scholarly journals Dependence of the Roll Angular Vestibuloocular Reflex (aVOR) on Gravity

2009 ◽  
Vol 102 (5) ◽  
pp. 2616-2626 ◽  
Author(s):  
Sergei B. Yakushin ◽  
Yongqing Xiang ◽  
Bernard Cohen ◽  
Theodore Raphan

Little is known about the dependence of the roll angular vestibuloocular reflex (aVOR) on gravity or its gravity-dependent adaptive properties. To study gravity-dependent characteristics of the roll aVOR, monkeys were oscillated about a naso-occipital axis in darkness while upright or tilted. Roll aVOR gains were largest in the upright position and decreased by 7–15% as animals were tilted from the upright. Thus the unadapted roll aVOR gain has substantial gravitational dependence. Roll gains were also decreased or increased by 0.25 Hz, in- or out-of-phase rotation of the head and the visual surround while animals were prone, supine, upright, or in side-down positions. Gain changes, determined as a function of head tilt, were fit with a sinusoid; the amplitudes represented the amount of the gravity-dependent gain change, and the bias, the gravity-independent gain change. Gravity-dependent gain changes were absent or substantially smaller in roll (≈5%) than in yaw (25%) or pitch (17%), whereas gravity-independent gain changes were similar for roll, pitch, and yaw (≈20%). Thus the high-frequency roll aVOR gain has an inherent dependence on head orientation re gravity in the unadapted state, which is different from the yaw/pitch aVORs. This inherent gravitational dependence may explain why the adaptive circuits are not active when the head is tilted re gravity during roll aVOR adaptation. These behavioral differences support the idea that there is a fundamental difference in the central organization of canal-otolith convergence of the roll and yaw/pitch aVORs.

1997 ◽  
Vol 78 (4) ◽  
pp. 1775-1790 ◽  
Author(s):  
Laura Telford ◽  
Scott H. Seidman ◽  
Gary D. Paige

Telford, Laura, Scott H. Seidman, and Gary D. Paige. Dynamics of squirrel monkey linear vestibuloocular reflex and interactions with fixation distance. J. Neurophysiol. 78: 1775–1790, 1997. Horizontal, vertical, and torsional eye movements were recorded using the magnetic search-coil technique during linear accelerations along the interaural (IA) and dorsoventral (DV) head axes. Four squirrel monkeys were translated sinusoidally over a range of frequencies (0.5–4.0 Hz) and amplitudes (0.1–0.7 g peak acceleration). The linear vestibuloocular reflex (LVOR) was recorded in darkness after brief presentations of visual targets at various distances from the subject. With subjects positioned upright or nose-up relative to gravity, IA translations generated conjugate horizontal (IA horizontal) eye movements, whereas DV translations with the head nose-up or right-side down generated conjugate vertical (DV vertical) responses. Both were compensatory for linear head motion and are thus translational LVOR responses. In concert with geometric requirements, both IA-horizontal and DV-vertical response sensitivities (in deg eye rotation/cm head translation) were related linearly to reciprocal fixation distance as measured by vergence (in m−1, or meter-angles, MA). The relationship was characterized by linear regressions, yielding sensitivity slopes (in deg⋅cm−1⋅MA−1) and intercepts (sensitivity at 0 vergence). Sensitivity slopes were greatest at 4.0 Hz, but were only slightly more than half the ideal required to maintain fixation. Slopes declined with decreasing frequency, becoming negligible at 0.5 Hz. Small responses were observed when vergence was zero (intercept), although no response is required. Like sensitivity slope, the intercept was largest at 4.0 Hz and declined with decreasing frequency. Phase lead was near zero (compensatory) at 4.0 Hz, but increased as frequency declined. Changes in head orientation, motion axis (IA vs. DV), and acceleration amplitude produced slight and sporadic changes in LVOR parameters. Translational LVOR response characteristics are consistent with high-pass filtering within LVOR pathways. Along with horizontal eye movements, IA translation generated small torsional responses. In contrast to the translational LVORs, IA-torsional responses were not systematically modulated by vergence angle. The IA-torsional LVOR is not compensatory for translation because it cannot maintain image stability. Rather, it likely compensates for the effective head tilt simulated by translation. When analyzed in terms of effective head tilt, torsional responses were greatest at the lowest frequency and declined as frequency increased, consistent with low-pass filtering of otolith input. It is unlikely that IA-torsional responses compensate for actual head tilt, however, because they were similar for both upright and nose-up head orientations. The IA-torsional and -horizontal LVORs seem to respond only to linear acceleration along the IA head axis, and the DV-vertical LVOR to acceleration along the head's DV axis, regardless of gravity.


2003 ◽  
Vol 89 (1) ◽  
pp. 571-586 ◽  
Author(s):  
Sergei B. Yakushin ◽  
Theodore Raphan ◽  
Bernard Cohen

The gain of the vertical angular vestibuloocular reflex (aVOR) was adaptively altered by visual-vestibular mismatch during rotation about an interaural axis, using steps of velocity in three head orientations: upright, left-side down, and right-side down. Gains were decreased by rotating the animal and visual surround in the same direction and increased by visual and surround rotation in opposite directions. Gains were adapted in one head position (single-state adaptation) or decreased with one side down and increased with the other side down (dual-state adaptation). Animals were tested in darkness using sinusoidal rotation at 0.5 Hz about an interaural axis that was tilted from horizontal to vertical. They were also sinusoidally oscillated from 0.5 to 4 Hz about a spatial vertical axis in static tilt positions from yaw to pitch. After both single- and dual-state adaptation, gain changes were maximal when the monkeys were in the position in which the gain had been adapted, and the gain changes progressively declined as the head was tilted away from that position. We call this gravity-specific aVOR gain adaptation. The spatial distribution of the specific aVOR gain changes could be represented by a cosine function that was superimposed on a bias level, which we called gravity-independent gain adaptation. Maximal gravity-specific gain changes were produced by 2–4 h of adaptation for both single- and dual-state adaptations, and changes in gain were similar at all test frequencies. When adapted while upright, the magnitude and distribution of the gravity-specific adaptation was comparable to that when animals were adapted in side-down positions. Single-state adaptation also produced gain changes that were independent of head position re gravity particularly in association with gain reduction. There was no bias after dual-state adaptation. With this difference, fits to data obtained by altering the gain in separate sessions predicted the modulations in gain obtained from dual-state adaptations. These data show that the vertical aVOR gain changes dependent on head position with regard to gravity are continuous functions of head tilt, whose spatial phase depends on the position in which the gain was adapted. From their different characteristics, it is likely that gravity-specific and gravity-independent adaptive changes in gain are produced by separate neural processes. These data demonstrate that head orientation to gravity plays an important role in both orienting and tuning the gain of the vertical aVOR.


1999 ◽  
Vol 82 (3) ◽  
pp. 1271-1285 ◽  
Author(s):  
David M. Lasker ◽  
Douglas D. Backous ◽  
Anna Lysakowski ◽  
Griffin L. Davis ◽  
Lloyd B. Minor

The horizontal angular vestibuloocular reflex (VOR) evoked by high-frequency, high-acceleration rotations was studied in four squirrel monkeys after unilateral plugging of the three semicircular canals. During the period (1–4 days) that animals were kept in darkness after plugging, the gain during steps of acceleration (3,000°/s2, peak velocity = 150°/s) was 0.61 ± 0.14 (mean ± SD) for contralesional rotations and 0.33 ± 0.03 for ipsilesional rotations. Within 18–24 h after animals were returned to light, the VOR gain for contralesional rotations increased to 0.88 ± 0.05, whereas there was only a slight increase in the gain for ipsilesional rotations to 0.37 ± 0.07. A symmetrical increase in the gain measured at the plateau of head velocity was noted after animals were returned to light. The latency of the VOR was 8.2 ± 0.4 ms for ipsilesional and 7.1 ± 0.3 ms for contralesional rotations. The VOR evoked by sinusoidal rotations of 0.5–15 Hz, ±20°/s had no significant half-cycle asymmetries. The recovery of gain for these responses after plugging was greater at lower than at higher frequencies. Responses to rotations at higher velocities for frequencies ≥4 Hz showed an increase in contralesional half-cycle gain, whereas ipsilesional half-cycle gain was unchanged. A residual response that appeared to be canal and not otolith mediated was noted after plugging of all six semicircular canals. This response increased with frequency to reach a gain of 0.23 ± 0.03 at 15 Hz, resembling that predicted based on a reduction of the dominant time constant of the canal to 32 ms after plugging. A model incorporating linear and nonlinear pathways was used to simulate the data. The coefficients of this model were determined from data in animals with intact vestibular function. Selective increases in the gain for the linear and nonlinear pathways predicted the changes in recovery observed after canal plugging. An increase in gain of the linear pathway accounted for the recovery in VOR gain for both responses at the velocity plateau of the steps of acceleration and for the sinusoidal rotations at lower peak velocities. The increase in gain for contralesional responses to steps of acceleration and sinusoidal rotations at higher frequencies and velocities was due to an increase in the gain of the nonlinear pathway. This pathway was driven into inhibitory cutoff at low velocities and therefore made no contribution for rotations toward the ipsilesional side.


2004 ◽  
Vol 96 (6) ◽  
pp. 2333-2340 ◽  
Author(s):  
Tomi Laitinen ◽  
Leo Niskanen ◽  
Ghislaine Geelen ◽  
Esko Länsimies ◽  
Juha Hartikainen

In elderly subjects, heart rate responses to postural change are attenuated, whereas their vascular responses are augmented. Altered strategy in maintaining blood pressure homeostasis during upright position may result from various cardiovascular changes, including age-related cardiovascular autonomic dysfunction. This exploratory study was conducted to evaluate impact of age on cardiovascular autonomic responses to head-up tilt (HUT) in healthy subjects covering a wide age range. The study population consisted of 63 healthy, normal-weight, nonsmoking subjects aged 23–77 yr. Five-minute electrocardiogram and finger blood pressure recordings were performed in the supine position and in the upright position 5 min after 70° HUT. Stroke volume was assessed from noninvasive blood pressure signals by the arterial pulse contour method. Heart rate variability (HRV) and systolic blood pressure variability (SBPV) were analyzed by using spectral analysis, and baroreflex sensitivity (BRS) was assessed by using sequence and cross-spectral methods. Cardiovascular autonomic activation during HUT consisted of decreases in HRV and BRS and an increase in SBPV. These changes became attenuated with aging. Age correlated significantly with amplitude of HUT-stimulated response of the high-frequency component ( r = -0.61, P < 0.001) and the ratio of low-frequency to high-frequency power of HRV ( r = -0.31, P < 0.05) and indexes of BRS (local BRS: r = -0.62, P < 0.001; cross-spectral baroreflex sensitivity in the low-frequency range: r = -0.38, P < 0.01). Blood pressure in the upright position was maintained well irrespective of age. However, the HUT-induced increase in heart rate was more pronounced in the younger subjects, whereas the increase in peripheral resistance was predominantly observed in the older subjects. Thus it is likely that whereas the dynamic capacity of cardiac autonomic regulation decreases, vascular responses related to vasoactive mechanisms and vascular sympathetic regulation become augmented with increasing age.


2002 ◽  
Vol 88 (1) ◽  
pp. 13-28 ◽  
Author(s):  
Marko Huterer ◽  
Kathleen E. Cullen

For frequencies >10 Hz, the vestibuloocular reflex (VOR) has been primarily investigated during passive rotations of the head on the body in humans. These prior studies suggest that eye movements lag head movements, as predicted by a 7-ms delay in the VOR reflex pathways. However, Minor and colleagues recently applied whole-body rotations of frequencies ≤15 Hz in monkeys and found that eye movements were nearly in phase with head motion across all frequencies. The goal of the present study was to determine whether VOR response dynamics actually differ significantly for whole-body versus head-on-body rotations. To address this question, we evaluated the gain and phase of the VOR induced by high-frequency oscillations of the head on the body in monkeys by directly measuring both head and eye movements using the magnetic search coil technique. A torque motor was used to rotate the heads of three Rhesus monkeys over the frequency range 5–25 Hz. Peak head velocity was held constant, first at ±50°/s and then ±100°/s. The VOR was found to be essentially compensatory across all frequencies; gains were near unity (1.1 at 5 Hz vs. 1.2 at 25 Hz), and phase lag increased only slightly with frequency (from 2° at 5 Hz to 11° at 25 Hz, a marked contrast to the 63° lag at 25 Hz predicted by a 7-ms VOR latency). Furthermore, VOR response dynamics were comparable in darkness and when viewing a target and did not vary with peak velocity. Although monkeys offered less resistance to the initial cycles of applied head motion, the gain and phase of the VOR did not vary for early versus late cycles, suggesting that an efference copy of the motor command to the neck musculature did not alter VOR response dynamics. In addition, VOR dynamics were also probed by applying transient head perturbations with much greater accelerations (peak acceleration >15,000°/s2) than have been previously employed. The VOR latency was between 5 and 6 ms, and mean gain was close to unity for two of the three animals tested. A simple linear model well described the VOR responses elicited by sinusoidal and transient head on body rotations. We conclude that the VOR is compensatory over a wide frequency range in monkeys and has similar response dynamics during passive rotation of the head on body as during passive rotation of the whole body in space.


2006 ◽  
Vol 96 (6) ◽  
pp. 3349-3361 ◽  
Author(s):  
Yongqing Xiang ◽  
Sergei B. Yakushin ◽  
Bernard Cohen ◽  
Theodore Raphan

A neural network model was developed to explain the gravity-dependent properties of gain adaptation of the angular vestibuloocular reflex (aVOR). Gain changes are maximal at the head orientation where the gain is adapted and decrease as the head is tilted away from that position and can be described by the sum of gravity-independent and gravity-dependent components. The adaptation process was modeled by modifying the weights and bias values of a three-dimensional physiologically based neural network of canal–otolith-convergent neurons that drive the aVOR. Model parameters were trained using experimental vertical aVOR gain values. The learning rule aimed to reduce the error between eye velocities obtained from experimental gain values and model output in the position of adaptation. Although the model was trained only at specific head positions, the model predicted the experimental data at all head positions in three dimensions. Altering the relative learning rates of the weights and bias improved the model-data fits. Model predictions in three dimensions compared favorably with those of a double-sinusoid function, which is a fit that minimized the mean square error at every head position and served as the standard by which we compared the model predictions. The model supports the hypothesis that gravity-dependent adaptation of the aVOR is realized in three dimensions by a direct otolith input to canal–otolith neurons, whose canal sensitivities are adapted by the visual-vestibular mismatch. The adaptation is tuned by how the weights from otolith input to the canal–otolith-convergent neurons are adapted for a given head orientation.


1992 ◽  
Vol 656 (1 Sensing and C) ◽  
pp. 305-314 ◽  
Author(s):  
R. JOHN LEIGH ◽  
ROBERT N. SAWYER ◽  
MICHAEL P. GRANT ◽  
SCOTT H. SEIDMAN

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