Model-based study of the human cupular time constant

1999 ◽  
Vol 9 (4) ◽  
pp. 293-301 ◽  
Author(s):  
Mingjia Dai ◽  
Avniel Klein ◽  
Bernard Cohen ◽  
Theodore Raphan

The time constant of the angular vestibulo-ocular reflex (aVOR), measured from the response to steps of rotation about a yaw axis, has frequently been estimated as a single exponential. However, the slow phase velocity envelope during per- or post-rotatory nystagmus is more accurately represented by two exponential modes. One represents activity in the vestibular nerve induced by deflection of the cupula, the other by activation that the input from the canals produces in the central velocity storage integrator. The sum of the cupula and the integrator responses describes the overall response of slow phase eye velocity and can be approximated by a double exponential. Frequently, there is a plateau in the initial portion of eye velocity response, but this may be masked by habituation, making the cupula contribution unobservable and impossible to estimate. Using a model-based technique to analyze responses with a clear plateau, we estimated peripheral and central vestibular time constants by double exponential fits to slow phase eye velocity. Cupular time constants were varied from 1 to 10 s to identify values that gave optimal fits of the data according to a Chi-square criterion. The mean cupular time constant for 10 human subjects was 4.2 ± 0.6 s. Fits of the data were also good for time constants between 3.5 to 7 s, but not for 1 to 3 or 7.5 to 10 s. The estimated cupular time constants also fit responses where there was no plateau. In 8 monkeys, cupular time constants were estimated as 3.9 ± 0.5 s, which agreed with those derived from activity in the vestibular nerve. There was no difference between monkey and human cupular time constants from these estimates. It is likely that the human cupular time constant is similar to that of the monkey and shorter than previously thought.

Author(s):  
Tugrul Irmak ◽  
Ksander N. de Winkel ◽  
Daan M. Pool ◽  
Heinrich H. Bülthoff ◽  
Riender Happee

AbstractPrevious literature suggests a relationship between individual characteristics of motion perception and the peak frequency of motion sickness sensitivity. Here, we used well-established paradigms to relate motion perception and motion sickness on an individual level. We recruited 23 participants to complete a two-part experiment. In the first part, we determined individual velocity storage time constants from perceived rotation in response to Earth Vertical Axis Rotation (EVAR) and subjective vertical time constants from perceived tilt in response to centrifugation. The cross-over frequency for resolution of the gravito-inertial ambiguity was derived from our data using the Multi Sensory Observer Model (MSOM). In the second part of the experiment, we determined individual motion sickness frequency responses. Participants were exposed to 30-minute sinusoidal fore-aft motions at frequencies of 0.15, 0.2, 0.3, 0.4 and 0.5 Hz, with a peak amplitude of 2 m/s2 in five separate sessions, approximately 1 week apart. Sickness responses were recorded using both the MIsery SCale (MISC) with 30 s intervals, and the Motion Sickness Assessment Questionnaire (MSAQ) at the end of the motion exposure. The average velocity storage and subjective vertical time constants were 17.2 s (STD = 6.8 s) and 9.2 s (STD = 7.17 s). The average cross-over frequency was 0.21 Hz (STD = 0.10 Hz). At the group level, there was no significant effect of frequency on motion sickness. However, considerable individual variability was observed in frequency sensitivities, with some participants being particularly sensitive to the lowest frequencies, whereas others were most sensitive to intermediate or higher frequencies. The frequency of peak sensitivity did not correlate with the velocity storage time constant (r = 0.32, p = 0.26) or the subjective vertical time constant (r = − 0.37, p = 0.29). Our prediction of a significant correlation between cross-over frequency and frequency sensitivity was not confirmed (r = 0.26, p = 0.44). However, we did observe a strong positive correlation between the subjective vertical time constant and general motion sickness sensitivity (r = 0.74, p = 0.0006). We conclude that frequency sensitivity is best considered a property unique to the individual. This has important consequences for existing models of motion sickness, which were fitted to group averaged sensitivities. The correlation between the subjective vertical time constant and motion sickness sensitivity supports the importance of verticality perception during exposure to translational sickness stimuli.


2002 ◽  
Vol 12 (1) ◽  
pp. 15-23
Author(s):  
Keiko Yasuda ◽  
Hiroaki Fushiki ◽  
Rinnosuke Wada ◽  
Yukio Watanabe

While the stimulation of otolith inputs reduces the duration of postrotatory nystagmus (PRN), there is still room for dialogue about the effect of static tilt on the orientation of PRN. We studied one possible influence of static roll tilt on the spatial orientation of PRN in cats. The animal was rotated about an earth-vertical axis (EVA) at a constant velocity of 100 deg/s with an acceleration and deceleration of 120 deg / s 2 . Within two seconds after stopping EVA rotation, the animal was passively tilted at 45 deg/s about its longitudinal axis by as much as ± 90 deg in steps of 15 deg. Eye movements were measured with magnetic search coils. The angle of the PRN plane and its slow phase eye velocity were measured. The time constant of PRN decreased with an increase in roll tilt. The PRN plane remained earth horizontal within a range of ± 30 deg roll tilt. Beyond this range, the velocity of PRN decreased too rapidly to measure any change in orientation. Our results indicate a spatially limited and temporally short interaction of the semicircular canal and otolith signals in the velocity storage mechanism of cat PRN. Our data, along with previous studies, suggest that different species show different solutions to the problem of the imbalance and spatial disorientation during contradictory stimuli.


2003 ◽  
Vol 89 (1) ◽  
pp. 355-366 ◽  
Author(s):  
Christopher J. Bockisch ◽  
Dominik Straumann ◽  
Thomas Haslwanter

The semi-circular canals and the otolith organs both contribute to gaze stabilization during head movement. We investigated how these sensory signals interact when they provide conflicting information about head orientation in space. Human subjects were reoriented 90° in pitch or roll during long-duration, constant-velocity rotation about the earth-vertical axis while we measured three-dimensional eye movements. After the reorientation, the otoliths correctly indicated the static orientation of the subject with respect to gravity, while the semicircular canals provided a strong signal of rotation. This rotation signal from the canals could only be consistent with a static orientation with respect to gravity if the rotation-axis indicated by the canals was exactly parallel to gravity. This was not true, so a cue-conflict existed. These conflicting stimuli elicited motion sickness and a complex tumbling sensation. Strong horizontal, vertical, and/or torsional eye movements were also induced, allowing us to study the influence of the conflict between the otoliths and the canals on all three eye-movement components. We found a shortening of the horizontal and vertical time constants of the decay of nystagmus and a trend for an increase in peak velocity following reorientation. The dumping of the velocity storage occurred regardless of whether eye velocity along that axis was compensatory to the head rotation or not. We found a trend for the axis of eye velocity to reorient to make the head-velocity signal from the canals consistent with the head-orientation signal from the otoliths, but this reorientation was small and only observed when subjects were tilted to upright. Previous models of canal-otolith interaction could not fully account for our data, particularly the decreased time constant of the decay of nystagmus. We present a model with a mechanism that reduces the velocity-storage component in the presence of a strong cue-conflict. Our study, supported by other experiments, also indicates that static otolith signals exhibit considerably smaller effects on eye movements in humans than in monkeys.


1994 ◽  
Vol 72 (5) ◽  
pp. 2480-2489 ◽  
Author(s):  
D. Tweed ◽  
M. Fetter ◽  
D. Sievering ◽  
H. Misslisch ◽  
E. Koenig

1. Gain matrices were used to quantify the three-dimensional vestibuloocular reflex (VOR) in five human subjects who were accelerated over 1 s and then spun at a constant 150 degrees/s for 29 s in darkness. Rotations were torsional, vertical and horizontal, about earth-vertical and earth-horizontal axes. 2. Elements on the main diagonal of the gain matrices were much smaller than the optimal value of -1, and torsional gain was weaker than vertical or horizontal. Off-diagonal elements, indicating cross talk, were minimal except for a small but consistent horizontal response to torsional head rotation. 3. Downward slow phases were more than twice as fast as upward at the start of rotation about both earth-vertical and earth-horizontal axes, but the asymmetry vanished later in the rotation. 4. During earth-vertical-axis rotation, all matrix elements decayed to zero. The main-diagonal torsional and vertical gains waned with time constants close to that of the cupula (6.7 and 7.3 s). Velocity storage prolonged the horizontal response to horizontal head rotation (time constant 14.2 s) but not the horizontal response to torsion (7.7 s). A simple explanation is that velocity storage acts on a central estimate of head motion that accurately distinguishes horizontal from torsional and that the inappropriate horizontal eye velocity response to torsion occurs because of cross talk downstream from velocity storage. 5. During earth-horizontal-axis rotation, the torsional, vertical, and horizontal main-diagonal elements declined, with time constants of 7.6, 8.2, and 7.9 s, to maintained nonzero values, all equal to about -0.1. Off-diagonal elements, including the horizontal response to torsion, decayed to zero, so that the otolith-driven reflex, late in the rotation, was equally strong in all dimensions and almost free of detectable cross talk. 6. The difference between gain curves over the course of earth-vertical- and earth-horizontal-axis rotations was not constant but increased with time, suggesting that the VOR response to earth-horizontal-axis rotation is not a simple sum of canal and otolith reflexes.


2015 ◽  
Vol 113 (10) ◽  
pp. 3866-3892 ◽  
Author(s):  
James O. Phillips ◽  
Leo Ling ◽  
Kaibao Nie ◽  
Elyse Jameyson ◽  
Christopher M. Phillips ◽  
...  

Animal experiments and limited data in humans suggest that electrical stimulation of the vestibular end organs could be used to treat loss of vestibular function. In this paper we demonstrate that canal-specific two-dimensionally (2D) measured eye velocities are elicited from intermittent brief 2 s biphasic pulse electrical stimulation in four human subjects implanted with a vestibular prosthesis. The 2D measured direction of the slow phase eye movements changed with the canal stimulated. Increasing pulse current over a 0–400 μA range typically produced a monotonic increase in slow phase eye velocity. The responses decremented or in some cases fluctuated over time in most implanted canals but could be partially restored by changing the return path of the stimulation current. Implantation of the device in Meniere's patients produced hearing and vestibular loss in the implanted ear. Electrical stimulation was well tolerated, producing no sensation of pain, nausea, or auditory percept with stimulation that elicited robust eye movements. There were changes in slow phase eye velocity with current and over time, and changes in electrically evoked compound action potentials produced by stimulation and recorded with the implanted device. Perceived rotation in subjects was consistent with the slow phase eye movements in direction and scaled with stimulation current in magnitude. These results suggest that electrical stimulation of the vestibular end organ in human subjects provided controlled vestibular inputs over time, but in Meniere's patients this apparently came at the cost of hearing and vestibular function in the implanted ear.


1992 ◽  
Vol 2 (3) ◽  
pp. 235-245
Author(s):  
S.J. Heinen ◽  
D.K. Oh ◽  
E.L. Keller

Electrical stimulation in the monkey vestibulocerebellum has previously been shown to produce ocular nystagmus, but large stimulating current values were used. Using long duration (⩽10-second) stimulus pulse trains and low current values (<50 μA), we studied the nystagmus evoked by microstimulation in the uvular/nodular regions of the cerebellum. In doing this, we found quantitative differences in the nystagmus evoked from these two regions. Stimulation of the nodulus typically produced a vigorous nystagmus with a contralateral slow phase and a prolonged afternystagmus in the same direction. In contrast, stimulation of the uvula typically produced a regular ipsilateral nystagmus pattern with a very short, if any, afternystagmus in the same direction. In addition, at some stimulation sites in the uvula we observed an adaptation in the slow phase eye velocity during the time that the stimulation remained on. This effect could result in a secondary nystagmus, with a slow phase velocity direction opposite to that first evoked by the stimulation, followed by a prolonged afternystagmus in the direction of the secondary nystagmus at stimulus offset. The nystagmus evoked by these cerebellar stimulations differs from both natural nystagmus produced by large field visual motion and from the nystagmus produced by electrical stimulation of the nucleus of the optic tract. The nystagmus produced by uvular and nodular stimulation shows a shorter latency and a more rapid slow phase eye velocity buildup. The uvula stimulations also showed a much shorter afternystagmus. Also, the same nystagmus was evoked whether the animal was in a lighted or dark surround. These characteristics and recent single-unit recording studies in the uvula seem to suggest that the uvula acts not as a direct input to the velocity storage mechanism, but instead perhaps as part of an internal regulator for balance between the bilateral vestibular nuclei which are normally part of the nystagmus response. On the other hand, the nodulus, with its prolonged afternystagmus in the same direction as the evoked nystagmus, may be involved as a part of the velocity storage mechanism.


1991 ◽  
Vol 1 (4) ◽  
pp. 347-355 ◽  
Author(s):  
S.H. Lafortune ◽  
D.J. Ireland ◽  
R.M. Jell

The effects of static tilts about the roll (anterior-posterior) axis on human horizontal optokinetic afternystagmus (HOKAN) were examined. Static tilts in roll, with subjects lying on their left side, produced significant tilt-dependent HOKAN suppression. Only the slow (indirect pathway) component time constant (1/D) of the double exponential model for human HOKAN decreased with angle of roll tilt. The effect was direction specific in that suppression occurred only following a leftward-going stimulus. These findings provide further support for the postulate that otolith-organ-mediated activity can couple to the horizontal velocity storage mechanism in humans. A slight trend towards a tilt-dependent reduction of coefficient A (initial slow phase velocity of fast component decay) was revealed, suggesting the possibility that otolith-organ-mediated activity could couple to direct (pursuit-mediated?) pathways as well. No horizontal-to-vertical cross-coupling occurred, indicating that this aspect of the 3-dimensional model for velocity storage proposed by Raphan & Cohen (1988) may not completely apply to humans.


1992 ◽  
Vol 67 (5) ◽  
pp. 1158-1170 ◽  
Author(s):  
D. Solomon ◽  
B. Cohen

1. Yaw eye in head (Eh) and head on body velocities (Hb) were measured in two monkeys that ran around the perimeter of a circular platform in darkness. The platform was stationary or could be counterrotated to reduce body velocity in space (Bs) while increasing gait velocity on the platform (Bp). The animals were also rotated while seated in a primate chair at eccentric locations to provide linear and angular accelerations similar to those experienced while running. 2. Both animals had head and eye nystagmus while running in darkness during which slow phase gaze velocity on the body (Gb) partially compensated for body velocity in space (Bs). The eyes, driven by the vestibuloocular reflex (VOR), supplied high-frequency characteristics, bringing Gb up to compensatory levels at the beginning and end of the slow phases. The head provided substantial gaze compensation during the slow phases, probably through the vestibulocollic reflex (VCR). Synchronous eye and head quick phases moved gaze in the direction of running. Head movements occurred consistently only when animals were running. This indicates that active body and limb motion may be essential for inducing the head-eye gaze synergy. 3. Gaze compensation was good when running in both directions in one animal and in one direction in the other animal. The animals had long VOR time constants in these directions. The VOR time constant was short to one side in one animal, and it had poor gaze compensation in this direction. Postlocomotory nystagmus was weaker after running in directions with a long VOR time constant than when the animals were passively rotated in darkness. We infer that velocity storage in the vestibular system had been activated to produce continuous Eh and Hb during running and to counteract postrotatory afterresponses. 4. Continuous compensatory gaze nystagmus was not produced by passive eccentric rotation with the head stabilized or free. This indicates that an aspect of active locomotion, most likely somatosensory feedback, was responsible for activating velocity storage. 5. Nystagmus was compared when an animal ran in darkness and in light. the beat frequency of eye and head nystagmus was lower, and the quick phases were larger in darkness. The duration of head and eye quick phases covaried. Eye quick phases were larger when animals ran in darkness than when they were passively rotated. The maximum velocity and duration of eye quick phases were the same in both conditions. 6. The platform was counterrotated under one monkey in darkness while it ran in the direction of its long vestibular time constant.(ABSTRACT TRUNCATED AT 400 WORDS)


2002 ◽  
Vol 88 (5) ◽  
pp. 2445-2462 ◽  
Author(s):  
Keisuke Kushiro ◽  
Mingjia Dai ◽  
Mikhail Kunin ◽  
Sergei B. Yakushin ◽  
Bernard Cohen ◽  
...  

Nystagmus induced by off-vertical axis rotation (OVAR) about a head yaw axis is composed of a yaw bias velocity and modulations in eye position and velocity as the head changes orientation relative to gravity. The bias velocity is dependent on the tilt of the rotational axis relative to gravity and angular head velocity. For axis tilts <15°, bias velocities increased monotonically with increases in the magnitude of the projected gravity vector onto the horizontal plane of the head. For tilts of 15–90°, bias velocity was independent of tilt angle, increasing linearly as a function of head velocity with gains of 0.7–0.8, up to the saturation level of velocity storage. Asymmetries in OVAR bias velocity and asymmetries in the dominant time constant of the angular vestibuloocular reflex (aVOR) covaried and both were reduced by administration of baclofen, a GABAB agonist. Modulations in pitch and roll eye positions were in phase with nose-down and side-down head positions, respectively. Changes in roll eye position were produced mainly by slow movements, whereas vertical eye position changes were characterized by slow eye movements and saccades. Oscillations in vertical and roll eye velocities led their respective position changes by ≈90°, close to an ideal differentiation, suggesting that these modulations were due to activation of the orienting component of the linear vestibuloocular reflex (lVOR). The beating field of the horizontal nystagmus shifted the eyes 6.3°/ g toward gravity in side down position, similar to the deviations observed during static roll tilt (7.0°/ g). This demonstrates that the eyes also orient to gravity in yaw. Phases of horizontal eye velocity clustered ∼180° relative to the modulation in beating field and were not simply differentiations of changes in eye position. Contributions of orientating and compensatory components of the lVOR to the modulation of eye position and velocity were modeled using three components: a novel direct otolith-oculomotor orientation, orientation-based velocity modulation, and changes in velocity storage time constants with head position re gravity. Time constants were obtained from optokinetic after-nystagmus, a direct representation of velocity storage. When the orienting lVOR was combined with models of the compensatory lVOR and velocity estimator from sequential otolith activation to generate the bias component, the model accurately predicted eye position and velocity in three dimensions. These data support the postulates that OVAR generates compensatory eye velocity through activation of velocity storage and that oscillatory components arise predominantly through lVOR orientation mechanisms.


2019 ◽  
Vol 121 (5) ◽  
pp. 1865-1878 ◽  
Author(s):  
A. M. Pastor ◽  
P. M. Calvo ◽  
R. R. de la Cruz ◽  
R. Baker ◽  
H. Straka

Computational capability and connectivity are key elements for understanding how central vestibular neurons contribute to gaze-stabilizing eye movements during self-motion. In the well-characterized and segmentally distributed hindbrain oculomotor network of goldfish, we determined afferent and efferent connections along with discharge patterns of descending octaval nucleus (DO) neurons during different eye motions. Based on activity correlated with horizontal eye and head movements, DO neurons were categorized into two complementary groups that either increased discharge during both contraversive (type II) eye (e) and ipsiversive (type I) head (h) movements (eIIhI) or vice versa (eIhII). Matching time courses of slow-phase eye velocity and corresponding firing rates during prolonged visual and head rotation suggested direct causality in generating extraocular motor commands. The axons of the dominant eIIhI subgroup projected either ipsi- or contralaterally and terminated in the abducens nucleus, Area II, and Area I with additional recurrent collaterals of ipsilaterally projecting neurons within the parent nucleus. Distinct feedforward commissural pathways between bilateral DO neurons likely contribute to the generation of eye velocity signals in eIhII cells. The shared contribution of DO and Area II neurons to eye velocity storage likely represents an ancestral condition in goldfish that is clearly at variance with the task separation between mammalian medial vestibular and prepositus hypoglossi neurons. This difference in signal processing between fish and mammals might correlate with a larger repertoire of visuo-vestibular-driven eye movements in the latter species that potentially required a shift in sensitivity and connectivity within the hindbrain-cerebello-oculomotor network. NEW & NOTEWORTHY We describe the structure and function of neurons within the goldfish descending octaval nucleus. Our findings indicate that eye and head velocity signals are processed by vestibular and Area II velocity storage integrator circuitries whereas the velocity-to-position Area I neural integrator generates eye position solely. This ancestral condition differs from that of mammals, in which vestibular neurons generally lack eye position signals that are processed and stored within the nucleus prepositus hypoglossi.


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