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.     

Enhancing human balance control with galvanic vestibular stimulation

 With galvanic vestibular stimulation (GVS), electrical current is delivered transcutaneously to the vestibular afferents through electrodes placed over the mastoid bones. This serves to modulate the continuous firing levels of the vestibular afferents, and causes a standing subject to lean in different directions depending on the polarity of the current. Our objective in this study was to test the hypothesis that the sway response elicited by GVS can be used to reduce the postural sway resulting from a mechanical perturbation. Nine subjects were tested for their postural responses to both galvanic stimuli and support-surface translations. Transfer-function models were fit to these responses and used to calculate a galvanic stimulus that would act to counteract sway induced by a support-surface translation. The subjects' responses to support-surface translations, without and with the stabilizing galvanic stimulus, were then measured. With the stabilizing galvanic stimulus, all subjects showed significant reductions in both sway amplitude and sway latency. Thus, with GVS, subjects maintained a more erect stance and followed the support-surface displacement more closely. These findings suggest that GVS could possibly form the basis for a vestibular prosthesis by providing a means through which an individual's posture can be systematically controlled. Received: 11 May 2000 / Accepted in revised form: 20 November 2000     

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.     

The Vestibular-Evoked Postural Response of Adolescents with Idiopathic Scoliosis Is Altered

Adolescent idiopathic scoliosis is a multifactorial disorder including neurological factors. A dysfunction of the sensorimotor networks processing vestibular information could be related to spine deformation. This study investigates whether feed-forward vestibulomotor control or sensory reweighting mechanisms are impaired in adolescent scoliosis patients. Vestibular evoked postural responses were obtained using galvanic vestibular stimulation while participants stood with their eyes closed and head facing forward. Lateral forces under each foot and lateral displacement of the upper body of adolescents with mild (n = 20) or severe (n = 16) spine deformation were compared to those of healthy control adolescents (n = 16). Adolescent idiopathic scoliosis patients demonstrated greater lateral displacement and net lateral forces than controls both during and immediately after vestibular stimulation. Altered sensory reweighting of vestibular and proprioceptive information changed balance control of AIS patients during and after vestibular stimulation. Therefore, scoliosis onset could be related to abnormal sensory reweighting, leading to altered sensorimotor processes.     

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.     

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.     

Vestibular reafference shapes voluntary movement

The vestibular organs in the inner ear are commonly thought of as sensors that serve balance, gaze control, and higher spatial functions such as navigation. Here, we investigate their role in the online control of voluntary movements. The central nervous system uses sensory feedback information during movement to detect and correct errors as they develop. Vestibular organs signal three-dimensional head rotations and translations and so could provide error information for body movements that transport the head in space. To test this, we electrically stimulated human vestibular nerves during a goal-directed voluntary tilt of the trunk. The stimulating current waveform was made identical to the angular velocity profile of the head in the roll plane. With this, we could proportionally increase or decrease the rate of vestibular nerve firing, as if the head were rotating faster or slower than it actually was. In comparison to movements performed without stimulation, subjects tilted their trunk faster and further or slower and less far, depending upon the polarity of the stimulus. The response was negligible when identical stimulus waveforms were replayed to stationary subjects. We conclude that the brain uses vestibular information for online error correction of planned body-movement trajectories.     

Exercise and dehydration: A possible role of inner ear in balance control disorder

To study the effect of exercise and dehydration on the postural sensory-motor strategies, 10 sportsmen performed a 45 min-exercise on a cycle ergometer at intensity just below the ventilatory threshold without fluid intake. They performed, before, immediately and 20 min after exercise, a sensory organization test to evaluate balance control in six different sensory situations, that combine three visual conditions (eyes open, eyes closed and sway-referenced visual surround motion) with two platform conditions (stable platform, sway-referenced platform motion). Blood samples were collected before and after exercise. Exercise induced a mild dehydration, characterized by body mass loss and increase in proteinemia. Postural performances decreased immediately after exercise, mainly in the standard situation (eyes open, stable visual surround and platform) and when only the vestibular cue was reliable (eyes closed and sway-referenced platform). Moreover, the decreased use of vestibular input was correlated with the dehydration level. Finally, postural performances normalized 20 min after exercise. Even though muscular fatigue could explain the decrease in postural performances, vestibular fluid modifications may also be involved by its influence on the intralabyrinthine homeostasis, lowering thus the contribution of vestibular information on balance control.     

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.     

Navigating sensory conflict in dynamic environments using adaptive state estimation

Most conventional robots rely on controlling the location of the center of pressure to maintain balance, relying mainly on foot pressure sensors for information. By contrast, humans rely on sensory data from multiple sources, including proprioceptive, visual, and vestibular sources. Several models have been developed to explain how humans reconcile information from disparate sources to form a stable sense of balance. These models may be useful for developing robots that are able to maintain dynamic balance more readily using multiple sensory sources. Since these information sources may conflict, reliance by the nervous system on any one channel can lead to ambiguity in the system state. In humans, experiments that create conflicts between different sensory channels by moving the visual field or the support surface indicate that sensory information is adaptively reweighted. Unreliable information is rapidly down-weighted, then gradually up-weighted when it becomes valid again. Human balance can also be studied by building robots that model features of human bodies and testing them under similar experimental conditions. We implement a sensory reweighting model based on an adaptive Kalman filter in a bipedal robot, and subject it to sensory tests similar to those used on human subjects. Unlike other implementations of sensory reweighting in robots, our implementation includes vision, by using optic flow to calculate forward rotation using a camera (visual modality), as well as a three-axis gyro to represent the vestibular system (non-visual modality), and foot pressure sensors (proprioceptive modality). Our model estimates measurement noise in real time, which is then used to recompute the Kalman gain on each iteration, improving the ability of the robot to dynamically balance. We observe that we can duplicate many important features of postural sway in humans, including automatic sensory reweighting, effects, constant phase with respect to amplitude, and a temporal asymmetry in the reweighting gains.     

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.     

The Influence of Diabetic Peripheral Neuropathy on Local Postural Muscle and Central Sensory Feedback Balance Control

Poor balance control and increased fall risk have been reported in people with diabetic peripheral neuropathy (DPN). Traditional body sway measures are unable to describe underlying postural control mechanism. In the current study, we used stabilogram diffusion analysis to examine the mechanism under which balance is altered in DPN patients under local-control (postural muscle control) and central-control (postural control using sensory cueing). DPN patients and healthy age-matched adults over 55 years performed two 15-second Romberg balance trials. Center of gravity sway was measured using a motion tracker system based on wearable inertial sensors, and used to derive body sway and local/central control balance parameters. Eighteen DPN patients (age = 65.4±7.6 years; BMI = 29.3±5.3 kg/m²) and 18 age-matched healthy controls (age = 69.8±2.9; BMI = 27.0±4.1 kg/m²) with no major mobility disorder were recruited. The rate of sway within local-control was significantly higher in the DPN group by 49% (healthy local-control_slope = 1.23±1.06×10^-2 cm²/sec, P<0.01), which suggests a compromised local-control balance behavior in DPN patients. Unlike local-control, the rate of sway within central-control was 60% smaller in the DPN group (healthy central-control_slope-Log = 0.39±0.23, P<0.02), which suggests an adaptation mechanism to reduce the overall body sway in DPN patients. Interestingly, significant negative correlations were observed between central-control rate of sway with neuropathy severity (r _Pearson = 0.65-085, P<0.05) and the history of diabetes (r _Pearson = 0.58-071, P<0.05). Results suggest that in the lack of sensory feedback cueing, DPN participants were highly unstable compared to controls. However, as soon as they perceived the magnitude of sway using sensory feedback, they chose a high rigid postural control strategy, probably due to high concerns for fall, which may increase the energy cost during extended period of standing; the adaptation mechanism using sensory feedback depends on the level of neuropathy and the history of diabetes.     

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

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% ofpreflight 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.     

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.     

Relationship between Spectral Characteristics of Spontaneous Postural Sway and Motion Sickness Susceptibility

Motion sickness (MS) usually occurs for a narrow band of frequencies of the imposed oscillation. It happens that this frequency band is close to that which are spontaneously produced by postural sway during natural stance. This study examined the relationship between reported susceptibility to motion sickness and postural control. The hypothesis is that the level of MS can be inferred from the shape of the Power Spectral Density (PSD) profile of spontaneous sway, as measured by the displacement of the center of mass during stationary, upright stance. In Experiment 1, postural fluctuations while standing quietly were related to MS history for inertial motion. In Experiment 2, postural stability measures registered before the onset of a visual roll movement were related to MS symptoms following the visual stimulation. Study of spectral characteristics in postural control showed differences in the distribution of energy along the power spectrum of the antero-posterior sway signal. Participants with MS history provoked by exposure to inertial motion showed a stronger contribution of the high frequency components of the sway signal. When MS was visually triggered, sick participants showed more postural sway in the low frequency range. The results suggest that subject-specific PSD details may be a predictor of the MS level. Furthermore, the analysis of the sway frequency spectrum provided insight into the intersubject differences in the use of postural control subsystems. The relationship observed between MS susceptibility and spontaneous posture is discussed in terms of postural sensory weighting and in relation to the nature of the provocative stimulus.     

Shifts in coding properties and maintenance of information transmission during adaptation in barrel cortex

Neuronal responses to ongoing stimulation in many systems change over time, or “adapt.” Despite the ubiquity of adaptation, its effects on the stimulus information carried by neurons are often unknown. Here we examine how adaptation affects sensory coding in barrel cortex. We used spike-triggered covariance analysis of single-neuron responses to continuous, rapidly varying vibrissa motion stimuli, recorded in anesthetized rats. Changes in stimulus statistics induced spike rate adaptation over hundreds of milliseconds. Vibrissa motion encoding changed with adaptation as follows. In every neuron that showed rate adaptation, the input–output tuning function scaled with the changes in stimulus distribution, allowing the neurons to maintain the quantity of information conveyed about stimulus features. A single neuron that did not show rate adaptation also lacked input–output rescaling and did not maintain information across changes in stimulus statistics. Therefore, in barrel cortex, rate adaptation occurs on a slow timescale relative to the features driving spikes and is associated with gain rescaling matched to the stimulus distribution. Our results suggest that adaptation enhances tactile representations in primary somatosensory cortex, where they could directly influence perceptual decisions.     

Noisy Galvanic Vestibular Stimulation Modulates the Amplitude of EEG Synchrony Patterns

Noisy galvanic vestibular stimulation has been associated with numerous cognitive and behavioural effects, such as enhancement of visual memory in healthy individuals, improvement of visual deficits in stroke patients, as well as possibly improvement of motor function in Parkinson’s disease; yet, the mechanism of action is unclear. Since Parkinson’s and other neuropsychiatric diseases are characterized by maladaptive dynamics of brain rhythms, we investigated whether noisy galvanic vestibular stimulation was associated with measurable changes in EEG oscillatory rhythms within theta (4–7.5 Hz), low alpha (8–10 Hz), high alpha (10.5–12 Hz), beta (13–30 Hz) and gamma (31–50 Hz) bands. We recorded the EEG while simultaneously delivering noisy bilateral, bipolar stimulation at varying intensities of imperceptible currents – at 10, 26, 42, 58, 74 and 90% of sensory threshold – to ten neurologically healthy subjects. Using standard spectral analysis, we investigated the transient aftereffects of noisy stimulation on rhythms. Subsequently, using robust artifact rejection techniques and the Least Absolute Shrinkage Selection Operator regression and cross-validation, we assessed the combinations of channels and power spectral features within each EEG frequency band that were linearly related with stimulus intensity. We show that noisy galvanic vestibular stimulation predominantly leads to a mild suppression of gamma power in lateral regions immediately after stimulation, followed by delayed increase in beta and gamma power in frontal regions approximately 20–25 s after stimulation ceased. Ongoing changes in the power of each oscillatory band throughout frontal, central/parietal, occipital and bilateral electrodes predicted the intensity of galvanic vestibular stimulation in a stimulus-dependent manner, demonstrating linear effects of stimulation on brain rhythms. We propose that modulation of neural oscillations is a potential mechanism for the previously-described cognitive and motor effects of vestibular stimulation, and noisy galvanic vestibular stimulation may provide an additional non-invasive means for neuromodulation of functional brain networks.     

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     

Velocity of body lean evoked by leg muscle vibration potentiate the effects of vestibular stimulation on posture

To investigate the vestibular and somatosensory interaction in human postural control, a galvanic vestibular stimulation of cosine bell shape resulting in a small forward or backward body lean was paired with three vibrations of both soleus muscles. The induced body lean was registered by the position of the center of foot pressure (CoP). During a quiet stance with eyes closed the vibration of both soleus muscles with frequency (of) 40 Hz, 60 Hz and 80 Hz resulted in the body lean backward with velocities related to the vibration frequencies. The vestibular galvanic stimulation with the head turned to the right caused forward or backward modification of CoP backward response to the soleus muscles vibration and peaked at 1.5-2 s following the onset of the vibration. The effect of the paired stimulation was larger than the summation of the vestibular stimulation during the quiet stance and a leg muscle vibration alone. The enhancement of the galvanic stimulation was related to the velocity of body lean induced by the leg muscle vibration. The galvanic vestibular stimulation during a faster body movement had larger effects than during a slow body lean or the quiet stance. The results suggest that velocity of a body postural movement or incoming proprioceptive signal from postural muscles potentiate the effects of simultaneous vestibular stimulations on posture.     

Multisensory Interactions between Vestibular,Visual and Somatosensory Signals

Vestibular inputs are constantly processed and integrated with signals from other sensory modalities, such as vision and touch. The multiply-connected nature of vestibular cortical anatomy led us to investigate whether vestibular signals could participate in a multi-way interaction with visual and somatosensory perception. We used signal detection methods to identify whether vestibular stimulation might interact with both visual and somatosensory events in a detection task. Participants were instructed to detect near-threshold somatosensory stimuli that were delivered to the left index finger in one half of experimental trials. A visual signal occurred close to the finger in half of the trials, independent of somatosensory stimuli. A novel Near infrared caloric vestibular stimulus (NirCVS) was used to artificially activate the vestibular organs. Sham stimulations were used to control for non-specific effects of NirCVS. We found that both visual and vestibular events increased somatosensory sensitivity. Critically, we found no evidence for supra-additive multisensory enhancement when both visual and vestibular signals were administered together: in fact, we found a trend towards sub-additive interaction. The results are compatible with a vestibular role in somatosensory gain regulation.