Sensory processing in the vestibular nuclei during active head movements

Many secondary vestibular neurons are sensitive to head on trunk rotation during reflex-induced and voluntary head movements. During passive whole body rotation the interaction of head on trunk signals related to the vestibulo-collic reflex with vestibular signals increases the rotational gain of many secondary vestibular neurons, including many that project to the spinal cord. In some units, the sensitivity to head on trunk and vestibular input is matched and the resulting interaction produces an output that is related to the trunk velocity in space. In other units the head on trunk inputs are stronger and the resulting interaction produces an output that is larger during the reflex. During voluntary head movements, inputs related to head on trunk movement combine destructively with vestibular signals, and often cancel the sensory reafferent consequences of self-generated movements. Cancellation of sensory vestibular signals was observed in all of the antidromically identified secondary vestibulospinal units, even though many of these units were not significantly affected by reflexive head on trunk movements. The results imply that the inputs to vestibular neurons related to head on trunk rotation during reflexive and voluntary movements arise from different sources. We suggest that the relative strength of reflexive head on trunk input to different vestibular neurons might reflect the different functional roles they have in controlling the posture of the neck and body.     

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.     

Directional sensitivity of velocity sense in the lumbar spine

Regulating spinal motion requires proprioceptive feedback. While studies have investigated the sensing of static lumbar postures, few have investigated sensing lumbar movement speed. In this study, proprioceptive contributions to lateral trunk motion were examined during paraspinal muscle vibration. Seventeen healthy subjects performed lateral trunk flexion movements while lying prone with pelvis fixed. A 44.5-Hz vibratory stimulus was applied to the paraspinal muscles at the L3 level. Subjects attempted to match target paces of 9.5, 13.5, and 17.5 deg/s with and without paraspinal muscle vibration. Vibration of the paraspinal musculature was found to result in slower overall lateral flexion. This effect was found to have a greater influence in the difference of directional velocities with vibration applied to the left musculature. These changes reflect the sensitivity of lumbar velocity sense to applied vibration leading to the perception of faster muscle lengthening and ultimately resulting in slower movement velocities. This suggests that muscle spindle organs modulate the ability to sense velocity of motion and are important in the control of dynamic motion of the spine.     

Action representation in patients with bilateral vestibular impairments

During mental actions subjects feel themselves performing a movement without any corresponding motor output. Although broad information is available regarding the influence of central lesions on action representation, little is known about how peripheral damages affect mental events. In the current study, we investigated whether lack of vestibular information influences action representation. Twelve healthy adults and twelve patients with bilateral vestibular damage actually performed and mentally simulated walking and drawing. The locomotor paths implied one (first walking task) and four (second walking task) changes in the walking direction. In the drawing task, participants drew on a sheet of paper a path that was similar to that of the second walking task. We recorded and compared between the two groups the timing of actual and mental movements. We found significant temporal discrepancies between actual and mental walking movements in the group of patients. Conversely, drawing actual and drawing mental durations were similar. For the control group, an isochrony between mental and actual movements was observed for the three tasks. This result denotes an inconsistency between action representation and action execution following vestibular damage, which is specific to walking movements, and emphasizes the role of the vestibular system upon mental states of actions. This observation may have important clinical implications. During action planning vestibular patients may overestimate the capacity of their motor system (imaging faster, executing slower) with harmful consequences for their health.     

Head Movements Evoked in Alert Rhesus Monkey by Vestibular Prosthesis Stimulation: Implications for Postural and Gaze Stabilization

The vestibular system detects motion of the head in space and in turn generates reflexes that are vital for our daily activities. The eye movements produced by the vestibulo-ocular reflex (VOR) play an essential role in stabilizing the visual axis (gaze), while vestibulo-spinal reflexes ensure the maintenance of head and body posture. The neuronal pathways from the vestibular periphery to the cervical spinal cord potentially serve a dual role, since they function to stabilize the head relative to inertial space and could thus contribute to gaze (eye-in-head + head-in-space) and posture stabilization. To date, however, the functional significance of vestibular-neck pathways in alert primates remains a matter of debate. Here we used a vestibular prosthesis to 1) quantify vestibularly-driven head movements in primates, and 2) assess whether these evoked head movements make a significant contribution to gaze as well as postural stabilization. We stimulated electrodes implanted in the horizontal semicircular canal of alert rhesus monkeys, and measured the head and eye movements evoked during a 100ms time period for which the contribution of longer latency voluntary inputs to the neck would be minimal. Our results show that prosthetic stimulation evoked significant head movements with latencies consistent with known vestibulo-spinal pathways. Furthermore, while the evoked head movements were substantially smaller than the coincidently evoked eye movements, they made a significant contribution to gaze stabilization, complementing the VOR to ensure that the appropriate gaze response is achieved. We speculate that analogous compensatory head movements will be evoked when implanted prosthetic devices are transitioned to human patients.     

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.     

Integrative responses of neurons in nucleus tractus solitarius to visceral afferent stimulation and vestibular stimulation in vertical planes

Anatomical studies have demonstrated that the vestibular nuclei project to nucleus tractus solitarius (NTS), but little is known about the effects of vestibular inputs on NTS neuronal activity. Furthermore, lesions of NTS abolish vomiting elicited by a variety of different triggering mechanisms, including vestibular stimulation, suggesting that emetic inputs may converge on the same NTS neurons. As such, an emetic stimulus that activates gastrointestinal (GI) receptors could alter the responses of NTS neurons to vestibular inputs. In the present study, we examined in decerebrate cats the responses of NTS neurons to rotations of the body in vertical planes before and after the intragastric administration of the emetic compound copper sulfate. The activity of more than one-third of NTS neurons was modulated by vertical vestibular stimulation, with most of the responsive cells having their firing rate altered by rotations in the head-up or head-down directions. These responses were aligned with head position in space, as opposed to the velocity of head movements. The activity of NTS neurons with baroreceptor, pulmonary, and GI inputs could be modulated by vertical plane rotations. However, injection of copper sulfate into the stomach did not alter the responses to vestibular stimulation of NTS neurons that received GI inputs, suggesting that the stimuli did not have additive effects. These findings show that the detection and processing of visceral inputs by NTS neurons can be altered in accordance with the direction of ongoing movements.     

Analysis of the middle latency evoked potentials to angular acceleration impulses in man

The middle latency vestibular evoked potential (ML-VsEP) recorded with scalp electrodes in man in response to impulses of angular acceleration is dominated by a forehead positive peak at about 15 ms and a negative peak at about 20 ms; the peak amplitude of this component is about 30 μV. This is followed by slower, smaller amplitude activity. The latency of this initial peak is similar to the latency of the vestibulo-ocular reflex (VOR) in monkeys. The present study was undertaken to elucidate the possible relation between the ML-VsEPs and VOR. This included recordings from forehead-mastoid electrodes (sites used to record VsEP) and other scalp electrodes and the recording of potentials due to eye movement: the electro-oculogram. Direct recording of eye movements was also conducted using an infra-red reflection device in those experiments in which the head was not moved. The recordings were conducted in man during vestibular stimulation eliciting VsEPs, during voluntary eye movements and during caloric and optokinetic stimulation. These experiments indicated that the 15–20 ms component of the ML-VsEP was not due to movements of the eye (corneoretinal dipole). The large amplitude 15–20 ms component of the ML-VsEP was similar in general magnitude, waveform, polarity, duration and rise time to the highly synchronous pre-saccadic spike (neural and/or myogenic) which precedes nystagnys and voluntary saccades. It therefore probably represents vestibular-initiated electrical activity in motor units of the extra-ocular muscles which then produce anti-compensatory saccades.     

On the predominance of anti-compensatory eye movements in vestibular nystagmus

The predominance of anti-compensatory eye movements in vestibular nystagmus recorded during sinusoidal and post-rotational tests is interpreted in terms of a mathematical model of the vestibulo-ocular system. Namely, a direct pathway between the vestibular nuclei and the saccadic mechanism is assumed. In the range of frequencies of natural head movements this pathway carries on a signal proportional to head angular velocity. Therefore, during active head movements the saccadic mechanism is forced to produce quick eye rotations in the direction of head movement and, thus, to cooperate in the task of picking up visual targets outside the visual field. During passive head movements giving rise to nystagmus the assumed pathway contributes to reduce the error in eye resetting due to the saccadic delay. Analytical considerations and simulation results seem to prove the adequacy of the proposed model.Work supported by the National Research Council (C.N.R.), Rome, Italy     

Artificial vestibular feedback in conditions of modified body scheme

Subjects standing in darkness on the rigid support, kept a vertical posture which was destabilized by vibration of the Achilles tendons. To create a feedback on the vestibular input, transmastoidal bipolar galvanic stimulation was used. Changes of current in the feedback contour looked as linear function considering amplitude and velocity of the subject's head displacements in reference to the vertical. To change the body scheme we used some posture configurations: turning of the head in relation to the trunk; turning of the trunk with the head fixed; joint turning of the head and trunk. As a result of these configurations, the head could be turned approximately at right angle in relation to the feet. In addition turning of one foot at right angle in relation to the other foot was used. Artificial feedback reduces body fluctuations caused by vibration only in the vertical plane which passes through interaural axis of the head. The authors assume that directional changes of vestibulo-motor responses and results of application of artificial feedback during changes of orientation of the head in relation to the feet can be connected to change of ensembles of vestibular hair cells, which signals dominate in responses of vestibulo-spinal neurones.     

A sustained hyper-g load as a tool to simulate space sickness

In April 1989 the three European scientist astronauts of the D1 Spacelab Mission were exposed to a 1.5 hours +3G centrifuge run in supine position, resulting in a linear acceleration along the subjects' x-axis. Afterwards, severe motion sickness symptoms were provoked by head movements (Sickness Induced by Centrifugation: SIC). The astronauts mentioned close similarities with what they experienced in space during the D1-Spacelab Mission in 1985, where head movements also provoked motion sickness symptoms (Space Adaptation Syndrome: SAS). Moreover, the astronauts agreed that the rank order of their susceptibility to SAS was the same as for SIC. It was therefore postulated that with this method SAS could be simulated on earth. Additionally, in otolith function tests following the centrifuge run, changes in visual-vestibular interaction were observed, which replicated objective findings obtained with the same astronauts immediately after the D1 Spacelab Mission. During the last couple of years a series of experiments has been carried out to determine the nature of the stimulus causing SIC, the incidence of SIC, and the underlying cardio-vascular and/or vestibular mechanisms. These experiments were carried out on several astronauts and some 50 'normal' healthy subjects. In the next sections the main findings of all these experiments and the implications are summarized.     

Computation of trunk equilibrium and stability in free flexion-extension movements at different velocities

Velocity of movement has been suggested as a risk factor for low-back disorders. The effect of changes in velocity during unconstrained flexion-extension movements on muscle activations, spinal loads, base reaction forces and system stability was computed. In vivo measurements of kinematics and ground reaction forces were initially carried out on young asymptomatic subjects. The collected kinematics of three subjects representing maximum, mean and minimum lumbar rotations were subsequently used in the kinematics-driven model to compute results during the entire movements at three different velocities. Estimated spinal loads and muscle forces were significantly larger in fastest pace as compared to slower ones indicating the effect of inertial forces. Spinal stability was improved in larger trunk flexion angles and fastest movement. Partial or full flexion relaxation of global extensor muscles occurred only in slower movements. Some local lumbar muscles, especially in subjects with larger lumbar flexion and at slower paces, also demonstrated flexion relaxation. Results confirmed the crucial role of movement velocity on spinal biomechanics. Predictions also demonstrated the important role on response of the magnitude of peak lumbar rotation and its temporal variation.     

Behavior of the oculomotor neurons discharge during sinusoidal lateral tilt in the rabbit

The characteristics of the control exerted by macular and ampullar vestibular receptors on oculomotor neurons (OMN) have been investigated by submitting unanesthetized, encéphale isolé rabbits to sinusoidal lateral tilts of varying frequencies (0.013-0.2 Hz). The phase of the response exhibited a progressive shift towards head velocity with increasing frequencies of tilt. The sensitivity of the OMN significantly increased at frequencies above 0.025 Hz, corresponding to peak accelerations suprathreshold for canals related vestibular neurons. The convergent action of macular and ampullar vestibular receptors in the control of vertical eye movements is discussed in relation with stimulus frequency.     

Spatial updating in human parietal cortex

Single neurons in monkey parietal cortex update visual information in conjunction with eye movements. This remapping of stimulus representations is thought to contribute to spatial constancy. We hypothesized that a similar process occurs in human parietal cortex and that we could visualize it with functional MRI. We scanned subjects during a task that involved remapping of visual signals across hemifields. We observed an initial response in the hemisphere contralateral to the visual stimulus, followed by a remapped response in the hemisphere ipsilateral to the stimulus. We ruled out the possibility that this remapped response resulted from either eye movements or visual stimuli alone. Our results demonstrate that updating of visual information occurs in human parietal cortex.     

Analysis of surface wave direction by the lateral line system of Xenopus: Source localization before and after inactivation of different parts of the lateral line

The turning responses of clawed toads (Xenopus laevis) to surface waves were examined in animals with an intact lateral line or with different combinations of lateral lines reversibly inactivated by CoCl₂. The responses were characterized with respect to response frequency, turning accuracy, turning side, response time, and swim distance. After the inactivation most animals still responded to surface waves but the responses were different from those of animals with an intact lateral line. They also differed according to the combination of inactivated lines. In all experiments the responses for stimuli in some sectors of the surface did not differ from controls. The location of these sectors co-varied with the position of the intact lines, i.e., normal responses were found for frontal stimulus directions when head lines were intact and for caudolateral stimulus directions when trunk lines were intact. Their size was larger when lines on both sides of the body were intact and smaller when only lines on one side were intact. When the number of functional lines was reduced to one or two on one side of the body the turning angles shown within the sector of normal responses were maintained for stimulus directions outside these sectors. These results can be interpreted as indicating that head and trunk lines represent different position values. When only a single line was functional the toads still turned towards the stimulus source more often than by chance.It is hypothesized that Xenopus uses two mechanisms to determine the direction of surface waves. One uses the position values of head and trunk lines; this mechanism is comparable to the place value postulated for individual head neuromasts of surface feeding fish. The other uses the information encoded in the activity pattern that is elicited in one line when the surface wave travels over the line. This second mechanism yields information about stimulus side but not about stimulus angle.     

Initial ventilatory and circulatory responses to dynamic exercise are slowed in the elderly.

To elucidate the characteristics of ventilatory and circulatory responses at the onset of brief and light exercise in the elderly, 13 healthy, elderly men, aged 66.8 yr (mean), exerted bilateral leg extension-flexion movements for only 20 s with a weight around each ankle, with each weight being approximately 2.5% of their body mass. Similar movements were passively performed on the subjects by the experimenters. These results were compared with those of 13 healthy, young men (22.9 yr). Minute ventilation increased at the onset of voluntary exercise and passive movements in both groups but showed a slower increase in the elderly. Heart rate also increased in both groups but showed less change in the elderly. Mean blood pressure temporarily decreased in both groups but less in the elderly. The magnitude of relative change (gain) of heart rate in the elderly was significantly smaller than that in the young, whereas the increasing rate to reach one-half of the gain (response time) of ventilation in the elderly was significantly slower than that in the young. Similar tendencies were observed in the passive movements. It is concluded that the elderly show slower ventilatory response and attenuated circulatory response at the onset of dynamic voluntary exercise and passive movements.     

Visual-manual tracking and vestibular function during a seven-day dry immersion

A seven-day dry immersion experiment provided the opportunity to study the effects of decreased proprioceptive tactile and support afferentations on the vestibular function and visual-manual tracking. Before and after immersion, six subjects participated in a video oculographic evaluation of the static torsion otolith-cervicoocular reflex (OCOR) in response to head tilt by 30° in the frontal plane and dynamic vestibular-cervicoocular reactions to head longitudinal rotations at 0.125 Hz. In addition, the hand-eye motor coordination of tracking a jerky (sinusoidal) or smooth (linear) movement of point targets along the horizontal or vertical lines was evaluated on the basis of the data of electrooculography and records of manipulations with the joystick during immersion. A computerized test was performed in virtual glasses displaying images of visual stimuli and hand motor acts. The computed parameters included the reaction’s latent time, amplitude, speed and time of eye and hand movements, and gains of optooculomotor reactions and manual tracking as a ratio of eye/hand to visual stimulus speed. Testing was carried out before the experiment, after 3 h of immersion, on days 3 and 6 of staying in the bath, in the initial hours after immersion and on the third day of recovery. It was shown that removal of support and minimization of proprioceptive afferentation had a profound effect on the ocular tracking rather than pursuing the visual stimulus by hand. The accuracy of manual tracking was better in comparison with the eye tracking in all subjects. This was the first observation of changes in the peripheral vestibular system in two out of six subjects, i.e., inversion of the static torsion OCOP and positional nystagmus against a background of converted reflex, which did not change the parameters of the visual-manual tracking.     

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     

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.