Vestibular Contributions to Primate Neck Postural Muscle Activity during Natural Motion.

To maintain stable posture of the head and body during our everyday activities, the brain integrates information across multiple sensory systems. Here, we examined how the primate vestibular system, independently and in combination with visual sensory input, contributes to the sensorimotor control of head posture across the range of dynamic motion experienced during daily life. We recorded activity of single motor units in the splenius capitis and sternocleidomastoid muscles in rhesus monkeys during yaw rotations spanning the physiological range of self-motion (up to 20 Hz) in darkness. Splenius capitis motor unit responses continued to increase with frequency up to 16 Hz in normal animals, and were strikingly absent following bilateral peripheral vestibular loss. To determine whether visual information modulated these vestibular-driven neck muscle responses, we experimentally controlled the correspondence between visual and vestibular cues of self-motion. Surprisingly, visual information did not influence motor unit responses in normal animals, nor did it substitute for absent vestibular feedback following bilateral peripheral vestibular loss. A comparison of muscle activity evoked by broadband versus sinusoidal head motion further revealed that low-frequency responses were attenuated when low- and high-frequency self-motion were experienced concurrently. Finally, we found that vestibular-evoked responses were enhanced by increased autonomic arousal, quantified via pupil size. Together, our findings directly establish the vestibular system's contribution to the sensorimotor control of head posture across the dynamic motion range experienced during everyday activities, as well as how vestibular, visual, and autonomic inputs are integrated for postural control.SIGNIFICANCE STATEMENT Our sensory systems enable us to maintain control of our posture and balance as we move through the world. Notably, the vestibular system senses motion of the head and sends motor commands, via vestibulospinal pathways, to axial and limb muscles to stabilize posture. By recording the activity of single motor units, here we show, for the first time, that the vestibular system contributes to the sensorimotor control of head posture across the dynamic motion range experienced during everyday activities. Our results further establish how vestibular, autonomic, and visual inputs are integrated for postural control. This information is essential for understanding both the mechanisms underlying the control of posture and balance, and the impact of the loss of sensory function.

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.

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.

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.

Reliability of the diaphragmatic compound muscle action potential evoked by cervical magnetic stimulation and recorded via chest wall surface EMG.

INTRODUCTION: Stimulation of the phrenic nerve via cervical magnetic stimulation (CMS) elicits a compound muscle action potential (CMAP) that allows for assessment of diaphragm activation. The reliability of CMS to evoke the CMAP recorded by chest wall surface EMG has yet to be comprehensively examined. METHODS: CMS was performed on healthy young males (n=10) and females (n=10). Surface EMG electrodes were placed on the right and left hemi-diaphragm between the 6-8th intercostal spaces. CMAPs were analysed for: latency, duration, peak-to-peak amplitude, and area. Reliability within and between experimental sessions was assessed using intraclass correlation coefficients (ICC). Bilateral (right-left) and sex-based (male-female) comparisons were also made (independent samples t-test). RESULTS: All CMAP characteristics demonstrated high reproducibility within (ICCs>0.96) and between (ICCs>0.89) experimental sessions. No statistically significant bilateral or sex-based differences were found (p>0.05). DISCUSSION: CMS is a reliable and non-invasive method to evaluate phrenic nerve conduction.

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.

Cutaneous afferent feedback from the posterior ankle contributes to proprioception.

Cutaneous mechanoreceptors in skin surrounding joints can respond to the skin strain generated by movement, and thus provide proprioceptive cues. The objective of this experiment was to determine the contribution of skin feedback from the posterior ankle to position sense during passive movements. In 28 healthy adults (12 male), a topical anesthetized (n=14) or placebo cream (n=14) was applied to an area of skin on the posterior ankle that undergoes stretch and compression during ankle dorsi- and plantar-flexion. Position sense was assessed before and after anesthetization using a passive joint matching task (target angles: 6°, 12°, and 18° dorsiflexion and plantar flexion). Results showed that reducing skin feedback caused the perception that the ankles were aligned when the anesthetized ankle was relatively more dorsiflexed, suggesting that posterior ankle skin primarily signals the magnitude of skin stretch. Larger movement into dorsiflexion was likely necessary to provide enough stretch of muscle and surrounding intact skin to compensate for reduced signals from the anesthetized skin region. Reducing skin feedback also increased matching variability during larger movements. These findings suggest that skin feedback from the posterior ankle has a significant contribution to position sense during passive movement. Therefore, the sensitivity of skin surrounding the ankle could be important to consider in populations with reduced peripheral skin sensitivity as a result of ageing or neurological disorders.

Vibrotactile stimulation of fast-adapting cutaneous afferents from the foot modulates proprioception at the ankle joint.

It has previously been shown that cutaneous sensory input from across a broad region of skin can influence proprioception at joints of the hand. The present experiment tested whether cutaneous input from different skin regions across the foot can influence proprioception at the ankle joint. The ability to passively match ankle joint position (17° and 7° plantar flexion and 7° dorsiflexion) was measured while cutaneous vibration was applied to the sole (heel, distal metatarsals) or dorsum of the target foot. Vibration was applied at two different frequencies to preferentially activate Meissner's corpuscles (45 Hz, 80 µm) or Pacinian corpuscles (255 Hz, 10 µm) at amplitudes ∼3 dB above mean perceptual thresholds. Results indicated that cutaneous input from all skin regions across the foot could influence joint-matching error and variability, although the strongest effects were observed with heel vibration. Furthermore, the influence of cutaneous input from each region was modulated by joint angle; in general, vibration had a limited effect on matching in dorsiflexion compared with matching in plantar flexion. Unlike previous results in the upper limb, we found no evidence that Pacinian input exerted a stronger influence on proprioception compared with Meissner input. Findings from this study suggest that fast-adapting cutaneous input from the foot modulates proprioception at the ankle joint in a passive joint-matching task. These results indicate that there is interplay between tactile and proprioceptive signals originating from the foot and ankle.

Reliability of the Achilles tendon tap reflex evoked during stance using a pendulum hammer.

The tendon tap reflex (T-reflex) is often evoked in relaxed muscles to assess spinal reflex circuitry. Factors contributing to reflex excitability are modulated to accommodate specific postural demands. Thus, there is a need to be able to assess this reflex in a state where spinal reflex circuitry is engaged in maintaining posture. The aim of this study was to determine whether a pendulum hammer could provide controlled stimuli to the Achilles tendon and evoke reliable muscle responses during normal stance. A second aim was to establish appropriate stimulus parameters for experimental use. Fifteen healthy young adults stood on a forceplate while taps were applied to the Achilles tendon under conditions in which postural sway was constrained (by providing centre of pressure feedback) or unconstrained (no feedback) from an invariant release angle (50°). Twelve participants repeated this testing approximately six months later. Within one experimental session, tap force and T-reflex amplitude were found to be reliable regardless of whether postural sway was constrained (tap force ICC=0.982; T-reflex ICC=0.979) or unconstrained (tap force ICC=0.968; T-reflex ICC=0.964). T-reflex amplitude was also reliable between experimental sessions (constrained ICC=0.894; unconstrained ICC=0.890). When a T-reflex recruitment curve was constructed, optimal mid-range responses were observed using a 50° release angle. These results demonstrate that reliable Achilles T-reflexes can be evoked in standing participants without the need to constrain posture. The pendulum hammer provides a simple method to allow researchers and clinicians to gather information about reflex circuitry in a state where it is involved in postural control.

Foot sole skin vibration perceptual thresholds are elevated in a standing posture compared to sitting.

Foot sole sensitivity is commonly assessed while individuals are seated or prone; however the primary role of foot sole cutaneous feedback is for the control of upright stance and gait. The aim of this study was to compare vibration perceptual thresholds across the foot sole between sitting and standing postures. Vibration perceptual thresholds were measured in sitting and standing postures in 18 healthy participants (8 male) using a custom vibration device. Two foot sole locations (heels and metatarsals) were tested at four vibration frequencies (3, 15, 40, and 250Hz) selected to target different cutaneous afferent populations. At each frequency, perceptual thresholds across the foot sole were significantly higher in the standing posture compared to the sitting posture; this is indicative of lower sensitivity while standing. In addition, threshold differences between the heels and metatarsals for lower frequency vibratory stimuli were more pronounced while standing, with higher thresholds observed at the heels. Our results demonstrate that standing significantly alters sensitivity across the foot sole. Therefore, conducting perceptual tests at the foot sole during stance could potentially provide more direct information about the ability of cutaneous afferents to signal tactile information in a state where this feedback can contribute to postural control.

Thresholds of cutaneous afferents related to perceptual threshold across the human foot sole.

Perceptual thresholds are known to vary across the foot sole, despite a reported even distribution in cutaneous afferents. Skin mechanical properties have been proposed to account for these differences; however, a direct relationship between foot sole afferent firing, perceptual threshold, and skin mechanical properties has not been previously investigated. Using the technique of microneurography, we recorded the monofilament firing thresholds of cutaneous afferents and associated perceptual thresholds across the foot sole. In addition, receptive field hardness measurements were taken to investigate the influence of skin hardness on these threshold measures. Afferents were identified as fast adapting [FAI (n = 48) or FAII (n = 13)] or slowly adapting [SAI (n = 21) or SAII (n = 20)], and were grouped based on receptive field location (heel, arch, metatarsals, toes). Overall, perceptual thresholds were found to most closely align with firing thresholds of FA afferents. In contrast, SAI and SAII afferent firing thresholds were found to be significantly higher than perceptual thresholds and are not thought to mediate monofilament perceptual threshold across the foot sole. Perceptual thresholds and FAI afferent firing thresholds were significantly lower in the arch compared with other regions, and skin hardness was found to positively correlate with both FAI and FAII afferent firing and perceptual thresholds. These data support a perceptual influence of skin hardness, which is likely the result of elevated FA afferent firing threshold at harder foot sole sites. The close coupling between FA afferent firing and perceptual threshold across foot sole indicates that small changes in FA afferent firing can influence perceptual thresholds.