John Timothy Inglis

The effects of stochastic galvanic vestibular stimulation on human postural sway

Abstract Galvanic vestibular stimulation serves to modulate the continuous firing level of the peripheral vestibular afferents. It has been shown that the application of sinusoidally varying, bipolar galvanic currents to the vestibular system can lead to sinusoidally varying postural sway. Our objective was to test the hypothesis that stochastic galvanic vestibular stimulation can lead to coherent stochastic postural sway. Bipolar binaural stochastic galvanic vestibular stimulation was applied to nine healthy young subjects. Three different stochastic vestibular stimulation signals, each with a different frequency content (0–1 Hz, 1–2 Hz, and 0–2 Hz), were used. The stimulation level (range 0.4–1.5 mA, peak to peak) was determined on an individual basis. Twenty 60-s trials were conducted on each subject – 15 stimulation trials (5 trials with each stimulation signal) and 5 control (no stimulation) trials. During the trials, subjects stood in a relaxed, upright position with their head facing forward. Postural sway was evaluated by using a force platform to measure the displacements of the center of pressure (COP) under each subject’s feet. Cross-spectral measures were used to quantify the relationship between the applied stimulus and the resulting COP time series. We found significant coherency between the stochastic vestibular stimulation signal and the resulting mediolateral COP time series in the majority of trials in 8 of the 9 subjects tested. The coherency results for each stimulation signal were reproducible from trial to trial, and the highest degree of coherency was found for the 1- to 2-Hz stochastic vestibular stimulation signal. In general, for the nine subjects tested, we did not find consistent significant coherency between the stochastic vestibular stimulation signals and the anteroposterior COP time series. This work demonstrates that, in subjects who are facing forward, bipolar binaural stochastic galvanic stimulation of the vestibular system leads to coherent stochastic mediolateral postural sway, but it does not lead to coherent stochastic anteroposterior postural sway. Our finding that the coherency was highest for the 1- to 2-Hz stochastic vestibular stimulation signal may be due to the intrinsic dynamics of the quasi-static postural control system. In particular, it may result from the effects of the vestibular stimulus simply being superimposed upon the quiet-standing COP displacements. By utilizing stochastic stimulation signals, we ensured that the subjects could not predict a change in the vestibular stimulus. Thus, our findings indicate that subjects can act as ”responders” to galvanic vestibular stimulation.

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.

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.

First trial and StartReact effects induced by balance perturbations to upright stance

Postural responses (PR) to a balance perturbation differ between the first and subsequent perturbations. One explanation for this first trial effect is that perturbations act as startling stimuli that initiate a generalized startle response (GSR) as well as the PR. Startling stimuli, such as startling acoustic stimuli (SAS), are known to elicit GSRs, as well as a StartReact effect, in which prepared movements are initiated earlier by a startling stimulus. In this study, a StartReact effect paradigm was used to determine if balance perturbations can also act as startle stimuli. Subjects completed two blocks of simple reaction time trials involving wrist extension to a visual imperative stimulus (IS). Each block included 15 CONTROL trials that involved a warning cue and subsequent IS, followed by 10 repeated TEST trials, where either a SAS (TESTSAS) or a toes-up support-surface rotation (TESTPERT) was presented coincident with the IS. StartReact effects were observed during the first trial in both TESTSAS and TESTPERT conditions as evidenced by significantly earlier wrist movement and muscle onsets compared with CONTROL. Likewise, StartReact effects were observed in all repeated TESTSAS and TESTPERT trials. In contrast, GSRs in sternocleidomastoid and PRs were large in the first trial, but significantly attenuated over repeated presentation of the TESTPERT trials. Results suggest that balance perturbations can act as startling stimuli. Thus first trial effects are likely PRs which are superimposed with a GSR that is initially large, but habituates over time with repeated exposure to the startling influence of the balance perturbation.

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.

Short-duration galvanic vestibular stimulation evokes prolonged balance responses

The application of galvanic vestibular stimulation (GVS) evokes distinct responses in lower limb muscles involved in the control of balance. The purpose of this study was to investigate the balance and lower limb muscle responses to short-duration GVS and to determine whether these responses are modulated by small changes in center of gravity (CoG) and baseline muscle activity occurring during quiet standing. Twelve subjects stood quietly on a force plate with their feet together and were instructed to look straight ahead. One thousand twenty-four GVS stimuli (4 mA, 20-ms pulses) were delivered bilaterally to the mastoid processes in a bipolar, binaural configuration. Bilateral surface electromyography (EMG) from soleus (Sol) and tibialis anterior (TA) and ground reaction forces were recorded. EMG and force responses were trigger averaged at the onset of the GVS pulse. Short-duration GVS applied during quiet standing with the head facing forward evoked characteristic balance responses and biphasic modulation of all muscles with the same polarity for ipsilateral Sol and TA. The amplitude of the GVS-evoked muscle responses was modulated by both the estimated position of the subjects CoG and the background activation of the recorded muscle. Muscle-dependent modulations of the GVS-evoked muscle responses were observed: the Sol responses decreased, while the TA responses increased when the CoG position shifted toward the heels. The well-defined balance responses evoked by short-duration GVS are important to acknowledge when studying the vestibulo-motor responses in healthy subjects and patient populations.

Vestibulo-spinal and vestibulo-ocular reflexes are modulated when standing with increased postural threat

We investigated how vestibulo-spinal reflexes (VSRs) and vestibulo-ocular reflexes (VORs) measured through vestibular evoked myogenic potentials (VEMPs) and video head impulse test (vHIT) outcomes, respectively, are modulated during standing under conditions of increased postural threat. Twenty-five healthy young adults stood quietly at low (0.8 m from the ground) and high (3.2 m) surface height conditions in two experiments. For the first experiment (n = 25) VEMPs were recorded with surface EMG from inferior oblique (IO), sternocleidomastoid (SCM), trapezius (TRP), and soleus (SOL) muscles in response to 256 air-conducted short tone bursts (125 dB SPL, 500 Hz, 4 ms) delivered via headphones. A subset of subjects (n = 19) also received horizontal and vertical head thrusts (∼150°/s) at each height in a separate session, comparing eye and head velocities by using a vHIT system for calculating the functional VOR gains. VEMP amplitudes (IO, TRP, SOL) and horizontal and vertical vHIT gains all increased with high surface height conditions (P < 0.05). Changes in IO and SCM VEMP amplitudes as well as horizontal vHIT gains were correlated with changes in electrodermal activity (ρ = 0.44-0.59, P < 0.05). VEMP amplitude for the IO also positively correlated with fear (ρ = 0.43, P = 0.03). Threat-induced anxiety, fear, and arousal have significant effects on VSR and VOR gains that can be observed in both physiological and functional outcome measures. These findings provide support for a potential central modulation of the vestibular nucleus complex through excitatory inputs from neural centers involved in processing fear, anxiety, arousal, and vigilance.

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.

Startle induces early initiation of classically conditioned postural responses

Startling acoustic stimuli (SAS) induce the early release of prepared motor responses. The current study used SAS, in conjunction with a classical conditioning paradigm, to examine advanced motor preparation of conditioned postural responses (PRs). After generalized startle responses were induced, standing posture was perturbed in 2 blocks of 15 Conditioning trials, where in each trial the onset of a nonstartling auditory cue [i.e., a conditioned stimulus (CS)] preceded a leftward support-surface translation. Upon completion of each block, a single trial was conducted. After block 1, a CS-Only trial was used to induce conditioned PRs in the absence of balance perturbations. After block 2, a post-Conditioning Startle trial that involved a CS subsequently followed by a SAS was used to examine motor preparation of conditioned PRs. PRs were quantified in terms of center of pressure displacements, ankle and hip kinematics, as well as surface electromyography of proximal and distal bilateral muscle pairs. Results indicated that repeated experience with cued balance perturbations led to PR conditioning and, more importantly, motor preparation of PRs. Conditioning was evidenced in biomechanical and electromyographic responses observed in CS-Only trials, as well as the progressive changes to evoked response parameters during repeated Conditioning trials. SAS presented in post-Conditioning Startle trials evoked early onsets of biomechanical and electromyographic responses, while preserving relative response parameters that were each distinct from generalized startle responses. These results provide important insight into both the consequences of using cues in dynamic postural control studies and the neural mechanisms governing PRs.

Cortical and vestibular stimulation reveal preserved descending motor pathways in individuals with motor-complete spinal cord injury.

OBJECTIVE To use a combination of electrophysiological techniques to determine the extent of preserved muscle activity below the clinically-defined level of motor-complete spinal cord injury. METHODS Transcranial magnetic stimulation and vestibular-evoked myogenic potentials were used to investigate whether there was any preserved muscle activity in trunk, hip and leg muscles of 16 individuals with motor-complete spinal cord injury (C4-T12) and 16 able-bodied matched controls. RESULTS Most individuals (14/16) with motor-complete spinal cord injury were found to have transcranial magnetic stimulation evoked, and/or voluntary evoked muscle activity in muscles innervated below the clinically classified lesion level. In most cases voluntary muscle activation was accompanied by a present transcranial magnetic stimulation response. Furthermore, motor-evoked potentials to transcranial magnetic stimulation could be observed in muscles that could not be voluntarily activated. Vestibular-evoked myogenic potentials responses were also observed in a small number of subjects, indicating the potential preservation of other descending pathways. CONCLUSION These results highlight the importance of using multiple electrophysiological techniques to assist in determining the potential preservation of muscle activity below the clinically-defined level of injury in individuals with a motor-complete spinal cord injury. These techniques may provide clinicians with more accurate information about the state of various motor pathways, and could offer a method to more accurately target rehabilitation.