The Superiority of the Otolith System

Background: The peripheral vestibular end organ is considered to consist of semi-circular canals (SCC) for detection of angular accelerations and the otoliths for detection of linear accelerations. However, otoliths being phylogenetically the oldest part of the vestibular sensory organs are involved in detection of all motions. Summary: This study elaborates on this property of the otolith organ, as this concept can be of importance for the currently designed vestibular implant devices. Key Message: The analysis of the evolution of the inner ear and examination of clinical examples shows the robustness of the otolith system and inhibition capacity of the SCC. The otolith system must be considered superior to the SCC system as illustrated by evolution, clinical evidence, and physical principles.

Coding strategies in the otolith system differ for translational head motion vs. static orientation relative to gravity

The detection of gravito-inertial forces by the otolith system is essential for our sense of balance and accurate perception. To date, however, how this system encodes the self-motion stimuli that are experienced during everyday activities remains unknown. Here, we addressed this fundamental question directly by recording from single otolith afferents in monkeys during naturalistic translational self-motion and changes in static head orientation. Otolith afferents with higher intrinsic variability transmitted more information overall about translational self-motion than their regular counterparts, owing to stronger nonlinearities that enabled precise spike timing including phase locking. By contrast, more regular afferents better discriminated between different static head orientations relative to gravity. Using computational methods, we further demonstrated that coupled increases in intrinsic variability and sensitivity accounted for the observed functional differences between afferent classes. Together, our results indicate that irregular and regular otolith afferents use different strategies to encode naturalistic self-motion and static head orientation relative to gravity.

Decreased otolith-mediated vestibular response in 25 astronauts induced by long-duration spaceflight

The information coming from the vestibular otolith organs is important for the brain when reflexively making appropriate visual and spinal corrections to maintain balance. Symptoms related to failed balance control and navigation are commonly observed in astronauts returning from space. To investigate the effect of microgravity exposure on the otoliths, we studied the otolith-mediated responses elicited by centrifugation in a group of 25 astronauts before and after 6 mo of spaceflight. Ocular counterrolling (OCR) is an otolith-driven reflex that is sensitive to head tilt with regard to gravity and tilts of the gravito-inertial acceleration vector during centrifugation. When comparing pre- and postflight OCR, we found a statistically significant decrease of the OCR response upon return. Nine days after return, the OCR was back at preflight level, indicating a full recovery. Our large study sample allows for more general physiological conclusions about the effect of prolonged microgravity on the otolith system. A deconditioned otolith system is thought to be the cause of several of the negative effects seen in returning astronauts, such as spatial disorientation and orthostatic intolerance. This knowledge should be taken into account for future long-term space missions.

Response of Vestibular Nerve Afferents Innervating Utricle and Saccule During Passive and Active Translations

The distinction between sensory inputs that are a consequence of our own actions from those that result from changes in the external world is essential for perceptual stability and accurate motor control. In this study, we investigated whether linear translations are encoded similarly during active and passive translations by the otolith system. Vestibular nerve afferents innervating the saccule or utricle were recorded in alert macaques. Single unit responses were compared during passive whole body, passive head-on-body, and active head-on-body translations (vertical, fore-aft, or lateral) to assess the relative influence of neck proprioceptive and efference copy-related signals on translational coding. The response dynamics of utricular and saccular afferents were comparable and similarly encoded head translation during passive whole body versus head-on-body translations. Furthermore, when monkeys produced active head-on-body translations with comparable dynamics, the responses of both regular and irregular afferents remained comparable to those recorded during passive movements. Our findings refute the proposal that neck proprioceptive and/or efference copy inputs coded by the efferent system function to modulate the responses of the otolith afferents during active movements. We conclude that the vestibular periphery provides faithful information about linear movements of the head in the space coordinates, regardless of whether they are self- or externally generated.

Changes in the perceived head transversal plane and the subjective visual horizontal induced by Coriolis stimulation during gondola centrifugation

For studying the influence of the vertical semicircular canals on spatial orientation in roll, the subjective visual horizontal (SVH) and the subjective transversal plane of the head (STP) were measured in a situation where the vertical canals sense a roll-velocity stimulus while the otolith organs persistently signal that the head is upright in roll. During gondola centrifugation (resultant gravitoinertial force vector 2.5 G, gondola inclination 66 degrees) subjects were exposed to controlled rotational head movements (angular speed 27 degrees/s, magnitude 40 degrees) about the yaw (body z-) axis, produced by means of a motor-driven helmet. This causes a roll-plane Coriolis stimulus to the canals, while the otoliths persistently sense upright head position in roll. The subjects reported intense sensations of rotation and tilt in the roll plane. This was reflected in tilts of both the SVH and STP. The initial tilt of the SVH was 13.0 ± 9.7 degrees (mean ± S.D., n=10). {The STP was changed in the opposite direction}. The initial tilt was 23.8 ± 12.2 degrees (mean ± S.D., n=5). {The changes in the SVH and STP were not of equal magnitude.} A few subjects who had almost no deviations in the SVH showed pronounced tilts of the STP. The time constant for exponential decay of the tilts of the SVH and STP was on average approximately 1 minute. These findings indicate that a difference in activity of the vertical canals in the right versus left ear may cause substantial tilts of the SVH even if there is no asymmetry in the activity of the otolith system. Further, the canal stimulus may induce a tilt of the fundamental egocentric frame of reference.

Ocular counterrolling in response to static and dynamic tilting: Implications for human otolith function

Nineteen subjects underwent rotation about the naso-occipital axis to examine ocular counterrolling (OCR) responses in both dynamic and static conditions. Dynamic rotation consisted of tilt to 90Âř right and left at constant velocity of 3Âř/s, with acceleration at 0.2Âř/s 2 . Static rotation (stepwise tilting) consisted of one minute at steps 30Âř, 60Âř, 90Âř, 60Âř, 30Âř to each side. OCR amplitudes at each of the above head tilts in dynamic vs. static tilt showed highly significant differences, with dynamic tilt exceeding that of static. Although OCR disconjugacy was greater in static than dynamic in most subjects, that difference was not statistically significant. Possible explanations for the disparity in the responses to dynamic and static tilt in humans lie in vestibular experiments leading to the conclusion that the otolith membrane in cats moves not as a unit, but rather in patches [28]. This is supported by work showing the otolith membrane in bullfrogs does not move en bloc [1]. In addition, hair cell responses are found to be amplified during motion as compared to the responses during static positioning [20]. Functionally, it is suggested that the otolith system may perform better in moving than in static conditions.