Probing the human vestibular system with galvanic stimulation.

Galvanic vestibular stimulation (GVS) is a simple, safe, and specific way to elicit vestibular reflexes. Yet, despite a long history, it has only recently found popularity as a research tool and is rarely used clinically. The obstacle to advancing and exploiting GVS is that we cannot interpret the evoked responses with certainty because we do not understand how the stimulus acts as an input to the system. This paper examines the electrophysiology and anatomy of the vestibular organs and the effects of GVS on human balance control and develops a model that explains the observed balance responses. These responses are large and highly organized over all body segments and adapt to postural and balance requirements. To achieve this, neurons in the vestibular nuclei receive convergent signals from all vestibular receptors and somatosensory and cortical inputs. GVS sway responses are affected by other sources of information about balance but can appear as the sum of otolithic and semicircular canal responses. Electrophysiological studies showing similar activation of primary afferents from the otolith organs and canals and their convergence in the vestibular nuclei support this. On the basis of the morphology of the cristae and the alignment of the semicircular canals in the skull, rotational vectors calculated for every mode of GVS agree with the observed sway. However, vector summation of signals from all utricular afferents does not explain the observed sway. Thus we propose the hypothesis that the otolithic component of the balance response originates from only the pars medialis of the utricular macula.     

Dependence of the Magnitude of Postural Reactions in Humans on the Strength of Unilateral Galvanic Anodal and Cathodal Vestibular Stimulations

In 13 healthy volunteers, we recorded stabilographic postural reactions (side inclinations of the body) to unilateral galvanic vestibular stimulation (GVS) by rectangular current pulses (4 sec long, 2, 3, 4, 5, or 6 mA). For the cathodal GVS, the dependence of the magnitude of reaction was linear within this range. The corresponding dependence for the anodal GVS was close to linear at small currents, but the increment of the magnitude became smaller with further increase in the stimulation intensity, and a plateau was formed. A significant divergence between the two curves was observed with stimulation currents 4 mA and higher. This difference can be explained considering modern concepts on the mechanism of GVS-induced effects (an increase or a decrease in the level of tonic impulsation in fibers of the vestibular nerve under the influence of polarization). Anodal GVS continues to suppress tonic activity up to the moment where all GVS-sensitive vestibular afferents stop to generate impulses; a further increase in the intensity of hyperpolarizing current is not accompanied by a decrease in the activity in the vestibular nerve and, consequently, by an increase in the magnitude of postural reactions. The tested approach can be used for qualitative estimation of the vestibular tone in humans. Neirofiziologiya/Neurophysiology, Vol. 37, No. 2, pp. 169–176, March–April, 2005.     

Stabilometry and definition of the threshold of galvanic vestibular stimulation in normal subjects: an experimental study

The effect of the galvanic stimulation on the vestibular apparatus has been evaluated by registration on the postural deviations, using a stabilometry platform. We have studied the galvanic body-sway responses in a group of normal subjects, using a binauricolar bipolar stimulation, with the electrodes attached by means of surgical tape to the mastoid area. The records of body-sway responses have demonstrated in 80% of the considered cases a significant variation of all positional parameters after a current intensity of 2 mA, according the body sways toward the positive stimulus. At the same current intensity only five of the studied subjects have shown multidirectional swinging, in three cases joined with a subjective slight sway toward the ear stimulated with positive polarity. Therefore the galvanic test, joined with the posturography, proves to be a useful auxiliary method in vestibular investigation, allowing us to lower the threshold of galvanic stimulation and to make the electric stimulus better supported for the patient.     

Somatosensory influence on postural response to galvanic vestibular stimulation

We investigated how postural responses to galvanic vestibular stimulation were affected by standing on a translating support surface and by somatosensory loss due to diabetic neuropathy. We tested the hypothesis that an unstable surface and somatosensory loss can result in an increase of vestibulospinal sensitivity. Bipolar galvanic vestibular stimulation was applied to subjects who were standing on a force platform, either on a hard, stationary surface or during a backward platform translation (9 cm, 4.2 cm/s). The intensity of the galvanic stimulus was varied from 0.25 to 1 mA. The amplitude of the peak body CoP displacement in response to the galvanic stimulus was plotted as a function of stimulus intensity for each individual. A larger increase in CoP displacement to a given increase in galvanic current was interpreted as an increase of vestibulospinal sensitivity. Subjects with somatosensory loss in the feet due to diabetes showed higher vestibulospinal sensitivity than healthy subjects when tested on a stationary support surface. Control subjects and patients with somatosensory loss standing on translating surface also showed increased galvanic response gains compared to stance on a stationary surface. The severity of the somatosensory loss in the feet correlated with the increased postural sensitivity to galvanic vestibular stimulation. These results showed that postural responses to galvanic vestibular stimulus were modified by somatosensory information from the surface. Somatosensory loss due to diabetic neuropathy and alteration of somatosensory input during stance on translating support surface resulted in increased vestibulospinal sensitivity.     

Vestibular-dependent spinal reflexes evoked by brief lateral accelerations of the heads of standing subjects

An impulsive acceleration stimulus, previously shown to activate vestibular afferents, was applied to the mastoid. Evoked EMG responses from the soleus muscles in healthy subjects (n = 10) and patients with bilateral vestibular dysfunction (n = 3) were recorded and compared with the effects of galvanic stimulation (GVS). Subjects were stimulated while having their eyes closed, head rotated, and while tonically activating their soleus muscles. Rectified EMG responses were recorded from the leg contralateral to the direction of head rotation. Responses were characterized by triphasic potentials that consisted of short-latency (SL), medium-latency (ML), and long-latency (LL) components beginning at (mean ± SD) 54.2 ± 4.8, 88.4 ± 4.7, and 121 ± 7.1 ms, respectively. Mean amplitudes for the optimum stimulus rise times were 9.05 ± 3.44% for the SL interval, 16.70 ± 4.41% for the ML interval, and 9.75 ± 4.89% for the LL interval compared with prestimulus values. Stimulus rise times of 14 and 20 ms evoked the largest ML amplitudes. GVS evoked biphasic responses (SL and ML) with similar latencies. Like GVS, the polarity of the initial interval was determined by the polarity of the stimulus and the evoked EMG response was attenuated when subjects were seated. There was no significant EMG response evoked when subjects were stimulated using 500-Hz vibration or in patients with bilateral vestibular dysfunction. Our study demonstrates that a brief lateral acceleration, likely to activate the utricle, can evoke spinal responses with properties similar to those previously shown for vestibular activation by GVS. The triphasic nature of the responses may allow the nervous system to respond differently to short compared with long-duration linear accelerations, consistent with their differing significance.     

Cross-Modal Calibration of Vestibular Afference for Human Balance

To determine how the vestibular sense controls balance, we used instantaneous head angular velocity to drive a galvanic vestibular stimulus so that afference would signal that head movement was faster or slower than actual. In effect, this changed vestibular afferent gain. This increased sway 4-fold when subjects (N = 8) stood without vision. However, after a 240 s conditioning period with stable balance achieved through reliable visual or somatosensory cues, sway returned to normal. An equivalent galvanic stimulus unrelated to sway (not driven by head motion) was equally destabilising but in this situation the conditioning period of stable balance did not reduce sway. Reflex muscle responses evoked by an independent, higher bandwidth vestibular stimulus were initially reduced in amplitude by the galvanic stimulus but returned to normal levels after the conditioning period, contrary to predictions that they would decrease after adaptation to increased sensory gain and increase after adaptation to decreased sensory gain. We conclude that an erroneous vestibular signal of head motion during standing has profound effects on balance control. If it is unrelated to current head motion, the CNS has no immediate mechanism of ignoring the vestibular signal to reduce its influence on destabilising balance. This result is inconsistent with sensory reweighting based on disturbances. The increase in sway with increased sensory gain is also inconsistent with a simple feedback model of vestibular reflex action. Thus, we propose that recalibration of a forward sensory model best explains the reinterpretation of an altered reafferent signal of head motion during stable balance.     

Galvanic vestibular stimulation improves the results of vestibular rehabilitation

Here, we present findings from a three-step investigation of the effect of galvanic vestibular stimulation (GVS) in normal subjects and in subjects undergoing vestibular rehabilitation (VR). In an initial study, we examined the body sway of 10 normal subjects after one minute of 2 mA GVS. The effect of the stimulation lasted for at least 20 minutes in all subjects and up to two hours in 70% of the subjects. We then compared a group of patients who received conventional VR (40 patients) with a group that received a combination of VR and GVS. Results suggest a significant improvement in the second group. Finally, we attempted to establish the optimal number of GVS sessions and to rule out a placebo effect. Fifteen patients received "systematic" GVS: five sessions, once a week. Five patients received "nonsystematic" galvanic stimulation in a sham protocol, which included two stimulations of the clavicle. These data were analyzed with Fisher's exact test and indicated that the best results were obtained after three sessions of GVS and no placebo effect was observed.     

Vestibulospinal influences on lower limb motoneurons

Galvanic vestibular stimulation (GVS) is a research tool used to activate the vestibular system in human subjects. When a low-intensity stimulus (1-4 mA) is delivered percutaneously to the vestibular nerve, a transient electromyographic response is observed a short time later in lower limb muscles. Typically, galvanically evoked responses are present when the test muscle is actively engaged in controlling standing balance. However, there is evidence to suggest that GVS may be able to modulate the activity of lower limb muscles when subjects are not in a free-standing situation. The purpose of this review is to examine 2 studies from our laboratory that examined the effects of GVS on the lower limb motoneuron pool. For instance, a monopolar monaural galvanic stimulus modified the amplitude of the ipsilateral soleus H-reflex. Furthermore, bipolar binaural GVS significantly altered the onset of activation and the initial firing frequency of gastrocnemius motor units. The following paper examines the effects of GVS on muscles that are not being used to maintain balance. We propose that GVS is modulating motor output by influencing the activity of presynaptic inhibitory mechanisms that act on the motoneuron pool.     

Central Adaptation to Repeated Galvanic Vestibular Stimulation: Implications for Pre-Flight Astronaut Training

Healthy subjects (N = 10) were exposed to 10-min cumulative pseudorandom bilateral bipolar Galvanic vestibular stimulation (GVS) on a weekly basis for 12 weeks (120 min total exposure). During each trial subjects performed computerized dynamic posturography and eye movements were measured using digital video-oculography. Follow up tests were conducted 6 weeks and 6 months after the 12-week adaptation period. Postural performance was significantly impaired during GVS at first exposure, but recovered to baseline over a period of 7–8 weeks (70–80 min GVS exposure). This postural recovery was maintained 6 months after adaptation. In contrast, the roll vestibulo-ocular reflex response to GVS was not attenuated by repeated exposure. This suggests that GVS adaptation did not occur at the vestibular end-organs or involve changes in low-level (brainstem-mediated) vestibulo-ocular or vestibulo-spinal reflexes. Faced with unreliable vestibular input, the cerebellum reweighted sensory input to emphasize veridical extra-vestibular information, such as somatosensation, vision and visceral stretch receptors, to regain postural function. After a period of recovery subjects exhibited dual adaption and the ability to rapidly switch between the perturbed (GVS) and natural vestibular state for up to 6 months.     

Dynamic Reweighting of Three Modalities for Sensor Fusion

We simultaneously perturbed visual, vestibular and proprioceptive modalities to understand how sensory feedback is re-weighted so that overall feedback remains suited to stabilizing upright stance. Ten healthy young subjects received an 80 Hz vibratory stimulus to their bilateral Achilles tendons (stimulus turns on-off at 0.28 Hz), a ±1 mA binaural monopolar galvanic vestibular stimulus at 0.36 Hz, and a visual stimulus at 0.2 Hz during standing. The visual stimulus was presented at different amplitudes (0.2, 0.8 deg rotation about ankle axis) to measure: the change in gain (weighting) to vision, an intramodal effect; and a change in gain to vibration and galvanic vestibular stimulation, both intermodal effects. The results showed a clear intramodal visual effect, indicating a de-emphasis on vision when the amplitude of visual stimulus increased. At the same time, an intermodal visual-proprioceptive reweighting effect was observed with the addition of vibration, which is thought to change proprioceptive inputs at the ankles, forcing the nervous system to rely more on vision and vestibular modalities. Similar intermodal effects for visual-vestibular reweighting were observed, suggesting that vestibular information is not a “fixed” reference, but is dynamically adjusted in the sensor fusion process. This is the first time, to our knowledge, that the interplay between the three primary modalities for postural control has been clearly delineated, illustrating a central process that fuses these modalities for accurate estimates of self-motion.     

An adaptive model of sensory integration in a dynamic environment applied to human stance control

An adaptive estimator model of human spatial orientation is presented. The adaptive model dynamically weights sensory error signals. More specific, the model weights the difference between expected and actual sensory signals as a function of environmental conditions. The model does not require any changes in model parameters. Differences with existing models of spatial orientation are that: (1) environmental conditions are not specified but estimated, (2) the sensor noise characteristics are the only parameters supplied by the model designer, (3) history-dependent effects and mental resources can be modelled, and (4) vestibular thresholds are not included in the model; instead vestibular-related threshold effects are predicted by the model. The model was applied to human stance control and evaluated with results of a visually induced sway experiment. From these experiments it is known that the amplitude of visually induced sway reaches a saturation level as the stimulus level increases. This saturation level is higher when the support base is sway referenced. For subjects experiencing vestibular loss, these saturation effects do not occur. Unknown sensory noise characteristics were found by matching model predictions with these experimental results. Using only five model parameters, far more than five data points were successfully predicted. Model predictions showed that both the saturation levels are vestibular related since removal of the vestibular organs in the model removed the saturation effects, as was also shown in the experiments. It seems that the nature of these vestibular-related threshold effects is not physical, since in the model no threshold is included. The model results suggest that vestibular-related thresholds are the result of the processing of noisy sensory and motor output signals. Model analysis suggests that, especially for slow and small movements, the environment postural orientation can not be estimated optimally, which causes sensory illusions. The model also confirms the experimental finding that postural orientation is history dependent and can be shaped by instruction or mental knowledge. In addition the model predicts that: (1) vestibular-loss patients cannot handle sensory conflicting situations and will fall down, (2) during sinusoidal support-base translations vestibular function is needed to prevent falling, (3) loss of somatosensory information from the feet results in larger postural sway for sinusoidal support-base translations, and (4) loss of vestibular function results in falling for large support-base rotations with the eyes closed. These predictions are in agreement with experimental results. Received: 12 November 1999 / Accepted in revised form: 30 June 2000     

Vestibular postural control model

Current models for physiological components and a posture control experiment conducted with three normal subjects form the basis for a model which seeks to describe quantitatively the control of body sway when only vestibular motion cues are used. Emphasis is placed on delineating the relative functional roles of the linear and the angular acceleration sensors and on modeling the functional interface between these sensors and the initiation of compensatory responses at the ankle joint.The model predicts the form of the postural response to a small sway disturbance; including initial detection of sway, characteristics of the transient correction, and maintenance of stability. The model suggests that postural stability requires a short time constant integration of semicircular canal output. Separation of semicircular canal and utricular otolith function into sway motion detector and static reference sensors respectively is demonstrated.This work was supported by NASA under Grant NGR-22-009-156.     

Effects of Near-Threshold Stimulation of the Vestibular Apparatus on Postural Responses Evoked by Displacements of the Visualized Surrounding

In healthy subjects in the relaxed upward stance and perceiving a virtual visual environment (VVE), we recorded postural reactions to isolated visual and vestibular stimulations or their combinations. Lateral displacements of the visualized virtual scene were used as visual stimuli. The vestibular apparatus was stimulated by application of near-threshold galvanic current pulses to the proc. mastoidei of the temporal bones. Isolated VVE shifts evoked mild, nonetheless clear, body tilts readily distinguished in separate trials; at the same time, postural effects of isolated vestibular stimulation could be detected only after averaging of several trials synchronized with respect to the beginning of stimulation. Under conditions of simultaneous combined presentation of visual and vestibular stimuli, the direction of the resulting postural responses always corresponded to the direction of responses induced by VVE shifts. The contribution of an afferent volley from the vestibular organ depended on the coincidence/mismatch of the direction of motor response evoked by such a volley with the direction of response to visual stimulation. When both types of stimulations evoked unidirectional body tilts, postural responses were facilitated, and the resulting effect was greater than that of simple summation of the reactions to isolated actions of the above stimuli. In the case where isolated galvanic stimulation evoked a response opposite with respect to that induced by visual stimulation, the combined action of these stimuli of different modalities evoked postural responses identical in their magnitude, direction, and shape to those evoked by isolated visual stimulation. The above findings allow us to conclude that the effects of visual afferent input on the vertical posture under conditions of our experiments clearly dominate. In general, these results confirm the statement that neuronal structures involved in integrative processing of different afferent volleys preferably select certain type of afferentation carrying more significant or more detailed information on displacements (including oscillations) of the body in space.     

Velocity of head movements and sensory-motor adaptation during and after short spaceflight

To investigate to time course of sensory-motor adaptation to microgravity, we tested spatially-directed voluntary head movements before, during and after short spaceflight. We also tested the re-adaptation of postural responses to sensory stimulation after space flight. The cosmonaut performed in microgravity six cycles of voluntary head rotation in pitch, roll and yaw directions. During the first days of weightlessness the angular velocity of head movements increased. Over the next days of microgravity the velocity of head movements gradually decreased. On landing day a significant decrease of head rotation velocity was observed compared to the head movement velocity before spaceflight. Re-adaptation to Earth condition measured by body sway on soft support showed similar time course, but re-adaptation measured by postural responses to vestibular galvanic stimulation was prolonged. These results showed that the angular velocity of aimed head movements of cosmonauts is a good indicator of sensory-motor adaptation in altered gravity conditions.     

Frequency dependence of the action-perception cycle for postural control in a moving visual environment: relative phase dynamics

When standing human subjects are exposed to a moving visual environment, the induced postural sway displays varying degrees of coherence with the visual information. In our experiment we varied the frequency of an oscillatory visual display and analysed the temporal relationship between visual motion and sway. We found that subjects maintain sizeable sway amplitudes even as temporal coherence with the display is lost. Postural sway tended to phase lead (for frequencies below 0.2 Hz) or phase lag (above 0.3 Hz). However, we also observed at a fixed frequency, highly variable phase relationships in which a preferred range of phase lags is prevalent, but phase jumps occur that return the system into the preferred range after phase has begun drifting out of the preferred regime. By comparing the results quantitatively with a dynamical model (the sine-circle map), we show that this effect can be understood as a form of relative coordination and arises through an instability of the dynamics of the action-perception cycle. Because such instabilities cannot arise in passively driven systems, we conclude that postural sway in this situation is actively generated as rhythmic movement which is coupled dynamically to the visual motion. Received: 7 September 1993/Accepted in revised form: 2 May 1994     

Multi-stimulus multi-response posturography

In this study a method for the analysis of simultaneous multiple measurements of kinematics and stabilizing forces related to human postural dynamics is proposed. Each subject in a group of normal subjects (n=10) was tested with eyes-open and eyes-closed with simultaneous but uncorrelated vestibular and proprioceptive stimuli in order to investigate the contributions of individual sensory feedback loops. Statistical analysis was made by means of multi-input multi-output identification of a transfer function from stimuli to stabilizing forces of the feet and the resulting body position, the transfer function being compatible with a biomechanical model formulated as a stabilized segmented inverted pendulum subject to feedback of body sway and position. Each individual model estimated is effective in predicting a subject's response to new stimuli and in describing the interacting effects of stimuli on body kinetics. The proposed methodology responds to the current needs of data analysis of multi-stimulus multi-response experiments.     

Vestibular and somatosensory interaction during recovery of balance instability after spaceflight

The aim of our contribution was to characterize vestibular and somatosensory influence on human balance recovery during readaptation to the earth conditions after spaceflight. We tested how post-spaceflight postural reactions to galvanic stimulus (related to vestibular input) and to vibration of the lower leg muscles (somatosensory input) were changed.     

Characteristics of postural corrective responses before and after long-term spaceflights

Balance function is dramatically deteriorated after exposure to microgravity. The purpose of the present study was to investigate the role and the contribution of different gravity sensory systems to the development of balance impairment after long-term spaceflights. Postural perturbations (pushes to the chest) of the threshold, medium, and sub-maximal intensities were produced in eight cosmonauts before, and on the day 3, 7, and 11 following spaceflight. Postural corrective responses were analyzed by anterior-posterior body sway fluctuation and electromyographic activity of leg muscles. The characteristics of the postural corrective responses changed significantly on the day 3 following spaceflight: the amplitude of posterior sway caused by perturbation of threshold intensity was increased reaching 135% of preflight value; the corrective responses lasted more than 6 s in 50% of all trials, while it did not last more than 4 s in 96% before spaceflight. The EMG responses were characterized by increased contribution of medium- and long-latency reactions. On the day 11 following spaceflight, most of the characteristics of postural corrective responses were close to preflight values. We assumed that the balance alterations after spaceflight are caused by changes in weightlessness of functions of two main gravity sensory systems, namely, weight-bearing and vestibular one. The deficit of weight-bearing afferentation triggers a decline of the extensors’ muscle tone, while changes of vestibular function cause a decline of accuracy of postural corrections.     

Stance stability with unilateral and bilateral light touch of an external stationary object

Unilateral light fingertip touch of a stationary object has a significant stabilizing effect on postural sway during stance. The purpose of this study was to find out if this effect is enhanced by bilateral light touch of parallel stationary objects. The postural sway of 54 healthy subjects was tested in four stance conditions: no touch; unilateral left light touch of the left handle of a walker; unilateral right light touch of the right handle of the same walker; and bilateral light touch of the two handles. During testing, subjects stood blindfolded on two foam pads placed on the left and right force plates of the Tetrax balance system. Testing in each condition lasted 45 s and was executed twice in a random order. As expected, postural sway was significantly reduced by unilateral left or right light fingertip touch. It was significantly further decreased by bilateral light touch. In addition, light touch conditions were associated with a reduction in pressure fluctuations between the heel and forefoot of the same foot as well as those of the contralateral foot, with a concomitant increase in weight shift fluctuations between the two feet. The decrease in postural sway with bilateral light touch suggests cortical modulation of the bilateral touch inputs, with enhancement of the stabilizing response.     

Modeling postural control in the lamprey

 A phenomenological model of the mechanism of stabilization of the body orientation during locomotion (dorsal side up) in the lamprey is presented. The mathematical modeling is based on experimental results obtained during investigations of postural control in lampreys using a combined in vivo and robotics approach. The dynamics of the model agree qualitatively with the experimental data. It is shown by computer simulations that postural correction commands from reticulospinal neurons provide information sufficient to stabilize body orientation in the lamprey. The model is based on differences between the effects exerted by the vestibular apparatus on the left and the right side. Received: 16 February 2000 / Accepted in revised form: 29 September 2000