Detection of rotating gravity signals

It is shown in the preceding paper that neurons with two-dimensional spatio-temporal properties to linear acceleration behave like one-dimensional rate sensors: they encode the component of angular velocity (associated with a rotating linear acceleration vector) that is normal to their response plane. During off-vertical axis rotation (OVAR) otolith-sensitive neurons are activated by the gravity vector as it rotates relative to the head. Unlike one-dimensional linear accelerometer neurons which exhibit equal response magnitudes for both directions of rotation, two-dimensional neurons can be shown to respond with unequal magnitudes to clockwise and counterclockwise off-vertical axis rotations. The magnitudes of the sinusoidal responses of these neurons is not only directionally selective but also proportional to rotational velocity. Thus, responses from such two-dimensional neurons may represent the first step in the computations necessary to generate the steady-state eye velocity during OVAR. An additional step involving a nonlinear operation is necessary to transform the sinusoidally modulated output of these neurons into a signal proportional to sustained eye velocity. Similarly to models of motion detection in the visual system, this transformation is proposed to be achieved through neuronal operations involving mathematical multiplication followed by a leaky integration by the velocity storage mechanism. The proposed model for the generation of maintained eye velocity during OVAR is based on anatomical and physiological properties of vestibular nuclei neurons and capable of predicting the experimentally observed steady-state characteristics of the eye velocity.     

Bayesian processing of vestibular information

Complex self-motion stimulations in the dark can be powerfully disorienting and can create illusory motion percepts. In the absence of visual cues, the brain has to use angular and linear acceleration information provided by the vestibular canals and the otoliths, respectively. However, these sensors are inaccurate and ambiguous. We propose that the brain processes these signals in a statistically optimal fashion, reproducing the rules of Bayesian inference. We also suggest that this processing is related to the statistics of natural head movements. This would create a perceptual bias in favour of low velocity and acceleration. We have constructed a Bayesian model of self-motion perception based on these assumptions. Using this model, we have simulated perceptual responses to centrifugation and off-vertical axis rotation and obtained close agreement with experimental findings. This demonstrates how Bayesian inference allows to make a quantitative link between sensor noise and ambiguities, statistics of head movement, and the perception of self-motion.     

Two-dimensional coding of linear acceleration and the angular velocity sensitivity of the otolith system

There exist otolith-sensitive vestibular nuclei neurons with spatio-temporal properties that can be described by two response vectors that are in temporal and spatial quadrature. These neurons respond to the component of a stimulus vector on a plane rather than a single axis. It is demonstrated here that these two-dimensional linear accelerometer neurons can function as one-dimensional angular velocity detectors. The two-dimensional property in both space and time allows these neurons to encode the component of the stimulus angular velocity vector that is normal to the plane defined by the two response vectors. The angular velocity vector in space can then be reconstructed by three populations of such neurons having linearly independent response planes. Thus, we propose that these two-dimensional spatio-temporal linear accelerometer neurons, in addition to participating in functions of the otolith system that are based on detection of linear acceleration, are also involved in the generation of compensatory ocular responses during off-vertical axis rotations.     

Time constants of vestibular nuclei neurons in the goldfish: A model with ocular proprioception

A simple model of the vestibular-ocular reflex with a proprioceptive eye velocity feedback loop is used to simulate recent data on the vestibular responses of neurons in the vestibular nuclei of spinal goldfish. The data support the hypothesis that a proprioceptive feedback loop elongates the vestibular nucleus time constant to equal that of the slow phase eye movements of vestibular nystagmus.     

A linear canal-otolith interaction model to describe the human vestibulo-ocular reflex

A control systems model of the vestibulo-ocular reflex (VOR) originally derived for yaw rotation about an eccentric axis (Crane et al. 1997) was applied to data collected during ambulation and dynamic posturography. The model incorporates a linear summation of an otolith response due to head translation scaled by target distance, adding to a semi-circular canal response that depends only on angular head rotation. The results of the model were compared with human experimental data by supplying head angular velocity as determined by magnetic search coil recording as the input for the canal branch of the model and supplying linear acceleration as determined by flux gate magnetometer measurements of otolith position. The model was fit to data by determining otolith weighting that enabled the model to best fit the data. We fit to the model experimental data from normal subjects who were: standing quietly, walking, running, or making active sinusoidal head movements. We also fit data obtained during dynamic posturography tasks of: standing on a platform sliding in a horizontal plane at 0.2 Hz, standing directly on a platform tilting at 0.1 Hz, and standing on the tilting platform buffered by a 5-cm thick foam rubber cushion. Each task was done with the subject attending a target approximately 500, 100, or 50 cm distant, both in light and darkness. The model accurately predicted the observed VOR response during each test. Greater otolith weighting was required for near targets for nearly all activities, consistent with weights for the otolith component found in previous studies employing imposed rotations. The only exceptions were for vertical axis motion during standing, sliding, and tilting when the platform was buffered with foam rubber. In the horizontal axis, the model always fit near target data better with a higher otolith component. Otolith weights were similar with the target visible and in darkness. The model predicts eye movement during both passive whole-body rotation and free head movement in space implying that the VOR is controlled by a similar mechanism during both situations. Factors such as vision, proprioception, and efference copy that are available during head free motion but not during whole-body rotation are probably not important to gaze stabilization during ambulation and postural stabilizing movement. The linearity of the canal-otolith interaction was tested by re-analysis of the whole body rotation data on which the model is based (Crane et al. 1997). Normalized otolith-mediated gain enhancement was determined for each axis of rotation. This analysis uncovered minor non-linearities in the canal-otolith interaction at frequencies above 1.6 Hz and when the axis of rotation was posterior to the head. Received: 11 March 1998 / Received in revised form: 1 March 1999     

Effect of active head movements about the pitch, roll, and yaw axes on human optokinetic afternystagmus

Effects of active head movements about the pitch, roll, or yaw axes on horizontal optokinetic afternystagmas (OKAN) were examined in 16 subjects to test the hypothesis that otolith organ mediated activity induced by a change in head position can couple to the horizontal velocity storage in humans. Active head movements about the pitch axis, forwards or backwards, produced significant OKAN suppression. Pitch forward head movements exerted the strongest effect. Active head movements about the roll axis towards the right also produced OKAN suppression but only if the tilted position was sustained. No suppression was observed following sustained yaw. However, an unsustained yaw left movement after rightward drum rotation significantly enhanced OKAN. Sustained head movement trials did not significantly alter subsequent control trials. In contrast, unsustained movements about the pitch axis, which involve more complex interactions, exerted long-term effects on subsequent control trials. We conclude that otolith organ mediated activity arising from pitch or roll head movements couples to the horizontal velocity storage in humans, thereby suppressing ongoing OKAN. Activity arising from the horizontal canals during an unsustained yaw movement (observed mainly with yaw left), following drum rotation in a direction contralateral to the movement, may also couple to the velocity storage, resulting in increased activity instead of suppression.     

Simulation of vestibular semicircular canal responses during righting movements of a freely falling cat

The righting maneuver of a freely falling cat was filmed at 1000 pictures per second, and the head position about the roll axis was digitized from each film frame using a graphics input tablet. The head angular velocity and acceleration were computed from the roll axis position trajectory. Head acceleration trajectories approximated two periods of a damped sinusoid at a frequency of 26 Hz. Head acceleration peak amplitudes exceeded 120,000 deg/s². These trajectories were used as stimuli for the horizontal semicircular canals in a computer simulation of first-order afferent responses during the fall. Linear system afferent response dynamics, characterized in a previous study of the cat horizontal canal using pseudorandom rotations, provided the basis for linear predictions of falling cat afferent responses. Results showed predicted single afferent firing rates that exceeded physiological values; and variations in afferent sensitivities and phase were predicted among different neurons. Fast head movement information could be carried by ensemble populations of vestibular neurons, and a phase-locking encoding hypothesis is proposed which accomplishes this. Implications for central program versus peripheral vestibular feedback strategies for motor control during falling are presented and discussed.     

The cerebellar nodulus/uvula integrates otolith signals for the translational vestibulo-ocular reflex

BACKGROUND: The otolith-driven translational vestibulo-ocular reflex (tVOR) generates compensatory eye movements to linear head accelerations. Studies in humans indicate that the cerebellum plays a critical role in the neural control of the tVOR, but little is known about mechanisms of this control or the functions of specific cerebellar structures. Here, we chose to investigate the contribution of the nodulus and uvula, which have been shown by prior studies to be involved in the processing of otolith signals in other contexts. METHODOLOGY/PRINCIPAL FINDINGS: We recorded eye movements in two rhesus monkeys during steps of linear motion along the interaural axis before and after surgical lesions of the cerebellar uvula and nodulus. The lesions strikingly reduced eye velocity during constant-velocity motion but had only a small effect on the response to initial head acceleration. We fit eye velocity to a linear combination of head acceleration and velocity and to a dynamic mathematical model of the tVOR that incorporated a specific integrator of head acceleration. Based on parameter optimization, the lesion decreased the gain of the pathway containing this new integrator by 62%. The component of eye velocity that depended directly on head acceleration changed little (gain decrease of 13%). In a final set of simulations, we compared our data to the predictions of previous models of the tVOR, none of which could account for our experimental findings. CONCLUSIONS/ SIGNIFICANCE: Our results provide new and important information regarding the neural control of the tVOR. Specifically, they point to a key role for the cerebellar nodulus and uvula in the mathematical integration of afferent linear head acceleration signals. This function is likely to be critical not only for the tVOR but also for the otolith-mediated reflexes that control posture and balance.     

Perspectives for the comprehensive examination of semicircular canal and otolith function.

A review is presented on the three-dimensional aspects of the vestibulo-oculomotor system and the current functional tests for unilateral examination of the individual receptors in the vestibular labyrinth. In the presentation, attention is directed towards the recently developed vestibular tests, which promise a more comprehensive examination of labyrinth function. More explicitly, unilateral tests for the utricle, saccule and the individual semicircular canals are discussed. Caloric irrigation and rotatory testing are widely used as tests for the integrity of the (horizontal) semicircular canals. Little useful diagnosis is made however on the vertical canals, not to mention the otolith organs. A promising approach to the examination of individual semicircular canal function has been described. This involves the perception of self-rotation in each of the planes of the semicircular canals. The patient/subject is rotated by an arbitrary amount on a standard Barany chair and then required to return the chair to its original position, by joystick control of the chair velocity. In order to test the vertical canals, the head of the subject/patient is positioned so that the plane of each canal lies in the plane of rotation. A promising unilateral test of saccular function involves the use of vestibular evoked myogenic potentials. Here it has been demonstrated that the saccules can be activated using brief, high-intensity acoustic clicks. The myogenic potential is measured using surface electrodes over the sternocleidomastoid muscles. Initial data from patients has indicated that the test is specific for unilateral saccule disorders. The unilateral test of utricle function is based on the eccentric displacement profile. Thus, eccentric displacement of the head to 3.5 cm during constant velocity rotation about the earth-vertical axis generates an adequate unilateral stimulation of the otolith organ, without involving the semicircular canals. This paradigm has also proved efficient in localizing peripheral otolith dysfunction by means of SVV estimation. This represents a novel test of otolith function that can be easily integrated into routine clinical testing. In contrast to the otolith-ocular response, the subjective visual vertical also reflects the processing of otolithic information in the higher brain centres (thalamus, vestibular cortex). Exploitation of the two complementary approaches therefore provides useful information for both experimental and clinical scientists. Of direct interest is the finding that testing with the subject rotating on-centre is sufficient to localize peripheral otolith dysfunction by means of SVV estimation. This represents a novel test of otolith function that can be easily integrated into routine clinical testing. In addition to caloric testing, which has remained the classical unilateral test of vestibular function, the newly developed tests should improve the differential diagnosis of vestibular disorders.     

Effect of otoliths upon function of the semicircular canals after long-term stay under conditions of microgravitation

Results of studies performed in 12 astronauts after flights revealed that in some of them re-adaptation to the Earth gravitation involved increase of spontaneous oculomotor activity in immobile position of the head, suppression of the otolith function in static 40 degrees bending of the head towards right or left shoulders, enhancement of vestibular responsiveness in rotation of the head around the body longitudinal axis at the rate of 0.125 Hz.     

Interaction of the angular and linear components of the horizontal vestibulo-ocular reflex in the pigeon

Pigeons were exposed to centric and eccentric horizontal rotations in darkness by velocity trapezoid. Different in sign the duration alterations of the opposite directed horizontal eye nystagmus occurred during otolith membrane shifts in sagittal as well as frontal planes. A direct dependence was found between the duration alterations of the primary nystagmus phase and the peak value alterations of its slow phase velocity under increased (but not decreased) centrifugal force. In the both cases, if duration of the primary nystagmus phase was enlarged, duration of its secondary phase was diminished and vice versa. It suggests the otolith component does not decay up to zero by constant velocity and at once after rotation; by deceleration it is biphasic. In affirms the own hypothesis that the linear component is asymmetric central neuronal activity that modifies the canal component even if this activity by itself is not enough for eye movement initiation.     

Sympathetic responses to vestibular activation in humans

Activation of sympathetic neural traffic via the vestibular system is referred to as the vestibulosympathetic reflex. Investigations of the vestibulosympathetic reflex in humans have been limited to the past decade, and the importance of this reflex in arterial blood pressure regulation is still being determined. This review provides a summary of sympathetic neural responses to various techniques used to engage the vestibulosympathetic reflex. Studies suggest that activation of the semicircular canals using caloric stimulation and yaw rotation do not modulate muscle sympathetic nerve activity (MSNA) or skin sympathetic nerve activity (SSNA). In contrast, activation of the otolith organs appear to alter MSNA, but not SSNA. Specifically, head-down rotation and off-vertical axis rotation increase MSNA, while sinusoidal linear accelerations decrease MSNA. Galvanic stimulation, which results in a nonspecific activation of the vestibule, appears to increase MSNA if the mode of delivery is pulse trained. In conclusion, evidence strongly supports the existence of a vestibulosympathetic reflex in humans. Furthermore, attenuation of the vestibulosympathetic reflex is coupled with a drop in arterial blood pressure in the elderly, suggesting this reflex may be important in human blood pressure regulation.     

Vestibulo-ocular reflex and gravity in fish.

An otolith organ on ground behave as a detector of both gravity and linear acceleration, and play an important role in controlling posture and eye movement for tilt of the head or translational motion. On the other hand, a gravitational acceleration ingredient to an otolith organ disappears in microgravity environment. However, linear acceleration can be received by otolith organ and produce a sensation that is different from that on Earth. It is suggested that in microgravity signal from the otolith organ may cause abnormality of posture control and eye movement. We examined function of otolith organ in goldfish revealed from analysis of eye movement induced by linear acceleration. We analyzed vertical eye movements from video images frame by frame. In normal fish, leftward lateral acceleration induced downward eye rotation in the left eye and upward eye rotation in the right eye. Acceleration from caudal to rostra1 evoked downward eye rotation in both eyes. When the direction of acceleration was shifted 15 degrees left, the responses in the left eye disappeared. These results suggested that otolith organs in each side transmitted different signals.     

Experimental research on maculo-ampullar interactions in normal subjects

The AA. investigated 20 normal subjects to evaluated the influence of the otolith organ on the nystagmus, induced by angular accelerations in centrifugal and eccentric rotations. The nystagmus has been recorded by electronystagmostical analysis. The results show that centrifugal and eccentric tests reduce the nystagmus intensity and particularly the amplitude, duration and slow-phase velocity during the per-rotatory accelerations. These findings confirm that the macular activity may inhibit the nystagmus reactions induced by angular acceleration.     

Sensory convergence solves a motion ambiguity problem

Our inner ear is equipped with a set of linear accelerometers, the otolith organs, that sense the inertial accelerations experienced during self-motion. However, as Einstein pointed out nearly a century ago, this signal would by itself be insufficient to detect our real movement, because gravity, another form of linear acceleration, and self-motion are sensed identically by otolith afferents. To deal with this ambiguity, it was proposed that neural populations in the pons and midline cerebellum compute an independent, internal estimate of gravity using signals arising from the vestibular rotation sensors, the semicircular canals. This hypothesis, regarding a causal relationship between firing rates and postulated sensory contributions to inertial motion estimation, has been directly tested here by recording neural activities before and after inactivation of the semicircular canals. We show that, unlike cells in normal animals, the gravity component of neural responses was nearly absent in canal-inactivated animals. We conclude that, through integration of temporally matched, multimodal information, neurons derive the mathematical signals predicted by the equations describing the physics of the outside world.     

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.     

Head movements of the mealworm beetle Tenebrio molitor

Tethered walking imagines of the mealworm beetle Tenebrio molitor wave their heads in random fashion. If a periodic pattern of vertical black and white stripes is rotated around the animal a regular nystagmic head movement is superimposed upon the random waving, the frequency of the latter equals the contrast frequency within large ranges of the angular velocity of the pattern. The nystagmus is inverted: After a short period of tracking, during which the angular velocity of the head is the same as that of the panorama, the head returns slowly toward its normal position according to an exponential-like function. Resting animals do not wave their heads. However, if the above panorama is rotated, the beetle turns its head in the direction of the movement of the panorama and holds it in a side-way position, as long as the rotation is maintained. The angular position reached depends in the same manner on the angular velocity of the panorama as the turning tendency of walking animals established in open loop experiments using the spherical Y-maze method.     

Brain function in antarctic fish: Activity of central vestibular neurons in relation to head rotation and eye movement

Summary Recordings were made from central vestibular neurons responding to horizontal head rotation in antarctic fish,Pagothenia borchgrevinki, at a temperature close to 0 °C. The spontaneous activity of these units varied between 0 and 56 Imp/s with a mean value of 20. Almost all units responded to horizontal rotation with a maximum firing rate that was approximately in phase with head velocity, either towards the recording side (type I units) or away from the recording side (type II), with no alteration of firing pattern during saccadic eye movements. The mean gain of these units was 2.6 Imp/s//s at 0.35 Hz which is higher than that reported for central vestibular neurons in other fish.     

On the Vertigo Due to Static Magnetic Fields

Vertigo is sometimes experienced in and around MRI scanners. Mechanisms involving stimulation of the vestibular system by movement in magnetic fields or magnetic field spatial gradients have been proposed. However, it was recently shown that vestibular-dependent ocular nystagmus is evoked when stationary in homogenous static magnetic fields. The proposed mechanism involves Lorentz forces acting on endolymph to deflect semicircular canal (SCC) cupulae. To investigate whether vertigo arises from a similar mechanism we recorded qualitative and quantitative aspects of vertigo and 2D eye movements from supine healthy adults (n = 25) deprived of vision while pushed into the 7T static field of an MRI scanner. Exposures were variable and included up to 135s stationary at 7T. Nystagmus was mainly horizontal, persisted during long-exposures with partial decline, and reversed upon withdrawal. The dominant vertiginous perception with the head facing up was rotation in the horizontal plane (85% incidence) with a consistent direction across participants. With the head turned 90 degrees in yaw the perception did not transform into equivalent vertical plane rotation, indicating a context-dependency of the perception. During long exposures, illusory rotation lasted on average 50 s, including 42 s whilst stationary at 7T. Upon withdrawal, perception re-emerged and reversed, lasting on average 30 s. Onset fields for nystagmus and perception were significantly correlated (p<.05). Although perception did not persist as long as nystagmus, this is a known feature of continuous SSC stimulation. These observations, and others in the paper, are compatible with magnetic-field evoked-vertigo and nystagmus sharing a common mechanism. With this interpretation, response decay and reversal upon withdrawal from the field, are due to adaptation to continuous vestibular input. Although the study does not entirely exclude the possibility of mechanisms involving transient vestibular stimulation during movement in and out of the bore, we argue these are less likely.