Gravity-Specific Adaptation of the Angular Vestibuloocular Reflex: Dependence on Head Orientation With Regard to Gravity

2003 ◽  
Vol 89 (1) ◽  
pp. 571-586 ◽  
Author(s):  
Sergei B. Yakushin ◽  
Theodore Raphan ◽  
Bernard Cohen
Keyword(s):  
Head Tilt ◽  
Vertical Axis ◽  
Continuous Functions ◽  
Head Position ◽  
Head Orientation ◽  
Vestibuloocular Reflex ◽  
Specific Adaptation ◽  
Gain Adaptation ◽  
Bias Level ◽  
Single State

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.

Context-Specific Adaptation of the Vertical Vestibuloocular Reflex With Regard to Gravity

2000 ◽  
Vol 84 (6) ◽  
pp. 3067-3071 ◽  
Author(s):  
Sergei B. Yakushin ◽  
Theodore Raphan ◽  
Bernard Cohen
Keyword(s):  
Head Movement ◽  
Contralateral Side ◽  
Head Position ◽  
Head Orientation ◽  
Vestibuloocular Reflex ◽  
Ipsilateral Side ◽  
Specific Adaptation ◽  
Specific Effects ◽  
Gain Adaptation ◽  
Context Specific

We determined whether head position with regard to gravity is an important context for angular vestibuloocular reflex (aVOR) gain adaptation. Vertical aVOR gains were adapted with monkeys upright or on side by rotating the animals about an interaural axis in phase or out of phase with the visual surround for 4 h. When aVOR gains were adapted with monkeys upright, gain changes were symmetrical when tested in either on-side position (23 ± 7%; mean ± SD). After on-side adaptation, however, gain changes were always larger when animals were tested in the same on-side position in which they were adapted. Gain changes were 43 ± 16% with ipsilateral side down and 9 ± 8% with contralateral side down. The context-specific effects of head position on vertical aVOR gain were the same whether the gain was increased or decreased. The data indicate that vertical aVOR gain changes are stored in the context of the head orientation in which changes were induced. This association could be an important context for expressing the adapted state of the aVOR gain during vertical head movement.

Spatial Distribution of Gravity-Dependent Gain Changes in the Vestibuloocular Reflex

2005 ◽  
Vol 93 (6) ◽  
pp. 3693-3698 ◽  
Author(s):  
Sergei B. Yakushin ◽  
Yongqing Xiang ◽  
Theodore Raphan ◽  
Bernard Cohen
Keyword(s):  
Dimensional Space ◽  
Three Dimensional ◽  
Head Tilt ◽  
Fundamental Property ◽  
Head Position ◽  
Three Dimensions ◽  
Vestibuloocular Reflex ◽  
Gain Adaptation ◽  
The Stability ◽  
Three Dimensional Space

This study determined whether dependence of angular vestibuloocular reflex (aVOR) gain adaptation on gravity is a fundamental property in three dimensions. Horizontal aVOR gains were adaptively increased or decreased in two cynomolgus monkeys in upright, side down, prone, and supine positions, and aVOR gains were tested in darkness by yaw rotation with the head in a wide variety of orientations. Horizontal aVOR gain changes peaked at the head position in which the adaptation took place and gradually decreased as the head moved away from this position in any direction. The gain changes were plotted as a function of head tilt and fit with a sinusoid plus a bias to obtain the gravity-dependent (amplitude) and gravity-independent (bias) components. Peak-to-peak gravity-dependent gain changes in planes containing the position of adaptation and the magnitude of the gravity-independent components were both ∼25%. We assumed that gain changes over three-dimensional space could be described by a sinusoid the amplitude of which also varied sinusoidally. Using gain changes obtained from the head position in which the gains were adapted, a three-dimensional surface was generated that was qualitatively similar to a surface obtained from the experimental data. This extends previous findings on vertical aVOR gain adaptation in one plane and introduces a conceptual framework for understanding plasticity in three dimensions: aVOR gain changes are composed of two components, one of which depends on head position relative to gravity. It is likely that this gravitational dependence optimizes the stability of retinal images during movement in three-dimensional space.

scholarly journals Angular vestibuloocular reflex responses in Otop1 mice. I. Otolith sensor input is essential for gravity context-specific adaptation

2019 ◽  
Vol 121 (6) ◽  
pp. 2291-2299 ◽  
Author(s):  
Serajul I. Khan ◽  
Charles C. Della Santina ◽  
Americo A. Migliaccio
Keyword(s):  
Semicircular Canals ◽  
Vertical Axis ◽  
Neural Circuitry ◽  
Vestibuloocular Reflex ◽  
Training Context ◽  
Specific Adaptation ◽  
Axis Parallel ◽  
Vor Adaptation ◽  
Context Specific

The role of the otoliths in mammals in the angular vestibuloocular reflex (VOR) has been difficult to determine because there is no surgical technique that can reliably ablate them without damaging the semicircular canals. The Otopetrin1 (Otop1) mouse lacks functioning otoliths because of failure to develop otoconia but seems to have otherwise normal peripheral anatomy and neural circuitry. By using these animals we sought to determine the role of the otoliths in angular VOR baseline function and adaptation. In six Otop1 mice and six control littermates we measured baseline ocular countertilt about the three primary axes in head coordinates; baseline horizontal (rotation about an Earth-vertical axis parallel to the dorsal-ventral axis) and vertical (rotation about an Earth-vertical axis parallel to the interaural axis) sinusoidal (0.2–10 Hz, 20–100°/s) VOR gain (= eye/head velocity); and the horizontal and vertical VOR after gain-increase (1.5×) and gain-decrease (0.5×) adaptation training. Countertilt responses were significantly reduced in Otop1 mice. Baseline horizontal and vertical VOR gains were similar between mouse types, and so was horizontal VOR adaptation. For control mice, vertical VOR adaptation was evident when the testing context, left ear down (LED) or right ear down (RED), was the same as the training context (LED or RED). For Otop1 mice, VOR adaptation was evident regardless of context. Our results suggest that the otolith translational signal does not contribute to the baseline angular VOR, probably because the mouse VOR is highly compensatory, and does not alter the magnitude of adaptation. However, we show that the otoliths are important for gravity context-specific angular VOR adaptation. NEW & NOTEWORTHY This is the first study examining the role of the otoliths (defined here as the utricle and saccule) in adaptation of the angular vestibuloocular reflex (VOR) in an animal model in which the otoliths are reliably inactivated and the semicircular canals preserved. We show that they do not contribute to adaptation of the normal angular VOR. However, the otoliths provide the main cue for gravity context-specific VOR adaptation.

Dynamics of Squirrel Monkey Linear Vestibuloocular Reflex and Interactions with Fixation Distance

1997 ◽  
Vol 78 (4) ◽  
pp. 1775-1790 ◽  
Author(s):  
Laura Telford ◽  
Scott H. Seidman ◽  
Gary D. Paige
Keyword(s):  
Eye Movements ◽  
Squirrel Monkey ◽  
Head Tilt ◽  
Linear Acceleration ◽  
Head Orientation ◽  
Vestibuloocular Reflex ◽  
Response Characteristics ◽  
Fixation Distance ◽  
Eye Rotation ◽  
Low Pass

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.

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
Keyword(s):  
High Frequency ◽  
Head Tilt ◽  
Upright Position ◽  
Head Orientation ◽  
Vestibuloocular Reflex ◽  
Behavioral Differences ◽  
Adaptive Circuits ◽  
Phase Rotation ◽  
Central Organization ◽  
Gain Change

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.

The Goldmeier Effect in Adults and Children: Environmental, Retinal, and Phenomenal Influences on Judgments of Visual Symmetry

Perception ◽  
1987 ◽  
Vol 16 (1) ◽  
pp. 29-39 ◽  
Author(s):  
Celia B Fisher ◽  
Maria P Fracasso
Keyword(s):  
Age Groups ◽  
Head Tilt ◽  
Head Rotation ◽  
Vertical Axis ◽  
Horizontal Axis ◽  
Head Orientation ◽  
Stimulus Complexity ◽  
Adults And Children ◽  
Symmetry Perception ◽  
Retinal Information

Adults judge that patterns symmetrical about the vertical axis are more similar to standard patterns symmetrical about both major orthogonal axes than are patterns which are symmetrical only about the horizontal axis (the Goldmeier effect). Thus, symmetry about the vertical axis is more salient for adults than symmetry about the horizontal axis. Two experiments are reported in which subjects from three age groups (preschool, 8 years old, and adult) were given Goldmeier problems under different conditions. In experiment 1 three head-tilt conditions were used (0°, 45°, 90°); in experiment 2 there were four conditions defined by head orientation (0°, 90°) and phenomenal instructions (top of figure at 0° or at 90°). In both experiments, increasing head tilt from 0° decreased the consistency with which the environmentally vertical pattern was chosen. Noncorrespondence between the three spatial frameworks (environmental, retinal, and phenomenal) failed to produce biases in favor of either retinal-egocentric or phenomenal systems. For rotated adult subjects in experiment 2, 0° phenomenal instructions strengthened an environmental bias, and 90° phenomenal instructions shifted responses toward a retinal bias. These findings provide strong refutation of explanations for symmetry perception that are based solely upon the anatomical symmetry of the visual system. The data also fail to support arguments for environmental or phenomenal frameworks as singular influences. The results are best explained in terms of failure of constancy mechanisms to coordinate environmental and retinal information as a function of degree of head rotation and stimulus complexity.

Responses of Monkey Vestibular-Only Neurons to Translation and Angular Rotation

2006 ◽  
Vol 96 (6) ◽  
pp. 2915-2930 ◽  
Author(s):  
Wu Zhou ◽  
Bing Feng Tang ◽  
Shawn D. Newlands ◽  
W. M. King
Keyword(s):  
Head Tilt ◽  
High Sensitivity ◽  
Vertical Axis ◽  
Head Movements ◽  
Head Orientation ◽  
Angular Rotation ◽  
Discharge Rates ◽  
Static Head ◽  
Low Sensitivity ◽  
Head Translation

Single-unit recordings were obtained from central vestibular neurons in three monkeys during passive head movements. Neurons that discharged in relation to head translation or changes in head orientation, but not eye movement (“vestibular-only,” n = 154), were examined in detail. Neuronal discharge rates were analyzed during four stimulus conditions: sinusoidal head translation in the horizontal plane (0.2–4 Hz, 0.2 g peak acceleration), static head tilt in the vertical plane (±20°), oscillatory head tilt (0.5–2 Hz), and sinusoidal angular rotation about an earth-vertical axis (0.5 or 1 Hz). Vestibular-only cells were divided into two groups based on the regularity of their spontaneous discharge rates (CV*). One group (low-sensitivity units) exhibited regular discharge rates (CV* < 0.2), weak discharge modulation during head translation (<25 spikes · s−1 · g−1 at f = 1 Hz), and persistent discharge rates related to static head tilt (0.68 spikes · s−1 · °−1 of head tilt). The second group (high sensitivity neurons) exhibited irregular discharge rates (CV* > 0.2), strong discharge modulation during head translation (∼100 spikes · s−1 · g−1 at f = 1 Hz), and little or no change in discharge rate during static head tilt (0.32 spikes · s−1 · °−1). The firing rates of some neurons in both groups were modulated during rotation about an earth-vertical axis (42%), but the modulation was greater for neurons classified as high sensitivity units. Previous reports have described neurons similar to the high sensitivity group; however, the low sensitivity or tilt neurons have not previously been characterized. Significantly, recent theoretical models have predicted neurons with discharge patterns similar to those of low- and high-sensitivity neurons.

Modeling 3-D Slow Phase Velocity Estimation During Off-Vertical-Axis Rotation (OVAR)

1992 ◽  
Vol 2 (1) ◽  
pp. 1-14
Author(s):  
Charles Schnabolk ◽  
Theodore Raphan
Keyword(s):  
Polarization Vector ◽  
Vertical Axis ◽  
Cross Product ◽  
Interesting Property ◽  
Velocity Estimation ◽  
Three Dimensions ◽  
Slow Phase ◽  
Head Orientation ◽  
Head Velocity ◽  
Axis Rotation

Off-vertical-axis rotation (OVAR) in darkness generates continuous compensatory eye velocity. No model has yet been presented that defines the signal processing necessary to estimate head velocity in three dimensions for arbitrary rotations during OVAR. The present study develops a model capable of estimating all 3 components of head velocity in space accurately. It shows that processing of two patterns of otolith activation, one delayed with respect to the other, for each plane of eye movement is not sufficient. (A pattern in this context is an array of signals emanating from the otoliths. Each component of the array is a signal corresponding to a class of otolith hair cells with a given polarization vector as described by Tou and Gonzalez in 1974.) The key result is that estimation of head velocity in space can be achieved by processing three temporally displaced patterns, each representing a sampling of gravity as the head rotates. A vector cross product of differences between pairs of the sampled gravity vectors implements the estimation. An interesting property of this model is that the component of velocity about the axis of rotation reduces to that derived previously using the pattern estimator model described by Raphan and Schnabolk in 1988 and Fanelli et al in 1990. This study suggests that the central nervous system (CNS) maintains a current as well as 2 delayed representations of gravity at every head orientation during rotation. It also suggests that computing vector cross products and implementing delays may be fundamental operations in the CNS for generating orientation information associated with motion.

Rapid horizontal gaze movement in the monkey

1995 ◽  
Vol 73 (4) ◽  
pp. 1632-1652 ◽  
Author(s):  
J. O. Phillips ◽  
L. Ling ◽  
A. F. Fuchs ◽  
C. Siebold ◽  
J. J. Plorde
Keyword(s):  
Eye Movement ◽  
Head Movement ◽  
Vertical Axis ◽  
Head Position ◽  
Head Movements ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Small Correction ◽  
Horizontal Gaze

1. We studied horizontal eye and head movements in three monkeys that were trained to direct their gaze (eye position in space) toward jumping targets while their heads were both fixed and free to rotate about a vertical axis. We considered all gaze movements that traveled > or = 80% of the distance to the new visual target. 2. The relative contributions and metrics of eye and head movements to the gaze shift varied considerably from animal to animal and even within animals. Head movements could be initiated early or late and could be large or small. The eye movements of some monkeys showed a consistent decrease in velocity as the head accelerated, whereas others did not. Although all gaze shifts were hypometric, they were more hypometric in some monkeys than in others. Nevertheless, certain features of the gaze shift were identifiable in all monkeys. To identify those we analyzed gaze, eye in head position, and head position, and their velocities at three points in time during the gaze shift: 1) when the eye had completed its initial rotation toward the target, 2) when the initial gaze shift had landed, and 3) when the head movement was finished. 3. For small gaze shifts (< 20 degrees) the initial gaze movement consisted entirely of an eye movement because the head did not move. As gaze shifts became larger, the eye movement contribution saturated at approximately 30 degrees and the head movement contributed increasingly to the initial gaze movement. For the largest gaze shifts, the eye usually began counterrolling or remained stable in the orbit before gaze landed. During the interval between eye and gaze end, the head alone carried gaze to completion. Finally, when the head movement landed, it was almost aimed at the target and the eye had returned to within 10 +/- 7 degrees, mean +/- SD, of straight ahead. Between the end of the gaze shift and the end of the head movement, gaze remained stable in space or a small correction saccade occurred. 4. Gaze movements < 20 degrees landed accurately on target whether the head was fixed or free. For larger target movements, both head-free and head-fixed gaze shifts became increasingly hypometric. Head-free gaze shifts were more accurate, on average, but also more variable. This suggests that gaze is controlled in a different way with the head free. For target amplitudes < 60 degrees, head position was hypometric but the error was rather constant at approximately 10 degrees.(ABSTRACT TRUNCATED AT 400 WORDS)

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