measures demonstrate area under the curve (AUC), sensitivity, and specificity above 90% for their respective diagnoses. Phybrata spectral analyses demonstrate utility for quantifying the severity of concussion-induced physiological impairments, sensory reweighting, and subsequent monitoring of improvements throughout treatment and rehabilitation. CONCLUSION: Phybrata testing assists with objective concussion diagnosis and provides an important adjunct to standard concussion assessment tools by objectively ascertaining neurological and vestibular impairments, guiding targeted rehabilitation strategies, monitoring recovery, and assisting with return-to-sport/work/learn decision-making.

Subthreshold Electrical Noise Applied to the Plantar Foot Enhances Lower-Limb Cutaneous Reflex Generation.

Reflex responses generated by cutaneous mechanoreceptors of the plantar foot are important for the maintenance of balance during postural tasks and gait. With aging, reflex generation, particularly from fast adapting type I receptors, is reduced, which likely contributes to impaired postural stability in this population. Therefore, improving reflex generation from these receptors may serve as a tool to improve balance performance. A mechanism to enhance reflexes may lie in the phenomenon of stochastic resonance, whereby the addition of certain intensities and frequencies of noise stimuli improves the performance of a system. This study was conducted to determine whether tactile noise stimuli could improve cutaneous reflex generation. In 12 healthy young adults, we evoked cutaneous reflex responses using a 0-50 Hz Gaussian noise vibration applied to the plantar heel. Concurrently, we applied one of six subthreshold intensities of electrical tactile noise to the plantar heel [0%, 20%, 40%, 60%, 80% or 100% (threshold)] and were able to analyze data from 0%, 20% and 40% trials. Across participants, it was found that the addition of a 20% perceptual threshold (PT) noise resulted in enhanced reflex responses when analyzed in both the time and frequency domains. These data provide evidence that cutaneous reflex generation can be enhanced via a stochastic resonance effect and that 20% PT is the optimal intensity of noise to do so. Therefore, the addition of noise stimuli may be a valuable clinical intervention to improve reflex responses associated with postural balance in populations with impairments.

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.

Soleus single motor units show stronger coherence with Achilles tendon vibration across a broad bandwidth relative to medial gastrocnemius units while standing.

To probe the frequency characteristics of somatosensory responses in the triceps surae muscles, we previously applied suprathreshold noisy vibration to the Achilles tendon and correlated it with ongoing triceps surae muscle activity (recorded via surface EMG) during standing. Stronger responses to tendon stimuli were observed in soleus (Sol) relative to medial gastrocnemius (MGas) surface EMG; however, it is unknown whether differences in motor unit activity or limitations of surface EMG could have influenced this finding. Here, we inserted indwelling EMG into Sol and MGas to record the activity of single motor units while we applied noisy vibration (10-115 Hz) to the right Achilles tendon of standing participants. We analyzed the relationship between vibration acceleration and the spike activity of active single motor units through estimates of coherence, gain, phase, and cross-covariance. We also applied sinusoidal vibration at frequencies from 10 to 100 Hz (in 5-Hz increments) to examine whether motor units demonstrate nonlinear synchronization or phase locking at higher frequencies. Relative to MGas single motor units, Sol units demonstrated stronger coherence and higher gain with noisy vibration across a bandwidth of 7-68 Hz, and larger peak-to-peak cross-covariance at all four stimulus amplitudes examined. Sol and MGas motor unit activity was modulated over the time course of the sinusoidal stimuli across all frequencies, but their phase-locking behavior was minimal. These findings suggest Sol plays a prominent role in responding to disturbances transmitted through the Achilles tendon across a broad frequency band during standing.NEW & NOTEWORTHY We examined the relationship between Achilles tendon stimuli and spike times of single soleus (Sol) and medial gastrocnemius (MGas) motor units during standing. Relative to MGas, Sol units demonstrated stronger coherence and higher gain with noisy stimuli across a bandwidth of 7-68 Hz. Sol and MGas units demonstrated minimal nonlinear phase locking with sinusoidal stimuli. These findings indicate Sol plays a prominent role in responding to tendon stimuli across a broad frequency band.

Cutaneous afferent innervation of the human foot sole: what can we learn from single-unit recordings?

Cutaneous afferents convey exteroceptive information about the interaction of the body with the environment and proprioceptive information about body position and orientation. Four classes of low-threshold mechanoreceptor afferents innervate the foot sole and transmit feedback that facilitates the conscious and reflexive control of standing balance. Experimental manipulation of cutaneous feedback has been shown to alter the control of gait and standing balance. This has led to a growing interest in the design of intervention strategies that enhance cutaneous feedback and improve postural control. The advent of single-unit microneurography has allowed the firing and receptive field characteristics of foot sole cutaneous afferents to be investigated. In this review, we consolidate the available cutaneous afferent microneurographic recordings from the foot sole and provide an analysis of the firing threshold, and receptive field distribution and density of these cutaneous afferents. This work enhances the understanding of the foot sole as a sensory structure and provides a foundation for the continued development of sensory augmentation insoles and other tactile enhancement interventions.

Precise coding of ankle angle and velocity by human calf muscle spindles.

Human standing balance control requires the integration of sensory feedback to produce anticipatory, stabilizing ankle torques. However, the ability of human triceps surae muscle spindles to provide reliable sensory feedback regarding the small, slow ankle movements that occur during upright standing has recently come under question. We performed microneurography to directly record axon potentials from single muscle spindle afferents in the human triceps surae during servo-controlled movement of the ankle joint. To simulate movements of the ankle while standing, we delivered random 90-s dorsiflexion/plantar flexion oscillations of the ankle joint, with a peak-to-peak amplitude of 0.7° and frequency content below 0.5Hz. In roughly half of the trials (46%), participants held a low-level, near-isometric contraction of the triceps surae muscles. We demonstrate that afferent activity in a population of muscle spindles closely reflects ankle movements at frequencies and amplitudes characteristic of human standing. Four out of five soleus spindles, and three out of seven gastrocnemius spindles coded for at least a single frequency component of anteroposterior ankle rotation. Concatenating within muscles, coherence was significantly greater for soleus spindles at all stimulus frequencies. Voluntary contraction of the parent muscle reduced spindle sensitivity, but only significantly near the mean power frequency of the stimulus (∼0.3Hz). In conclusion, these results provide direct evidence that triceps surae muscle spindles are potentially capable of providing important sensory feedback for the control of human standing balance.

Frequency characteristics of human muscle and cortical responses evoked by noisy Achilles tendon vibration.

Noisy stimuli, along with linear systems analysis, have proven to be effective for mapping functional neural connections. We explored the use of noisy (10-115 Hz) Achilles tendon vibration to examine somatosensory reflexes in the triceps surae muscles in standing healthy young adults (n = 8). We also examined the association between noisy vibration and electrical activity recorded over the sensorimotor cortex using electroencephalography. We applied 2 min of vibration and recorded ongoing muscle activity of the soleus and gastrocnemii using surface electromyography (EMG). Vibration amplitude was varied to characterize reflex scaling and to examine how different stimulus levels affected postural sway. Muscle activity from the soleus and gastrocnemii was significantly correlated with the tendon vibration across a broad frequency range (~10-80 Hz), with a peak located at ~40 Hz. Vibration-EMG coherence positively scaled with stimulus amplitude in all three muscles, with soleus displaying the strongest coupling and steepest scaling. EMG responses lagged the vibration by ~38 ms, a delay that paralleled observed response latencies to tendon taps. Vibration-evoked cortical oscillations were observed at frequencies ~40-70 Hz (peak ~54 Hz) in most subjects, a finding in line with previous reports of sensory-evoked γ-band oscillations. Further examination of the method revealed 1) accurate reflex estimates could be obtained with <60 s of low-level (root mean square = 10 m/s2) vibration; 2) responses did not habituate over 2 min of exposure; and importantly, 3) noisy vibration had a minimal influence on standing balance. Our findings suggest noisy tendon vibration is an effective novel approach to characterize somatosensory reflexes during standing.NEW & NOTEWORTHY We applied noisy (10-115 Hz) vibration to the Achilles tendon to examine the frequency characteristics of lower limb somatosensory reflexes during standing. Ongoing muscle activity was coherent with the noisy vibration (peak coherence ~40 Hz), and coherence positively scaled with increases in stimulus amplitude. Our findings suggest that noisy tendon vibration, along with linear systems analysis, is an effective novel approach to study somatosensory reflex actions in active muscles.

Losing touch: age-related changes in plantar skin sensitivity, lower limb cutaneous reflex strength, and postural stability in older adults.

Age-related changes in the density, morphology, and physiology of plantar cutaneous receptors negatively impact the quality and quantity of balance-relevant information arising from the foot soles. Plantar perceptual sensitivity declines with age and may predict postural instability; however, alteration in lower limb cutaneous reflex strength may also explain greater instability in older adults and has yet to be investigated. We replicated the age-related decline in sensitivity by assessing monofilament and vibrotactile (30 and 250 Hz) detection thresholds near the first metatarsal head bilaterally in healthy young and older adults. We additionally applied continuous 30- and 250-Hz vibration to drive mechanically evoked reflex responses in the tibialis anterior muscle, measured via surface electromyography. To investigate potential relationships between plantar sensitivity, cutaneous reflex strength, and postural stability, we performed posturography in subjects during quiet standing without vision. Anteroposterior and mediolateral postural stability decreased with age, and increases in postural sway amplitude and frequency were significantly correlated with increases in plantar detection thresholds. With 30-Hz vibration, cutaneous reflexes were observed in 95% of young adults but in only 53% of older adults, and reflex gain, coherence, and cumulant density at 30 Hz were lower in older adults. Reflexes were not observed with 250-Hz vibration, suggesting this high-frequency cutaneous input is filtered out by motoneurons innervating tibialis anterior. Our findings have important implications for assessing the risk of balance impairment in older adults.

Plantar cutaneous function in Parkinson's disease patients ON and OFF L-dopa.

While Parkinson's disease (PD) is traditionally viewed as a motor disorder, there is mounting evidence that somatosensory function becomes affected as well. However, conflicting reports exist regarding whether plantar sensitivity is reduced in early-onset PD patients. Plantar sensitivity was assessed using monofilaments and a gold-standard, two-interval two-alternative forced choice vibrotactile detection task at both 30 and 250Hz. Lower-limb cutaneous reflexes were assessed by delivering continuous, sinusoidal vibration at 30 and 250Hz while recording muscle activity in Tibialis Anterior. We found no evidence of elevated plantar thresholds or dysfunctional lower-limb cutaneous reflexes in PD patients ON medication. We also found no acute effect of ceasing L-dopa intake on either plantar sensitivity or cutaneous reflexes. Our finding of intact cutaneous function in PD supports the further exploration of therapeutics that enhance plantar sensitivity to minimize postural instability, a source of considerable morbidity in this clinical population.

Older adults demonstrate superior vestibular perception for virtual rotations.

Adult ageing results in a progressive loss of vestibular hair cell receptors and afferent fibres. Given the robustness of vestibulo-ocular and vestibular-evoked whole-body responses to age-related deterioration, it was proposed that the vestibular system compensates centrally. Here we examine the potential for central compensation in vestibular sensitivity with adult ageing by using a combination of real and virtual rotation-based psychophysical testing at two stimulus frequencies (0.1 & 1Hz). Real rotations activate semi-circular canal hair cell receptors naturally via mechanotransduction, while electrical current used to evoke virtual rotations does not rely on mechanical deformation of hair cell receptors to activate vestibular afferents. This two-pronged approach allows us to determine the independent effects of age-related peripheral afferent receptor loss and potential compensatory mechanisms. Older adults had thresholds for discriminating real rotations that were significantly greater than young adults at 0.1Hz (7.2 vs. 3°/s), but the effect of age was weaker (non-significant) at 1Hz (2.4 vs. 1.3°/s). For virtual rotations, older adults had greater thresholds than young adults at 0.1Hz (1.2 vs. 0.5mA), however, older adults outperformed young adults at 1Hz (0.6 vs. 1.1mA). Based on these thresholds, we argue that central vestibular processing gain is enhanced in older adults for 1Hz real and virtual rotations, partially offsetting the negative impact of normal age-related hair cell receptor and primary afferent loss. We propose that the frequency dependence of this compensation reflects the physiological importance of the 1-5Hz range in natural vestibular input.