Christopher J. Dakin

Frequency-Specific Modulation of Vestibular-Evoked Sway Responses in Humans

Galvanic vestibular stimulation (GVS) results in characteristic muscle and whole-body responses in humans maintaining standing balance. However, the relationship between these two vestibular-evoked responses remains elusive. This study seeks to determine whether mechanical filtering from conversion of lower-limb muscle activity to body sway, during standing balance, can be used to attenuate sway while maintaining biphasic lower-limb muscle responses using frequency-limited stochastic vestibular stimulation (SVS). We hypothesized that SVS deprived of frequencies <2 Hz would evoke biphasic muscle responses with minimal whole-body sway due to mechanical filtering of the higher-frequency muscle responses. Subjects were exposed to five stimulus bandwidths: two meant to induce sway responses (0-1 and 0-2 Hz) and three to dissociate vestibular-evoked muscle responses from whole-body sway (0-25, 1-25, and 2-25 Hz). Two main results emerged: 1) SVS-related sway was attenuated when frequencies <2 Hz were excluded, whereas multiphasic muscle and force responses were retained; and 2) the gain of the estimated transfer functions exhibited successive low-pass filtering of vestibular stimuli during conversion to muscle activity, anteroposterior (AP) moment, and sway. This successive low-pass filtering limited the transfer of signal power to frequencies <20 Hz in muscle activity, <5 Hz in AP moment, and <2 Hz in AP trunk sway. Consequently, the present results show that SVS delivered at frequencies >2 Hz to standing humans do not cause a destabilizing whole-body sway response but are associated with the typical biphasic lower-limb muscle responses.

Lack of otolith involvement in balance responses evoked by mastoid electrical stimulation

Passing current through mastoid electrodes (conventionally termed galvanic vestibular stimulation; GVS) evokes a balance response containing a short‐ and a medium‐latency response. The origins of these two responses are debated. Here we test the hypotheses that they originate from net signals evoked by stimulation of otolith and semi‐circular canal afferents, respectively. Based on anatomy and function, we predicted the directions of the stimulus‐evoked net head rotation vector from the canals and the linear acceleration net vector from the otoliths. We tested these predictions in healthy adults by obtaining responses with the head in strategic postures to alter the relevance of the signals to the balance system. Cross‐covariance between a stochastic waveform of stimulating current and motor output was used to assess the balance responses. Consistent with the canal hypothesis, with the head pitched down the medium‐latency EMG response was abolished while the short‐latency EMG response was maintained. The results, however, did not support the otolith hypothesis. The direction of the linear acceleration signal from the otoliths was predicted to change substantially when using monaural stimuli compared to binaural stimuli. In contrast, short‐latency response direction measured from ground‐reaction forces was not altered. It was always directed along the inter‐aural axis irrespective of whether the stimulus was applied binaurally or monaurally, whether the head was turned in yaw through 90 deg, whether the head was pitched down through 90 deg, or combinations of these manipulations. We conclude that a net canal signal evoked by GVS contributes to the medium‐latency response whilst a net otolith signal does not make a significant contribution to either the short‐ or medium‐latency responses.

Absence of lateral gastrocnemius activity and differential motor unit behavior in soleus and medial gastrocnemius during standing balance.

In a standing position, the vertical projection of the center of mass passes in front of the ankle, which requires active plantar-flexor torque from the triceps surae to maintain balance. We recorded motor unit (MU) activity in the medial (MG) and lateral (LG) gastrocnemius muscle and the soleus (SOL) in standing balance and voluntary isometric contractions to understand the effect of functional requirements and descending drive from different neural sources on motoneuron behavior. Single MU activity was recorded in seven subjects with wire electrodes in the triceps surae. Two 3-min standing balance trials and several ramp-and-hold contractions were performed. Lateral gastrocnemius MU activity was rarely observed in standing. The lowest thresholds for LG MUs in ramp contractions were 20-35 times higher than SOL and MG MUs (P < 0.001). Compared with MUs from the SOL, MG MUs were intermittently active (P < 0.001), had higher recruitment thresholds (P = 0.022), and greater firing rate variability (P < 0.001); this difference in firing rate variability was present in standing balance and isometric contractions. In SOL and MG MUs, both recruitment of new MUs (R(2) = 0.59-0.79, P < 0.01) and MU firing rates (R(2) = 0.05-0.40, P < 0.05) were associated with anterior-posterior and medio-lateral torque in standing. Our results suggest that the two heads of the gastrocnemius may operate in different ankle ranges with the larger MG being of primary importance when standing, likely due to its fascicle orientation. These differences in MU discharge behavior were independent of the type of descending neural drive, which points to a muscle-specific optimization of triceps surae motoneurons.

Modulation of human vestibular reflexes with increased postural threat

The vestibular system is an important sensory contributor to the control of standing balance. Fear, anxiety and arousal are thought to influence the excitability of the vestibular system, but it is not clear if these changes lead to altered vestibular‐evoked balance reflexes. Low and high standing surface heights were used to manipulate fear and anxiety in this study, while stochastic vestibular stimulation was used to evoke balance reflexes. High surface heights lead to greater coupling between vestibular inputs and balance reflexes, as well as larger responses. These results support the idea that the manner in which vestibular information is processed is altered when people are exposed to a threat to their balance, and this altered processing may explain why normal balance behaviour is different in threatening scenarios.

Extracting phase-dependent human vestibular reflexes during locomotion using both time and frequency correlation approaches

Daily activities, such as walking, may require dynamic modulation of vestibular input onto motoneurons. This dynamic modulation is difficult to identify in humans due to limitations in the delivery and analysis of current vestibular probes, such as galvanic vestibular stimulation. Stochastic vestibular stimulation, however, provides an alternative method to extract human vestibular reflexes. Here, we used time-dependent coherence and time-dependent cross-correlation, coupled with stochastic vestibular stimulation, to investigate the phase dependency of human vestibular reflexes during locomotion. We found that phase-dependent activity from the medial gastrocnemius muscles is correlated with the vestibular signals over the 2- to 20-Hz bandwidth during the stance phase of locomotion. Vestibular-gastrocnemius coherence and time-dependent cross-correlations reached maximums at 21 ± 4 and 23 ± 8% of the step cycle following heel contact and before the period of maximal electromyographic activity (38 ± 5%). These results demonstrate 1) the effectiveness of these techniques in extracting the phase-dependent modulation of vestibulomuscular coupling during a cyclic task; 2) that vestibulomuscular coupling is phasically modulated during locomotion; and 3) that the period of strongest vestibulomuscular coupling does not correspond to the period of maximal electromyographic activity in the gastrocnemius. Therefore, we have shown that stochastic vestibular stimulation, coupled with time-frequency decomposition, provides an effective tool to assess the contribution of vestibular ex-afference to the muscular control during locomotion.

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.

Muscle-specific modulation of vestibular reflexes with increased locomotor velocity and cadence.

Vestibular information is one of the many sensory signals used to stabilize the body during locomotion. When locomotor velocity increases, the influence of these signals appears to wane. It is unclear whether vestibular signals are globally attenuated with velocity or are influenced by factors such as whether a muscle is contributing to balance control. Here we investigate how vestibular sensory signals influence muscles of the leg during locomotion and what causes their attenuation with increasing locomotor velocity. We hypothesized that 1) vestibular signals influence the activity of all muscles engaged in the maintenance of medio-lateral stability during locomotion and 2) increases in both cadence and velocity would be associated with attenuation of these signals. We used a stochastic vestibular stimulus and recorded electromyographic signals from muscles of the ankle, knee, and hip. Participants walked using two cadences (52 and 78 steps/min) and two walking velocities (0.4 and 0.8 m/s). We observed phase-dependent modulation of vestibular influence over ongoing muscle activity in all recorded muscles. Within a stride, reversals of the muscle responses were observed in the biceps femoris, tibialis anterior, and rectus femoris. Vestibular-muscle coupling decreases with increases in both cadence and walking velocity. These results show that the observed vestibular suppression is muscle- and phase dependent. We suggest that the phase- and muscle-specific influence of vestibular signals on locomotor activity is organized according to each muscles functional role in body stabilization during locomotion.

Rectification is required to extract oscillatory envelope modulation from surface electromyographic signals

Rectification of surface electromyographic (EMG) recordings prior to their correlation with other signals is a widely used form of preprocessing. Recently this practice has come into question, elevating the subject of EMG rectification to a topic of much debate. Proponents for rectifying suggest it accentuates the EMG spike timing information, whereas opponents indicate it is unnecessary and its nonlinear distortion of data is potentially destructive. Here we examine the necessity of rectification on the extraction of muscle responses, but for the first time using a known oscillatory input to the muscle in the form of electrical vestibular stimulation. Participants were exposed to sinusoidal vestibular stimuli while surface and intramuscular EMG were recorded from the left medial gastrocnemius. We compared the unrectified and rectified surface EMG to single motor units to determine which method best identified stimulus-EMG coherence and phase at the single-motor unit level. Surface EMG modulation at the stimulus frequency was obvious in the unrectified surface EMG. However, this modulation was not identified by the fast Fourier transform, and therefore stimulus coherence with the unrectified EMG signal failed to capture this covariance. Both the rectified surface EMG and single motor units displayed significant coherence over the entire stimulus bandwidth (1-20 Hz). Furthermore, the stimulus-phase relationship for the rectified EMG and motor units shared a moderate correlation (r = 0.56). These data indicate that rectification of surface EMG is a necessary step to extract EMG envelope modulation due to motor unit entrainment to a known stimulus.

Vestibular Contribution to Balance Control in the Medial Gastrocnemius and Soleus

The soleus (Sol) and medial gastrocnemius (mGas) muscles have different patterns of activity during standing balance and may have distinct functional roles. Using surface electromyography we previously observed larger responses to galvanic vestibular stimulation (GVS) in the mGas compared with the Sol muscle. However, it is unclear whether this difference is an artifact that reflects limitations associated with surface electromyography recordings or whether a compensatory balance response to a vestibular error signal activates the mGas to a greater extent than the Sol. In the present study, we compared the effect of GVS on the discharge behavior of 9 Sol and 21 mGas motor units from freely standing subjects. In both Sol and mGas motor units, vestibular stimulation induced biphasic responses in measures of discharge timing [11 ± 5.0 (mGas) and 5.6 ± 3.8 (Sol) counts relative to the sham (mean ± SD)], and frequency [0.86 ± 0.6 Hz (mGas), 0.34 ± 0.2 Hz (Sol) change relative to the sham]. Peak-to-trough response amplitudes were significantly larger in the mGas (62% in the probability-based measure and 160% in the frequency-based measure) compared with the Sol (multiple P < 0.05). Our results provide direct evidence that vestibular signals have a larger influence on the discharge activity of motor units in the mGas compared with the Sol. More tentatively, these results indicate the mGas plays a greater role in vestibular-driven balance corrections during standing balance.

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.