Patrick A. Forbes

Task, muscle and frequency dependent vestibular control of posture

The vestibular system is crucial for postural control; however there are considerable differences in the task dependence and frequency response of vestibular reflexes in appendicular and axial muscles. For example, vestibular reflexes are only evoked in appendicular muscles when vestibular information is relevant to postural control, while in neck muscles they are maintained regardless of the requirement to maintain head on trunk balance. Recent investigations have also shown that the bandwidth of vestibular input on neck muscles is much broader than appendicular muscles (up to a factor of 3). This result challenges the notion that vestibular reflexes only contribute to postural control across the behavioral and physiological frequency range of the vestibular organ (i.e., 0–20 Hz). In this review, we explore and integrate these task-, muscle- and frequency-related differences in the vestibular system’s contribution to posture, and propose that the human nervous system has adapted vestibular signals to match the mechanical properties of the system that each group of muscles controls.

Muscle parameters for musculoskeletal modelling of the human neck

BACKGROUND To study normal or pathological neuromuscular control, a musculoskeletal model of the neck has great potential but a complete and consistent anatomical dataset which comprises the muscle geometry parameters to construct such a model is not yet available. METHODS A dissection experiment was performed on the left side of one 50th percentile male embalmed specimen. Geometrical data including muscle attachment sites were digitized using an Optotrak measurement system and laser diffraction was used to determine muscle sarcomere lengths. Bony landmarks were recorded and joint centres of rotation between different vertebrae were estimated using literature data. FINDINGS A total of 34 muscle parts of the neck were divided in 129 elements per body side. Muscle attachment sites, mass, physiological cross sectional area, fibre length, tendon length and optimal fibre length for each element are supplied as digital annexes to the paper. Results are coherent with other studies and new data are provided for several smaller muscles not reported elsewhere. INTERPRETATION Implementation of this dataset into a neck model is likely to improve the estimation of muscle forces and thus increase the model validity; this makes future neck models more suitable for the use as clinical tools.

Frequency response of vestibular reflexes in neck, back and lower limb muscles

Vestibular pathways form short-latency disynaptic connections with neck motoneurons, whereas they form longer-latency disynaptic and polysynaptic connections with lower limb motoneurons. We quantified frequency responses of vestibular reflexes in neck, back, and lower limb muscles to explain between-muscle differences. Two hypotheses were evaluated: 1) that muscle-specific motor-unit properties influence the bandwidth of vestibular reflexes; and 2) that frequency responses of vestibular reflexes differ between neck, back, and lower limb muscles because of neural filtering. Subjects were exposed to electrical vestibular stimuli over bandwidths of 0-25 and 0-75 Hz while recording activity in sternocleidomastoid, splenius capitis, erector spinae, soleus, and medial gastrocnemius muscles. Coherence between stimulus and muscle activity revealed markedly larger vestibular reflex bandwidths in neck muscles (0-70 Hz) than back (0-15 Hz) or lower limb muscles (0-20 Hz). In addition, vestibular reflexes in back and lower limb muscles undergo low-pass filtering compared with neck-muscle responses, which span a broader dynamic range. These results suggest that the wider bandwidth of head-neck biomechanics requires a vestibular influence on neck-muscle activation across a larger dynamic range than lower limb muscles. A computational model of vestibular afferents and a motoneuron pool indicates that motor-unit properties are not primary contributors to the bandwidth filtering of vestibular reflexes in different muscles. Instead, our experimental findings suggest that pathway-dependent neural filtering, not captured in our model, contributes to these muscle-specific responses. Furthermore, gain-phase discontinuities in the neck-muscle vestibular reflexes provide evidence of destructive interaction between different reflex components, likely via indirect vestibular-motor pathways.

Transformation of Vestibular Signals for the Control of Standing in Humans.

During standing balance, vestibular signals encode head movement and are transformed into coordinates that are relevant to maintaining upright posture of the whole body. This transformation must account for head-on-body orientation as well as the muscle actions generating the postural response. Here, we investigate whether this transformation is dependent upon a muscles ability to stabilize the body along the direction of a vestibular disturbance. Subjects were braced on top of a robotic balance system that simulated the mechanics of standing while being exposed to an electrical vestibular stimulus that evoked a craniocentric vestibular error of head roll. The balance system was limited to move in a single plane while the vestibular error direction was manipulated by having subjects rotate their head in yaw. Vestibular-evoked muscle responses were greatest when the vestibular error was aligned with the balance direction and decreased to zero as the two directions became orthogonal. This demonstrates that muscles respond only to the component of the error that is aligned with the balance direction and thus relevant to the balance task, not to the cumulative afferent activity, as expected for vestibulospinal reflex loops. When we reversed the relationship between balancing motor commands and associated vestibular sensory feedback, the direction of vestibular-evoked ankle compensatory responses was also reversed. This implies that the nervous system quickly reassociates new relationships between vestibular sensory signals and motor commands related to maintaining balance. These results indicate that vestibular-evoked muscle activity is a highly flexible balance response organized to compensate for vestibular disturbances. SIGNIFICANCE STATEMENT The postural corrections critical to standing balance and navigation rely on transformation of sensory information into reference frames that are relevant for the required motor actions. Here, we demonstrate that the nervous system transforms vestibular sensory signals of head motion according to a muscles ability to stabilize the body along the direction of a vestibular-evoked disturbance. By manipulating the direction of the imposed vestibular signal relative to a muscles action, we show that the vestibular contribution to muscle activity is a highly flexible and organized balance response. This study provides insight into the neural integration and central processing associated with transformed vestibulomotor relationships that are essential to standing upright.

Vestibulocollic reflexes in the absence of head postural control

Percutaneous electrical vestibular stimulation evokes reflexive responses in appendicular muscles that are suppressed during tasks in which the muscles are not contributing to balance control. In neck muscles, which stabilize the head on the torso and in space, it is unclear whether similar postural task dependence shapes vestibular reflexes. We investigated whether vestibulocollic reflexes are modulated during tasks in which vestibular information is not directly relevant to maintaining the head balanced on the torso. We hypothesized that vestibulocollic reflexes would be 1) evoked when neck muscles are not involved in balancing the head on the torso and 2) invariant across synergistic neck muscle contraction tasks. Muscle activity was recorded bilaterally in sternocleidomastoid and splenius capitis muscles during head-free and head-fixed conditions while subjects were exposed to stochastic electrical vestibular stimulation (± 5 mA, 0-75 Hz). Significant vestibular reflex responses (P < 0.05) were observed during head-free and head-fixed trials. Response magnitude and timing were similar between head-free and head-fixed trials for sternocleidomastoid, but splenius capitis magnitudes decreased with the head fixed by ∼ 25% (P < 0.05). Nevertheless, this indicates that vestibulocollic responses are evoked independent of the requirement to maintain postural control of the head on the torso. Response magnitude and timing were similar across focal muscle contractions (i.e., axial rotation/flexion/extension) provided the muscle was active. In contrast, when subjects cocontracted neck muscles, vestibular-evoked responses decreased in sternocleidomastoid by ∼ 30-45% (P < 0.05) compared with focal muscle contractions but remained unchanged in splenius capitis. These results indicate robust vestibulocollic reflex coupling, which we suggest functions through its closed-loop influence on head posture to ensure cervical spine stabilization.

Improved identification of dystonic cervical muscles via abnormal muscle activity during isometric contractions.

BACKGROUND The preferred treatment for cervical dystonia (CD) is injection of botulinum toxin in the dystonic muscles. Unfortunately, in the absence of reliable diagnostic methods it can be difficult to discriminate dystonic muscles from healthy muscles acting in compensation. We investigated if dystonic muscle activation patterns could be identified in cervical dystonia patients during a harmonized isometric contraction task. Furthermore, we investigated whether dystonia worsens at higher levels of voluntary contraction, which might further improve the identification of dystonic muscle activity. METHODS An isometric device was used to investigate muscle activation during voluntary contraction tasks in 10 controls and 10 CD patients. Surface electromyography (EMG) of the sternocleidomastoidus, splenius capitis, and semispinalis capitis muscles was evaluated during a rest task and when performing submaximal (20%) and maximal voluntary contractions for eight head transversal force directions and for head twist. Two measures were developed to identify dystonic activation: 1) Muscle activity in the contraction direction in which the contribution of the muscle was lowest (Minimum EMG), and 2) the average muscle activity over all contraction directions (Total Mean EMG). RESULTS Patients showed increased dystonic activity in the rest task and during submaximal contractions relative to controls, but not during maximal contractions. Increases in Minimum EMG indicated an inability of patients to deactivate dystonic muscles counteracting the task. Increases in Total Mean EMG indicated dystonic activity in all task directions. During maximal contractions these effects were absent in dystonic muscles. Dystonia is therefore found not to worsen at higher levels of isometric voluntary contraction. The activity of dystonic muscles modulated with different loading directions similar to controls. Using Minimum EMG 54% of the muscles clinically diagnosed as dystonic and 91% of non-dystonic muscles were predicted correctly. CONCLUSIONS Dystonic muscle activity was found in cervical dystonia patients during submaximal contractions in all task directions using a harmonized isometric task, but no differences were found during maximal contractions. With some adaptation this method may prove useful to identify dystonic muscles.

Galvanic Vestibular Stimulation Elicits Consistent Head–Neck Motion in Seated Subjects

Humans actively stabilize the head-neck system based on vestibular, proprioceptive and visual information. Galvanic vestibular stimulation (GVS) has been used previously to demonstrate the role of vestibular feedback in standing balance. This study explores the effect of GVS on head-neck kinematics and evaluates the approach to investigate the vestibular contribution to head-neck stabilization. GVS was applied to 11 seated subjects using seven different stimuli (single sinusoids and multisines) at amplitudes of 0.5-2 mA and frequencies of 0.4-5.2 Hz using a bilateral bipolar configuration while 3-D head and torso kinematics were recorded using motion capture. System identification techniques were used evaluating coherence and frequency response functions (FRFs). GVS resulted in significant coherence in roll, yaw and lateral translation, consistent with effects of GVS while standing as reported in the literature. The gain of the FRFs varied with frequency and no modulation was observed across the stimulus amplitudes, indicating a linear system response for the stimulations considered. Compared to single sine stimulation, equivalent FRFs were observed during unpredictable multisine stimulation, suggesting the responses during both stimuli to be of a reflexive nature. These results demonstrate the potential of GVS to investigate the vestibular contribution to head-neck stabilization.

Rapid limb‐specific modulation of vestibular contributions to ankle muscle activity during locomotion

The vestibular influence on human walking is phase‐dependent and modulated across both limbs with changes in locomotor velocity and cadence. Using a split‐belt treadmill, we show that vestibular influence on locomotor activity is modulated independently in each limb. The independent vestibular modulation of muscle activity from each limb occurs rapidly at the onset of split‐belt walking, over a shorter time course relative to the characteristic split‐belt error‐correction mechanisms (i.e. muscle activity and kinematics) associated with locomotor adaptation. Together, the present results indicate that the nervous system rapidly modulates the vestibular influence of each limb separately through processes involving ongoing sensory feedback loops. These findings help us understand how vestibular information is used to accommodate the variable and commonplace demands of locomotion, such as turning or navigating irregular terrain.

Electrical vestibular stimuli to enhance vestibulo-motor output and improve subject comfort.

Electrical vestibular stimulation is often used to assess vestibulo-motor and postural responses in both clinical and research settings. Stochastic vestibular stimulation (SVS) is a recently established technique with many advantages over its square-wave counterpart; however, the evoked muscle responses remain relatively small. Although the vestibular-evoked responses can be enhanced by increasing the stimulus amplitude, subjects often perceive these higher intensity electrical stimuli as noxious or painful. Here, we developed multisine vestibular stimulation (MVS) signals that include precise frequency contributions to increase signal-to-noise ratios (SNR) of stimulus-evoked muscle and motor responses. Subjects were exposed to three different MVS stimuli to establish that: 1) MVS signals evoke equivalent vestibulo-motor responses compared to SVS while improving subject comfort and reducing experimentation time, 2) stimulus-evoked vestibulo-motor responses are reliably estimated as a linear system and 3) specific components of the cumulant density time domain vestibulo-motor responses can be targeted by controlling the frequency content of the input stimulus. Our results revealed that in comparison to SVS, MVS signals increased the SNR 3–6 times, reduced the minimum experimentation time by 85% and improved subjective measures of comfort by 20–80%. Vestibulo-motor responses measured using both EMG and force were not substantially affected by nonlinear distortions. In addition, by limiting the contribution of high frequencies within the MVS input stimulus, the magnitude of the medium latency time domain motor output response was increased by 58%. These results demonstrate that MVS stimuli can be designed to target and enhance vestibulo-motor output responses while simultaneously improving subject comfort, which should prove beneficial for both research and clinical applications.

EMG coherence and spectral analysis in cervical dystonia: discriminative tools to identify dystonic muscles?

OBJECTIVE Botulinum toxin injections in the dystonic muscles are the preferred treatment for cervical dystonia (CD), but proper selection of the dystonic muscles remains a challenge. We investigated the use of EMG coherence and autospectral analysis as discriminative tools to identify dystonic muscles in CD patients. METHODS We compared the occurrence of 8-14 Hz autospectral peaks and 4-7 Hz intermuscular coherences between 10 CD patients and 10 healthy controls. Secondly, we compared the muscles with significant 4-7 Hz coherences with the muscles that were selected clinically for botulinum toxin treatment. RESULTS Autospectral peaks between 8 and 14 Hz were significantly more often absent in the splenius capitis (SPL) muscles of CD patients compared to controls (p<0.01). Contrary to previous findings, there was no significant difference in the occurrence of 4-7 Hz intermuscular coherences between patients and controls and the diagnostic accuracy of coherence analysis to identify the clinically dystonic muscles was low. CONCLUSION Intermuscular EMG coherence analysis cannot reliably discriminate patients from controls. Autospectral changes in the SPL muscles are a more discriminative feature of CD. In patients, coherence analysis does not seem to be a reliable method to identify dystonic muscles. The clinical relevance and the origin of the autospectral changes need further study.