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Extracellular single neuron recordings of primary vestibular neurons in Scarpa's ganglion in guinea pigs show that low-intensity 500 Hz bone-conducted vibration (BCV) or 500 Hz air-conducted sound (ACS) activate a high proportion of otolith irregular neurons from the utricular and saccular maculae but few semicircular canal neurons. In alert guinea pigs, and humans, 500 Hz BCV elicits otolith-evoked eye movements. In humans, it also elicits a myogenic potential on tensed sternocleidomastoid muscles. Although BCV and ACS activate both utricular and saccular maculae, it is possible to probe the functional status of these two sense organs separately because of their differential neural projections. Saccular neurons have a strong projection to neck muscles and a weak projection to the oculomotor system. Utricular afferents have a strong projection to eye muscles. So measuring oculomotor responses to ACS and BCV predominantly probes utricular function, while measuring neck muscle responses to these stimuli predominantly probes saccular function., (© 2011 New York Academy of Sciences.)

Head impulses are a routine clinical test of semicircular canal function. At the bedside, they are used to detect malfunctioning of the horizontal semicircular canals. So far, 3-D-search-coil recording is required to reliably test anterior and posterior canal function and to determine the gain of the vestibulo-ocular reflex (VOR). Search-coil recording cannot be done at the bedside. Here we tested whether video-oculography (VOG) is suitable to assess VOR gain for individual canals at the bedside. We recorded head impulses in healthy subjects using a mobile high-frame-rate, head-mounted VOG-device and compared the results with those obtained with standard search-coil recording. Our preliminary results indicate that high-frame-rate VOG is a promising tool to measure and quantify individual semicircular canal function not only at the bedside.

A recent study on static ocular counterroll suggested the existence of residual torsion (RT): when healthy subjects repositioned their head to the upright position after sustained static tilt, eye position differed from the original ocular torsion measured prior to the static head tilt. Our experiments aimed at further characterizing this phenomenon. Using a three-dimensional motorized turntable, healthy human subjects (n = 8) were rotated quasi-statically (0.05 deg/s2, 2 deg/s velocity plateau reached after 40 s) from the upright position about the naso-occipital axis. Three full whole-body rotations were completed while subjects fixed upon a blinking laser dot straight ahead in otherwise complete darkness. Three-dimensional eye movements were recorded with modified dual search coils (wires exiting inferiorly). Torsional position of the right eye at consecutive upright body positions was analyzed. The torsional eye position before the beginning of the chair rotation was defined as zero torsion. On average, the right eye was intorted by 1.3 degrees or extorted by 2.0 degrees after the first full chair rotation in the clockwise or counterclockwise direction, respectively. These torsional offset values of the right eye did not significantly change after the two subsequent full chair rotations. We conclude that RT observed after static ocular counterroll is the result of static hysteresis, that is, a position lag of the eye, which depends on the direction of head roll. The fact that residual torsion did not further increase after the first rotation cycle emphasizes that RT is a static rather than a dynamic phenomenon.

A decreasing drift of the counter-rolled eye position (OCR) during head tilt was recently described. The underlying mechanism is not known. OCR in eleven healthy subjects was recorded (Search coil, Skalar) during a head tilt paradigm in two test conditions. The head was tilted with a velocity below (test 1) and above (test 2) detection threshold for the semicircular canals (SC) and held static for eight minutes. A significant drift of OCR was revealed in test 2 (P = .0006, ANOVA) and close to significant in test 1 (P = .07). No statistical difference was found between the two test conditions. The results suggest that the OCR drift was not caused by the SC complex merely.

Research into vestibular responses to sound has evolved in four stages. The first, largely the work of Tullio in the 1920s, involved inspection of the eye, head, and postural responses to sound of alert animals with surgical fenestrae into various parts of the bony labyrinth. The second, begun in 1964 by Bickford and his group and continued by our group and then by others in the last 10 years, involves the measurement of evoked myogenic potentials to air-conducted and bone-conducted clicks and tones in normal humans. The third, begun by Mikaelian at about the same time as Bickford and continued by McCue, our group, and others, involves electrophysiological recordings of primary vestibular afferent neuron responses to sound in anesthetized animals. The fourth involves measurements of vestibulo-ocular responses to sound in humans with the Tullio phenomenon. It was begun by Minor and his group in 1998 with the observation that sound-induced nystagmus in humans, the Tullio phenomenon, aligned with the rotation axis of the superior semicircular canal. They then showed a defect in the temporal bone between the apex of the superior semicircular canal and the middle cranial fossa, which was the cause of most, if not all, cases of sound-induced nystagmus. Here some of the key observations made in each of these four stages are reviewed.

The eye movement component that rotates around the line of sight, i.e., the ocular torsion, is in many aspects different from horizontal and vertical eye movements. While ocular torsion is mediated only by reflexive pathways like the torsional vestibulo-ocular and optokinetic reflexes (TVOR and OKN, respectively), horizontal and vertical components are also subject to intentional control mechanisms that are mediated by the saccadic and the pursuit systems. Dynamic properties of torsional eye movements are also very distinct. While horizontal and vertical VOR components show a gain close to unity and a small neural integration leakage with a time constant around pi=30 s, the TVOR shows a smaller gain of 0.4 and also a greater leakage with pi=2 s. During slow head rotations in roll, the TVOR is even less compensatory. At small stimulation levels the gain drops to a value of 0.2 and proves thus to be nonlinear, i.e., to depend on the stimulus magnitude. In a recent study, we hypothesized that this nonlinearity might be the result of a nonlinear processing of nystagmus quick phases rather than a nonlinearity in direct or integrator TVOR pathways. In the present study, we experimentally tested this hypothesis by measuring ocular torsion responses at different head rotation speeds. In addition to the conventional approach of analyzing slow-phase velocity (SPV) gains, we also analyzed properties of nystagmus quick phases. This method proved to be suitable for determining whether nonlinear processing of nystagmus frequency is responsible for the TVOR nonlinearity.

When tilted subjects are asked to set a luminous line to the perceived earth-vertical in a dark surrounding, they systematically underestimate the true direction of earth-vertical at large tilt angles, a phenomenon first described by Aubert (A-phenomenon). At small tilt angles, subjects usually overestimate the direction of earth-vertical. Overestimation has been first reported by Müller, who termed the notion of E-phenomenon. Since these first reports, this rather remarkable error behavior has been studied extensively. The prevailing notion in most earlier studies was that the erroneous estimation of verticality results from otolith signals, which are thought to represent the major input for spatial orientation, and their interaction with somatosensory signals. To bring the subjects into tilted positions, most investigators used slow tilt velocities or waited for some time to prevent interaction with semicircular canal activity. Here, we tested the hypothesis that vestibular cues about self-orientation relative to gravity are most reliable when both the semicircular canals and the otolith organs are optimally activated. To compare the error behavior in estimations of the visual vertical and perceived body position, we used self-controlled passive tilts at constant velocity or acceleration.

The vestibular nerve sends signals to the brain that code the movement and position of the head in space. These signals are used by the brain for a variety of functions, including the control of reflex and voluntary movements and the construction of a sense of self-motion. If many of these functions are to be carried out, a distinction must be made between sensory vestibular signals related to active head movements and those related to passive head movements. Current evidence is that the distinction occurs at an early stage of sensory processing in the brain, and the results are evident in the firing behavior of neurons in the vestibular nuclei that receive direct inputs from the vestibular nerve. Several specific examples of how sensory information related to passive and active head movements is transformed in the vestibular nuclei are discussed.

The rostral fastigial nucleus contains vestibular neurons, which presumably are involved in spinal mechanisms (neck, gait, posture) and which are not modulated with individual eye movements. Single-unit recordings in the alert behaving monkey during natural stimulus conditions reveal that virtually all neurons demonstrate integration of several sensory inputs. This applies not only for canal-canal and canal-otolith interaction, but also for otolith-otolith interaction. There is also some evidence that most neurons receive not only an utriculus but also a sacculus input. Furthermore, most neurons also respond to large-field optokinetic stimulation, reflecting visual-vestibular interaction. Neurons are also affected by the head on trunk position, which would allow these neurons to operate in a body-centered rather than a head-centered reference frame. These complex, multisensory features could permit fastigial nucleus neurons to rather specifically affect spinal motor functions.

Rotational disturbances of the head about an off-vertical yaw axis induce a complex vestibuloocular reflex pattern that reflects the brain's estimate of head angular velocity as well as its estimate of instantaneous head orientation (at a reduced scale) in space coordinates. We show that semicircular canal and otolith inputs modulate torsional and, to a certain extent, also vertical ocular orientation of visually guided saccades and smooth-pursuit eye movements in a similar manner as during off-vertical axis rotations in complete darkness. It is suggested that this graviceptive control of eye orientation facilitates rapid visual spatial orientation during motion.

In order to test the human angular vestibulo-ocular reflex in the dynamic range of normal head movements, we measured 3-dimensional compensatory eye-movement responses to low-amplitude (10-12 degrees), high-acceleration (3000-4000 degrees/s/s), passive, manually delivered head rotations (head "impulses") in the three planes of the semicircular canals in normal subjects, in subjects who had recovered from surgical unilateral vestibular deafferentation, and in patients after acute unilateral peripheral vestibulopathy, that is, from vestibular "neuritis." We found that canal-plane head impulses away from an intact semicircular canal, that is, toward a lesioned semicircular canal, invariably produce a vestibulo-ocular reflex with permanently low gain, typically less that 0.4 if the lesion is complete. These results are a necessary consequence of primary semicircular canal afferents being driven into inhibitory saturation by rapid angular accelerations. With practice, clinicians can learn to recognize the telltale compensatory saccades that patients with unilateral loss of semicircular canal function will make if asked to look at an earth-fixed target during head impulses in any one of the three semicircular canal planes.

Inactivation of individual semicircular canals by surgical occlusion (plugging) of the slender duct has been used in basic studies to elucidate the role of individual canal inputs to vestibular-mediated control systems and in clinical applications to treat certain vestibular disorders. The procedure has been shown to be highly effective in blocking sensitivity of individual canals, at least for moderate angular motion stimuli. Effectiveness does not extend to stimuli involving high accelerations where a residual response persists even after complete occlusion of the duct. The residual can be quite large at high-stimulus frequencies where sensitivity to angular motion approaches that of patent canals. The overall physiological effect of canal plugging is reported here in terms of the frequency-dependent attenuation in gain and phase shift of primary afferents. Plug-canal responses are quantitatively described in terms of biomechanics of the deformable labyrinth.

New evidence for a central resolution of gravito-inertial signals has been recently obtained by analyzing the properties of the vestibulo-ocular reflex (VOR) in response to combined lateral translations and roll tilts of the head. It is found that the VOR generates robust compensatory horizontal eye movements independent of whether or not the interaural translatory acceleration component is canceled out by a gravitational acceleration component due to simultaneous roll-tilt. This response property of the VOR depends on functional semicircular canals, suggesting that the brain uses both otolith and semicircular canal signals to estimate head motion relative to inertial space. Vestibular information about dynamic head attitude relative to gravity is the basis for computing head (and body) angular velocity relative to inertial space. Available evidence suggests that the inertial vestibular system controls both head attitude and velocity with respect to a gravity-centered reference frame. The basic computational principles underlying the inertial processing of otolith and semicircular canal afferent signals are outlined.

A one-dimensional mathematical model of the compensatory linear vestibuloocular reflex (lVOR) was developed. The model was based on the concept that to effect oculomotor compensation, linear head acceleration sensed by the otoliths must be integrated twice to form the angular position-related signal required by the motoneurons. This contradicts the postulate that linear acceleration is differentiated to generate "jerk," which is then used to drive the compensatory lVOR. The transfer characteristics of different otolith afferent classes were modeled by a transfer function with a common modal structure and different degrees of compensation. Both the time and frequency domain behavior of regular and irregular otolith afferents were simulated. The outputs of the various afferent classes were superposed by a linear filter to generate the velocity command which drives the oculomotor velocity-position integrator. The model was used to simulate the dominant gain and phase characteristics of the compensatory lVOR in monkey and the dynamic characteristics of the compensatory human lVOR response for brief periods of linear acceleration on a sled. The model was then combined with the velocity storage-based model of the angular vestibulo-ocular reflex (aVOR) to simulate the eye velocity response to centrifugation in monkey and man. The model suggests that the orientation response that modifies the time constants of the velocity storage integrator is the dominant aspect of the response to linear acceleration in monkey. Human responses, on the other hand, are dominated by an effect of the beating field, which modifies the eye velocity command to the oculomotor system.

Present results separate the relative contributions of semicircular canal biomechanics from hair cell/afferent biophysics in determining the amplitude and phase of afferent responses to sinusoidal motion of the head. Separation was achieved by combining electrical polarization of the endolymph with mechanical indentation of the canal limb to modulate the instantaneous firing rate of horizontal semicircular canal afferents. The electrical stimulus drives hair cell transduction currents via modulation of the Nernst-Planck potential, whereas the mechanical stimulus mimics head rotation and modulates the open probability of the transduction channels. Responses for electrical polarization therefore reflect post-transduction-current (PTC) mechanisms, and responses for mechanical stimulation include the additional influence of canal mechanics. Linear transfer functions defining individual afferent response dynamics were obtained for low levels of each stimuli and are reported in Bode form providing gain (spikes/s per micron or mV) and phase (deg re: peak stim) over the frequency range from 0.02 to 40 Hz. Combined results for electrical and mechanical stimuli distinguish the component of sensory signal processing carried out by canal mechanics from that carried out by the hair cell/afferent complexes. Individual afferents were categorized according to their response to the mechanical stimuli as low-gain velocity (LG), high-gain velocity (HG) or acceleration (A) sensitive, groups as originally defined by Boyle and Highstein to describe interafferent diversity present within the population. In contrast to the results for mechanical stimuli, all afferent groups exhibit nearly equal increases in gain and phase for increasing frequencies of electrical stimulation. Comparison of individual afferent responses for the two stimuli leads to the conclusion that the LG, HG, and A groups are distinguished primarily by diversity in the mechanical activation of associated hair cells and not by PTC mechanisms. Even though PTC processing does not contribute significantly to determining these groups, it is the primary determinant underlying high-frequency gain and phase enhancements observed in the population average. Comparison of mechanical and electrical responses also reveals the mechanical lower-corner responsible for phase enhancements and gain decreases in all afferents at low frequencies of mechanical stimulation (< 0.05 Hz). Results imply that LG afferents encode angular head velocity by canceling a phase lag and gain attenuation due to the mechanics with a phase lead and gain enhancement due to PTC mechanisms above approximately 0.2 Hz. In contrast, A group afferents encode angular head acceleration by combining high-frequency phase leads and gain enhancements present in both the mechanics and PTC mechanisms across the physiological frequency spectrum. HG afferents fall between these two extremes, and, other than the influence of the mechanical lower-corner, their response primarily reflects PTC processing.

This study was performed to investigate the pattern of input and the pathways from the six semicircular canals to motoneurons of various neck muscles in anesthetized cats. Intracellular postsynaptic potentials from neck motoneurons were recorded in response to electrical stimulation of the six ampullary nerves. The results showed that motoneurons of a particular neck muscle have a homogeneous convergent pattern of input from the six semicircular canals; there are four patterns of input from the six semicircular canals to motoneurons of various neck muscles; and the trisynaptic connection between the semicircular canal nerves and neck motoneurons was identified in addition to the disynaptic connection.

Results of the five experiments are consistent with the following generalizations. Canal-mediated turn perception (pitch, roll, or yaw) in earth-horizontal or earth-vertical plane, is suppressed in direct relationship to the magnitude of a linear acceleration vector lying in the plane of a responding canal when the magnitude of the linear vector is constant or increasing and when its direction is either fixed or rotating in the same direction as the concomitant canal signal. Canal-mediated turn perception (pitch, roll, or yaw) is not suppressed by a coplanar linear vector that is counterrotating relative to the canal signal. Change in perceived attitude (pitch, roll, or yaw) is very sluggish in the absence of concordant canal information; attitude change may not be an immediate otolith-mediated perceptual event but a slowly developing perception dependent upon cognitive appreciation of an immediate otolith angular position signal. Otolith phasic neural units, unreinforced by appropriate canal signals, may contribute more to a brief linear velocity component in perception than to rate of attitude change. Otolith-mediated attitude perception within a given earth-vertical plane can be distorted by strong coplanar angular velocity canal information. Once distorted, return to veridical attitude perception can be gradual because, in the absence of complimentary canal or visual information, recovery is dependent upon relatively slow cognitive appreciation of a prevailing otolith position signal. Several attractive hypotheses relating to the dynamics of attitude perception can only be tested by substantially more data on the dynamics of spatial orientation perception. Most of our objectives cannot be achieved without models that yield valid prediction of the dynamics of spatial orientation perception. All of the observations in these experiments were carried out in darkness, or, in the simulated catapult experiment, without external visual reference. Various forms of visual information will change the dynamics of spatial orientation perception. My discussion has been limited to consideration of the vestibular system, as though the canal and otolith systems completely controlled the dynamics of spatial orientation perceptions. Obviously other partners in the dynamics of postural control, including vision, proprioception, and expectation, must be included in this challenging field of research. Dedication to stereotyped ideas about objectivity in the 20th century has hindered advancement of knowledge on the dynamics of spatial orientation perception relative to rate of progress achieved by several scientists of the 18th and 19th centuries, who provided word pictures of perceived motions and tilts along with descriptions of the motions that engendered the pictures.(ABSTRACT TRUNCATED AT 400 WORDS)

An "engineer's model" of the labyrinth is derived from the monoclinic crystal and the avian egg. The anatomy of the human cochlea and of the semicircular canals is then related by diffraction theory and Fresnel's explanation of optic activity. Increased cochlear electric potential, which represents stored energy, is associated with mechanical translation of the basilar membrane and angular separation of Corti's rods and is effected by "pumping" by the endolymphatic sac and the muscles that act on the auditory ossicles. The semicircular canals function as valves; the utricular and saccular macules form holograms and reflect the energy into the cochlear duct. Incoming acoustic waves excite dipole resonance and stimulate emission of a fraction of the stored energy; further amplification is effected by the hair cells, which, together with the tectorial membrane, behave like a transistor. These findings lead to a new theory of static balance and the action of Corti's organ: the labyrinth functions as a traveling wave maser of which the cochlea is the slow wave structure. Cochlear geometry itself effects resolution of incoming sound pitch. Corti's organ corresponds to the melatopes of the crystal, and the inter-rod angle is critical for any particular frequency, since it is related to dispersion of the optic axes.