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Vestibulo-ocular response of human subjects seated in a pivoting support system during 3 Gz centrifuge stimulation.

The vestibulo-ocular reflex (VOR) and spatial orientation perceptions were recorded in 15 subjects during 3 Gz centrifuge runs. These data were obtained to study two issues: (1) to gain insight into reports of asymmetrical disorientation and disturbance during acceleration and deceleration of centrifuge runs like those used to train pilots on the procedures to counteract G-induced loss of consciousness (G-LOC); (2) to study the effects of sustained vertical linear acceleration on the vestibular system. The centrifuge angular velocity profile consisted of a 19 s angular acceleration to 3 Gz that was sustained for 5 min during a period of constant angular velocity, and a 19 s deceleration to 1 Gz. The runs were repeated three times with the subject facing the motion and three times with the subject's back to the motion. The VOR and spatial orientation perceptions from the eight subjects who completed all six runs were analyzed. The total VOR response during acceleration and deceleration was composed of interacting angular (AVOR) and linear components (LVOR). Asymmetries in pitch orientation perception between centrifuge acceleration and decleration were not matched by asymmetries in the total VOR slow phase velocity. During the constant velocity high-G phase of the run, sustained up-beating LVOR (Lz nystagmus) was present in 14 of the 15 subjects. Significant individual differences in Lz nystagmus were found, but the maximum Lz response in our 15 subjects was probably of insufficient magnitude to degrade visual scan of cockpit instruments. Mean magnitudes ranged from 0 to 10 deg/s at 90 s from onset of centrifuge run.

Adult↗

Temporal dynamics of ocular position dependence of the initial human vestibulo-ocular reflex.

PURPOSE: While an ideal vestibulo-ocular reflex (VOR) generates ocular rotations compensatory for head motion, during visually guided movements, Listing's Law (LL) constrains the eye to rotational axes lying in Listing's Plane (LP). The present study was conducted to explore the recent proposal that the VOR's rotational axis is not collinear with the head's, but rather follows a time-dependent strategy intermediate between LL and an ideal VOR. METHODS: Binocular LPs were defined during visual fixation in eight normal humans. The VOR was evoked by a highly repeatable transient whole-body yaw rotation in darkness at a peak acceleration of 2800 deg/s2. Immediately before rotation, subjects regarded targets 15 or 500 cm distant located at eye level, 20 degrees up, or 20 degrees down. Eye and head responses were compared with LL predictions in the position and velocity domains. RESULTS: LP orientation varied both among subjects and between individual subject's eyes, and rotated temporally with convergence by 5 +/- 5 degrees (+/-SEM). In the position domain, the eye compensated for head displacement even when the head rotated out of LP. Even within the first 20 ms from onset of head rotation, the ocular velocity axis tilted relative to the head axis by 30% +/- 8% of vertical gaze position. Saccades increased this tilt. Regardless of vertical gaze position, the ocular rotation axis tilted backward 4 degrees farther in abduction than in adduction. There was also a binocular vertical eye velocity transient and lateral tilt of the ocular axis. CONCLUSIONS: These disconjugate, short-latency axis perturbations appear intrinsic to the VOR and may have neural or mechanical origins.

Adult↗

Spatial distribution of gravity-dependent gain changes in the vestibuloocular reflex.

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 approximately 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.

Adaptation, Physiological↗

Vestibular signals carried by pathways subserving plasticity of the vestibulo-ocular reflex in monkeys.

The vestibulo-ocular reflex (VOR) is subject to long-term adaptive changes that minimize retinal image slip and keep eye movement equal to and opposite head movement. As a step toward identifying the site of neural changes, we have used a transient vestibular stimulus to study the dynamic response properties of the vestibular signals carried by the modifiable pathways. In normal monkeys, "rapid changes in head velocity" (30 degrees/sec in 50 msec) evoke a VOR that has a slight overshoot and reaches a steady-state gain (eye velocity divided by head velocity) of 1.0. Adaptation to magnifying spectacles causes changes in both the steady-state gain and the degree of overshoot in the eye velocity of the VOR. When the steady-state gain is decreased, the transient overshoot increases, so that peak eye velocity is twice steady-state. When the steady-state gain is increased, the overshoot decreases, so that peak eye velocity is nearly equal to steady-state. The discharge of vestibular primary afferents suggests an explanation for the inverse relationship between the transient overshoot and the steady-state gain of the VOR. In normal monkeys, 73 afferents showed a range of transient responses during rapid changes in head velocity. The afferents with the most regular spontaneous discharge had little overshoot in firing rate. Afferents with less regular discharge had large overshoots in firing; the peak change in firing was 2-6 X the steady-state change. We suggest that the large overshoot in eye velocity when VOR gain is low represents the contribution of vestibular signals from afferents with large transient responses.(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗

Noradrenergic agents in the cerebellar vermis affect adaptation of the vestibulospinal reflex gain.

In precollicular decerebrate cats, the vestibulospinal reflex (VSR) was intermittently recorded from the triceps brachii during sinusoidal roll tilt of the whole animal (at 0.15 Hz, +/- 10 degrees), leading to selective stimulation of labyrinth receptors. This reflex, tested during and after a 3-h period of sustained animal tilt at the same parameters indicated above, showed an adaptive increase in gain in some experiments but not in others. In a second group of experiments, however, rotation of the head (at 0.15 Hz, +/- 10 degrees) was associated with a synchronous body rotation (at 0.15 Hz, +/- 12.5 degrees) which led to an additional neck input, due to 2.5 degrees of out-phase body-to-head displacement. In these experiments, the VSR, tested every 10-15 min, consistently showed an adaptive increase in gain during and after a 3-h period of sustained vestibular and neck stimulation. Microinjection into the cerebellar anterior vermis of beta-adrenergic agents (0.25 microliters at 8 micrograms/microliters saline) produced slight and short-lasting changes in the basic amplitude of the VSR, due to the neuromodulatory influence of these agents on the Purkinje cells activity. In addition, the beta-adrenergic agonist isoproterenol brought to the light an adaptive process in those experiments in which no adaptation occurred during a sustained roll tilt of the whole animal. On the other hand, the beta-adrenergic antagonists propranolol or sotalol either suppressed the increase in gain of the VSR which occurred in other experiments during sustained animal rotation, or prevented the occurrence of an adaptive increase in gain during a continuous out-phase head and body rotation. We conclude that the adaptive changes in gain of the VSR are facilitated by the noradrenergic system acting within the cerebellar cortex through beta-adrenoceptors.

Adaptation, Physiological↗

Influence of eye and head position on the vestibulo-ocular reflex.

For the vestibulo-ocular reflex (VOR) to function properly, namely to ensure a stable retinal image under all circumstances, it should be able to take into account varying eye positions in the orbit and varying orientations of the head with respect to the axis about which it is rotating. We tested this capability by quantifying the gain and the time constant of the horizontal component of the VOR during rotation about an earth vertical axis when the line of sight (optical axis) was moved out of the plane of head rotation--either by rotating the eyes up or down in the orbit or by pitching the head up or down with respect to earth-horizontal. In either case the gain of the horizontal component of the VOR was attenuated precisely by the cosine of the angle made between the optical axis and the plane of head rotation. Furthermore, if the head was pitched up or down but the eye rotated oppositely in the orbit so as to keep the line of sight in the plane of head rotation the gain of the horizontal component of the VOR was the same value as with the head and eyes both straight ahead. In contrast, the time constant of the VOR varied only as a function of the orientation of the head and not as a function of eye position in the orbit. During rotation about an earth vertical axis, the time constant was longest (about 18 s) when the head was pitched forward to place the lateral canals near earth-horizontal and shortest (about 11 s) when the head was pitched backward to place the vertical canals near earth-horizontal.(ABSTRACT TRUNCATED AT 250 WORDS)

Adult↗

Visual-vestibular interaction in humans during active and passive, vertical head movement.

We studied visual-vestibular interaction (VVI) in 9 normal human subjects using active and passive vertical head rotations. Gain and phase of the vertical vestibulo-ocular reflex (VOR) and visually enhanced vestibulo-ocular reflex (VVOR) were measured for single frequency sinusoidal motion, as well as for sinusoidal motion of continuously increasing frequency, over the range of 0.4 to 4.0 Hz. In addition to measurement of VVOR during normal vision, telescopic spectacles having a magnification of 1.9x were used to challenge VVI to facilitate measurement of visual enhancement of VOR gain. In the mid-frequency range (1.6 to 2.4 Hz), the active VOR exhibited gain closer to compensatory than did the passive VOR; at other frequencies, active and passive VOR gains were similar. VVOR gain during normal vision was compensatory for both active and passive motion throughout the frequency range tested. VVOR gain with 1.9x telescopic spectacles was greater than VOR gain at all frequencies tested, including up to 3.2 Hz for passive head movements, and up to 4.0 Hz for active head movement. However, gain enhancement with telescopic spectacles was consistently greater during active than during passive head movement. Phase errors for the VOR and VVOR were small under all testing conditions. Although active VOR and VVOR were directionally symmetrical, gain of upward slow phases differed from that of downward slow phases for passive VOR and VVOR in a manner depending on rotational frequency. For both active and passive testing, gain and phase values obtained during swept frequency rotations were similar to those obtained during single frequency sinusoidal testing. These data indicate that VVI can enhance gain of the passive vertical VOR even at frequencies above what is usually considered to be the upper limit of visual pursuit tracking. The additional enhancement observed during active head movements at these high frequencies is attributable to use of efference copy of the skeletal motor command to neck musculature.

Adult↗

Vestibulo-ocular responses during static head roll and three-dimensional head impulses after vestibular neuritis.

This study aimed to investigate whether unilateral vestibular neuritis (VN) causes the same deficits of ocular counter-roll during static head roll (OCR(S)) and dynamic vestibulo-ocular reflex gains during head impulses (VOR(HI)) as unilateral vestibular deafferentation (VD). Ten patients with acute and 14 patients with chronic vestibular paralysis after VN were examined. The testing battery included fundus photography of both eyes with the head upright (binocular cyclorotation) and dual search coil recordings in a three-field magnetic frame. With one dual search coil on the right eye and the other on the forehead, the following stimuli were given: i) Halmagyi-Curthoys head impulses about the vertical, horizontal and torsional axes. ii) Static roll positions of the head up to 20 degrees right- and left-ear-down by movement of the neck. The comparison group consisted of 19 healthy subjects. Compared with the VD-patients, as reported in the literature, acute VN-patients showed the same pattern of OCR(S) gain reduction and binocular cyclorotation (CRb). The main feature that distinguished chronic VN-patients from chronic VD-patients was the normalization of the torsional VOR(HI) gain to the affected side, whereas the VOR(HI) gains in the horizontal and vertical directions did not show recovery (as in the patients with chronic VD). Chronic VN-patients differed from acute VN-patients by: i) symmetrical OCR(S) gains, ii) a less pronounced CRb toward the affected side, and iii) a normal torsional VOR(HI) gain toward the affected side. Since the ipsilesional torsional VOR(HI) gain did not recover in VD-patients, the normalization of this gain in our VN-patients can only be explained by a (partial) recovery of otolith function on the side of the lesion after the neuritis.

Acute Disease↗

Senescence of human visual-vestibular interactions. 1. Vestibulo-ocular reflex and adaptive plasticity with aging.

The human horizontal vestibulo-ocular reflex (VOR) was studied as a function of aging (18 to 89 years) over a broad range of frequencies (0.025 to 4 Hz) and peak velocities (50 degrees to 300 degrees/s) of angular head movement. Eye movements were recorded using the search-coil technique. High stimulus frequencies and amplitudes were employed in order to challenge the VOR sufficiently to enhance potential age-related deficits in its pathways and functions. Further, the possibility that adaptive plastic mechanisms, which normally restore failing VOR function, might themselves deteriorate with aging was tested. Subjects were studied before and after an 8-h period while wearing 2 x binocular magnifying lenses. Demonstrable differences were observed in the human VOR as a function of natural aging. These differences were most pronounced in phase measures (increasing lead with aging), both at low frequency and low head velocity, and at modest frequency but high head velocity. Gain decrements were also observed with aging, but the changes were more subtle. The modifications in the VOR may be interpreted as an age-dependent deterioration in VOR performance. The course of age-related changes in response characteristics, particularly phase lead at the highest stimulus amplitude, are similar to age-related anatomical deterioration reported in peripheral vestibular structures. These changes resemble those in young patients with vestibular lesions, and are consistent with the notion that aging entails a progressive bilateral peripheral vestibular loss. Adaptive plastic mechanisms, which normally maintain VOR performance when altered responses result in visual-vestibular mismatch during head rotation, also deteriorate with aging. Again, the phenomenon resembles that in younger but vestibulopathic individuals. The effect is most profound at high frequencies and head velocities commensurate with natural behavior.

Adaptation, Physiological↗

Adaptive modification of the cat's vestibulospinal reflex during sustained vestibular and neck stimulation.

In decerebrate cats, rotation about the longitudinal axis of the whole animal at 0.15 Hz, +/- 10 degrees produced an increased electromyogram (EMG) activity of the triceps brachii during side-down tilt and a decreased activity during side-up tilt. This vestibulospinal reflex (VSR) was tested before, during and after a sustained (3-h) period of roll tilt of the head at the parameters indicated above, associated with a synchronous roll tilt of the body at 0.15 Hz, but at the peak amplitude of either 12.5 degrees or 7.5 degrees. This additional stimulus led to 2.5 degrees of neck rotation, which was respectively out of phase (condition A) or in-phase (condition B) with head rotation. In a few instances the peak amplitude of neck rotation was increased to 5 degrees. In the first experimental condition A, the gain of the VSR (tested every 10-15 min) progressively increased, starting from the first hour of out of phase neck-vestibular stimulation to reach, on average, 241% of the control value at the end of the third hour of stimulation. On the other hand, in the second experimental condition B, the mean gain of the VSR first decreased to 82% during the first hour of in-phase neck-vestibular stimulation, but then increased to 165% of the corresponding control during the last hour of recording. In other experiments an adaptive increase in gain of the pure VSR occurred during a sustained (3-h) period of selective roll tilt of the whole animal, but it was less consistent and, on average, smaller in amplitude than that obtained during out of phase neck-vestibular stimulation. The adaptive changes in gain of the VSR described above were not associated with changes in the phase angle of the responses, and were also observed during the post-adaptation period. Further experiments indicated that the gain of the N-VSR, i.e. of the EMG responses to combined neck-vestibular stimulation, displayed a prominent adaptive increase during the sustained out of phase stimulation, but not during the in phase stimulation.

Adaptation, Physiological↗

The influence of volume depletion and central hypovolemia on the plasma concentration of parathyroid hormone in dialysis patients.

Because changes in extracellular volume during dialysis cause reflex neurohonnonal changes that may influence parathyroid hormone (PTH) release independently of calcium, the influence of isotonic volume depletion (by isolated ultrafiltration) and central hypovolemia (70 degrees tilt) on serum PTH1-84 was studied in 16 hemodialysis patients. Tilting was performed in volume depleted state, i.e., immediately after hemodialysis. In the control study, patients underwent sham ultrafiltration (UF = 0) and after dialysis maintained the supine position for the same length of time they remained in the tilt position in the active experiment. Isolated ultrafiltration (-2.3 +/- SEM 0.3 L) caused a 21% fall in mean arterial pressure (from 101 +/- 6 to 80 +/- 6 mmHg, P < 0.01), a fall that was accompanied by a marked increase in plasma catecholamine levels (norepinephrine P < 0.001, epinephrine P < 0.025), in plasma renin activity (P < 0.001) and in plasma arginine vasopressin (P < O.001). Atrial natriuretic factor showed a slight reduction, whereas the plasma endothelin-1 level did not change. Serum Ca showed the expected, hemoconcentration-dependent rise (from 4.1 +/- 0.1 to 4.4 +/- 0.1 meq/L, P < 0.01). Interestingly, UF caused a marked rise in plasma PTH1-84 concentration (from 252 +/- 62 to 335 +/- 72 pg/ml, P < 0.01). UF-induced changes in serum PTH1-84 were related to norepinephrine changes (r = 0.57) as well as to plasma renin activity (r = 0.50). After hemodialysis, tilting induced a pronounced rise in serum PTH1-84 (from 102 +/- 29 to 200 +/- 55 pg/ml), and these changes were slightly related to plasma epinephrine (r = 0.49) but independent of other parameters. In the control experiment, neither sham UF nor recumbency modified serum PTH. In hemodialysis patients, serum PTH is sensitive to changes in extracellular and central blood volume of magnitude sufficient to decrease arterial pressure. Avoiding marked volume stimuli might help to refine the interpretation of the Ca/PTH curves during hemodialysis in these patients.

Adult↗

Comparison of head thrust test with head autorotation test reveals that the vestibulo-ocular reflex is enhanced during voluntary head movements.

OBJECTIVES: To compare 2 clinical tests of vestibular function, the head autorotation test (HART) and the head thrust test (HTT), and to determine why they give disparate results in patients with known unilateral vestibular deficiency (UVD) due to labyrinthectomy. METHODS: We used scleral coils to measure the horizontal (yaw) vestibulo-ocular reflex (VOR) in 5 healthy human subjects and in 11 patients who underwent labyrinthectomy. We used 2 paradigms. Using HART, subjects visually fixated a target during self-generated, swept-frequency, sinusoidal, horizontal head rotations. Using HTT, patients fixated the target during horizontal head thrusts delivered randomly in direction and time. RESULTS: In subjects without UVD, eye movements were almost perfectly compensatory for both paradigms. In subjects with UVD, VOR gain for ipsilesional head thrusts was low for both paradigms, but significantly (P<.001) higher (less abnormal) for HART (0.60 +/- 0.13) than for HTT (0.14 +/- 0.13). Contralesional gain was reduced for both, to 0.64 +/- 0.20 for HART and to 0.57 +/- 0.17 for HTT. Because ipsilesional and contralesional gains were not statistically different for HART (P =.69), comparison of VOR gains for half-cycle responses to the HART stimulus could not reliably identify the side of the known lesion. In contrast, HTT consistently identified the side of the lesion for all subjects with UVD. To investigate whether preprogramming contributes to the boost in VOR as measured by HART, we compared the gain and response delay of eye movements during actively self-generated and passively received head thrusts. For subjects without UVD, response delays were shorter for active (6 +/- 1 milliseconds) than for passive (12 +/- 1 milliseconds) HTT. For ipsilesional rotations of subjects with UVD, active HTT yielded a significantly higher gain (0.44 +/- 0.20) (P<.001) and a shorter delay (15 +/- 6 milliseconds) (P<.001) than did passive HTT (0.14 +/- 0.13 and 37 +/- 15 milliseconds, respectively). Contralesional test results revealed a similar performance boost for active head movements. Data are given as mean +/- SD. CONCLUSION: When comparison of half-cycle gains is used to identify the lesion side, self-generated predictable head movement paradigms, such as HART and active HTT, are less accurate than passive HTT in the characterization of UVD, in part because preprogramming can augment the VOR during voluntary head movements.

Adult↗

Mechanics of stretch in activated crustacean slow muscle. II. Dynamic changes in force in response to stretch.

1. The mechanical dynamics of the ventral superficial muscles (VSM) of the abdomen of the hermit crab, Pagurus pollicarus, have been analyzed to develop a quantitative model of gradedly excitable arthropod muscle. Such a model is important for understanding the role of proprioceptive reflexes in posture and movement. 2. The decay in force produced after ramp stretch of both passive and active muscle was approximated by the use of regression equations involving a direct term and one to three exponential terms. A second-order equation produced an acceptable description of this decay over short (0.5 s) sampling durations. 3. The rate constants of the regression equation did not vary with stretch length, velocity, or activation level of the muscle. For the two-exponential-term model, the rate constants were approximately 90 and 9 s-1 for a sample duration of 0.3 s. An additional rate constant of approximately 1 s-1 was needed to adapt the model to longer sample times. 4. The direct term and the middle-order (9 s-1) residual were both functions of stretch length and activation level. The high-order (90 s-1) residual was primarily a function of stretch length and velocity. Transfer functions omitting the velocity dependence adequately described the mechanical dynamics of the muscle for physiological ranges of stretch velocity. 5. White-noise length perturbations were used to calculate spectral density functions of muscle force and length. These measurements confirmed the principal observations of the ramp stretch analysis: the frequency response of the muscle was independent of the level of activation; the magnitude of the stiffness increased over the stretch frequency range of 4-40 Hz and was then almost constant; and the phase response of the muscle became slightly positive over the same range of stretch frequency. 6. The speed of activation of the muscle to different stimulus frequencies was estimated by fitting a single exponential equation to the rise in isometric tension at the onset of stimulation of the motor nerve. The rate constant increased with stimulus frequency, but its maximum value was only 1.8 s-1, about one-fourth of the middle mechanical rate constant. 7. Because muscle activation is slower than the mechanical dynamics, it is unlikely that the nervous system can regulate muscle dynamics. However, it is possible that mechanical impedance could be regulated to maintain a desired time-averaged value.

Animals↗

Inertial representation of angular motion in the vestibular system of rhesus monkeys. II. Otolith-controlled transformation that depends on an intact cerebellar nodulus.

1. We recently studied the spatial representation of angular motion signals in rhesus monkeys by examining the orientation of postrotatory vestibuloocular responses during tilt of the head and body relative to gravity after constant-velocity rotation about an earth-vertical axis. We have reported that low-frequency angular motion signals in the vestibuloocular reflex (VOR) of rhesus monkeys are spatially transformed such that they remain invariant relative to gravity. In the present study we examine the properties of these inertial vestibular signals by employing similar stimulation conditions in animals with either selective semicircular canal plugging or selective lesions of cerebellar lobule X (nodulus) and ventral lobule IX (uvula). 2. We studied the spatial organization of postrotatory VOR in two rhesus monkeys that had either the lateral or one of the vertical canal pairs inactivated by plugging. In both monkeys, the spatiotemporal characteristics of postrotatory velocity after rotation in the plane of an intact canal pair and tilting in the plane of the plugged canal pair were indistinguishable from those of intact animals: postrotatory responses after tilts in the plane of the plugged canal pair were strongly damped, whereas an orthogonal response component was generated that rotated the eye velocity vector toward alignment with gravity. Thus otolith information rather than transient semicircular canal inputs that normally coexist during tilts seem to provide the necessary cues for the central transformation of semicircular canal signals. 3. We studied the three-dimensional VOR properties in two animals in which the cerebellar nodulus and ventral uvula were surgically ablated. After these lesions the temporal properties of the horizontal, vertical, and torsional VOR during earth-vertical-axis rotations were differentially affected. For horizontal VOR, the duration of postrotatory nystagmus was prolonged and the responses acquired strongly underdamped (i.e., oscillatory) properties. Similarly, sinusoidal responses were characterized by smaller phase leads after the lesion. For torsional VOR, the duration of postrotatory nystagmus was significantly shorter after the lesions, reaching postlesion values of 3.6 +/- 1.7 (SD) s and 6.4 +/- 1.1 s compared with prelesion values of 22.4 +/- 4.5 and 33.6 +/- 5.3 s for each animal. In addition, large phase leads characterized the torsional VOR during low-frequency sinusoidal stimulation. The dynamic properties of the vertical VOR in the lesioned animals, on the other hand, were indistinguishable from those in controls. 4. The cerebellar lesions affected the spatial organization of the horizontal and vertical/torsional systems in a differential way. Inertial transformation of lateral canal activity was only partially affected.(ABSTRACT TRUNCATED AT 400 WORDS)

Animals↗

Effects of tilt of the gravito-inertial acceleration vector on the angular vestibuloocular reflex during centrifugation.

Effects of tilt of the gravito-inertial acceleration vector on the angular vestibuloocular reflex during centrifugation. Interaction of the horizontal linear and angular vestibuloocular reflexes (lVOR and aVOR) was studied in rhesus and cynomolgus monkeys during centered rotation and off-center rotation at a constant velocity (centrifugation). During centered rotation, the eye velocity vector was aligned with the axis of rotation, which was coincident with the direction of gravity. Facing and back to motion centrifugation tilted the resultant of gravity and linear acceleration, gravito-inertial acceleration (GIA), inducing cross-coupled vertical components of eye velocity. These components were upward when facing motion and downward when back to motion and caused the axis of eye velocity to reorient from alignment with the body yaw axis toward the tilted GIA. A major finding was that horizontal time constants were asymmetric in each monkey, generally being longer when associated with downward than upward cross coupling. Because of these asymmetries, accurate estimates of the contribution of the horizontal lVOR could not be obtained by simply subtracting horizontal eye velocity profiles during facing and back to motion centrifugation. Instead, it was necessary to consider the effects of GIA tilts on velocity storage before attempting to estimate the horizontal lVOR. In each monkey, the horizontal time constant of optokinetic after-nystagmus (OKAN) was reduced as a function of increasing head tilt with respect to gravity. When variations in horizontal time constant as a function of GIA tilt were included in the aVOR model, the rising and falling phases of horizontal eye velocity during facing and back to motion centrifugation were closely predicted, and the estimated contribution of the compensatory lVOR was negligible. Beating fields of horizontal eye position were unaffected by the presence or magnitude of linear acceleration during centrifugation. These conclusions were evaluated in animals in which the low-frequency aVOR was abolished by canal plugging, isolating the contribution of the lVOR. Postoperatively, the animals had normal ocular counterrolling and horizontal eye velocity modulation during off-vertical axis rotation (OVAR), suggesting that the otoliths were intact. No measurable horizontal eye velocity was elicited by centrifugation with angular accelerations </=40 degrees /s2 and angular velocities </=400 degrees /s. We conclude that in rhesus and cynomolgus monkeys, differences between horizontal eye velocities recorded during facing and back to motion constant velocity centrifugation can be explained by orienting effects of the GIA tilt on the time constants of the horizontal aVOR and not by a superposed lVOR.

Acceleration↗

Visual-vestibular interaction during standing, walking, and running.

In artificial laboratory situations where subjects undergo repetitive self-generated or externally imposed head rotations, visual-vestibular interaction during the wearing of telescopic spectacles can markedly augment gain of the vestibulo-ocular reflex (VOR). The present study was conducted to determine whether the wearing of these aids for the visually impaired is associated with similar visual-vestibular interaction during more natural activities. Angular eye and head movements of unrestrained normal volunteers were measured using magnetic search coils. In some subjects, head translations and rotations were also monitored by a flux gate magnetometer array. Measurements were performed of the VOR in darkness, and of the visually enhanced VOR (VVOR) in lit conditions, during three natural activities: 1) standing quietly; 2) walking in place; 3) running in place. These data were compared with similar measurements during repetitive voluntary head oscillations at 0.8 Hz in pitch or yaw. During VVOR, subjects viewed a target placed 6 to 10 m away and remembered this target during VOR trials in darkness. To assess the effects of altering visual-vestibular interactions, VVOR testing during normal vision was augmented by wearing of binocular telescopic spectacles of 2X, 4X, and 6X powers. Dorsoventral and mediolateral head translations were consistently phase-locked with pitch and yaw head rotations, respectively, such that head translation at least partially compensated for rotational disturbances of gaze. Angular velocity of the head was greater during walking than during standing, and was greater still during running, with a greater increase in each case for pitch as compared with yaw. Eye movements were phase compensatory for head movements. VOR gain (eye velocity divided by head velocity) was near 1.0 in both pitch and yaw during standing and during actively generated head rotation. During walking and running there was a significant decrease in angular VOR gain in pitch to approximately 0.75 (P < 0.0005). During ambulatory activities, normal and magnified vision were associated with VVOR gain enhancement in pitch and yaw that was statistically significant, but substantially less than was telescope magnification and markedly lower than was the corresponding VVOR gain measured during active head rotation. Measurements of unmagnified VOR and VVOR during walking and running showed that gain was lower than the "ideal" value of 1.0. However, since translational head perturbations during these activities partially offset the visual effects of angular disturbances, lower gains may nevertheless be associated with retinal image stability at typical indoor target distances. In contrast with performance during repetitive, uniplanar motion, vision has very limited influence on VOR gain during natural activities.

Adult↗

Role of primate flocculus during rapid behavioral modification of vestibuloocular reflex. II. Mossy fiber firing patterns during horizontal head rotation and eye movement.

1. Extracellular recordings were obtained from 113 mossu fibers (MFs) in the flocculus of alert monkeys trained to perform a visual tracking task during sinusoidal, horizontal head rotation. The analysis of MF discharge patterns was designed to allow quantitative comparison of the discharge properties of flocculus MFs with brain stem cell populations from which the MFs might originate and with flocculus Purkinje cells (P-cells). Based on their firing patterns, MFs were divided into two classes. Vestibular MFs discharged in relation to head velocity and, in some cases, also in relation to eye movement. Eye movement MFs discharged only in relation to one or more components of eye movement. 2. Vestibular MFs were subdivided into three classes. Vestibular-only MFs (n = 15) displayed a modulation in firing rate during head rotation but exhibited no relationship to spontaneous eye movements. Vestibular-plus-saccade MFs (n = 14) displayed a modulation in firing rate during head rotation that quantitatively resembled the modulation in vestibular-only MFs. In addition, a pause in firing rate interrupted the vestibular modulation during saccades in one or more directions. Vestibular-plus-position MFs (n = 4) exhibited steady firing rates that were linearly related to horizontal eye position in the absence of vestibular stimulation. Sinusoidal head rotation evoked a modulation ofiring rate above and below the firing rate set by the eye position. 3. during sinusoidal head rotation, vestibular MF firing rate led head velocity by an average of 24 degrees. The amplitude of MF firing-rate modulation increased as a function of the frequency of head rotation and, hence, maximum head velocity. Since these characteristics are similar to those displayed by P-cells during suppression of the VOR, vestibular MFs probably transmit the head velocity component of P-cell firing rate to the flocculus. Based on evidence from other mammals and a quantitative comparison of population discharge characteristics, it is likely that vestibular MFs originate from the vestibular nerve and from cells in the medial vestibular nucleus. 4. Based on their discharge patterns, eye movement MFs were also subdivided into three classes. Burst MFs (n = 14) emitted a high-frequency burst of spikes prior to and during saccades in one or more direction, but were silent during steady fixation. Burst-tonic MFs (n = 53) emitted a burst of spikes prior to saccades in a preferred ("on") direction, ceased firing during saccades in the opposite ("off") direction, and exhibited steady firing rates that increased as steady gaze shifted in the on direction. Tonic MFs (n = 13) displayed steady firing rates that increased as the position of steady gaze shifted in the on direction, and either paused or exhibited step changes in firing rate during saccades. 5. During steady fixation, 64% of tonic and burst-tonic MFs were recruited into maintained firing within +/- 10 degrees of the primary direction of gaze...

Animals↗

Inertial representation of angular motion in the vestibular system of rhesus monkeys. I. Vestibuloocular reflex.

1. The spatial organization of the vestibuloocular reflex (VOR) was studied in six rhesus monkeys by applying fast, short-lasting, passive head and body tilts immediately after constant-velocity rotation (+/- 90 degrees/s) about an earth-vertical axis. Two alternative hypotheses were investigated regarding the reference frame used for coding angular motion. 1) If the vestibular system is organized in head-centered coordinates, postrotatory eye velocity would decay invariably along the direction of applied head angular acceleration. 2) Alternatively, if the vestibular system codes angular motion in inertial, gravity-centered coordinates, postrotatory eye velocity would decay along the direction of gravity. 2. Horizontal VOR was studied with the monkeys upright. Pitch (roll) tilts away from upright elicited a transient vertical (torsional) VOR and shortened the time constant of the horizontal postrotatory slow phase velocity. In addition, an orthogonal torsional (after pitch tilts) or vertical (after roll tilts) response gradually built up. As a result, the eye velocity vector transiently deviated in the roll (pitch) plane and then gradually rotated in the same direction as gravity in the pitch (roll) head plane until the orthogonal component reached a peak value. Subsequently, the residual postrotatory eye velocity decayed along a line parallel to gravity. 3. The time constant of the horizontal postrotatory response was maximal in upright position (21.5 +/- 5.7 s, mean +/- SD) and minimal after tilts to prone (3.8 +/- 0.7 s), supine (4.5 +/- 1.2 s), and ear-down (5.2 +/- 1.6 s) positions. A similar dependence on head orientation relative to gravity characterized the dynamics of the resultant eye velocity vector in the pitch and roll planes. 4. Torsional VOR was studied with the monkeys in supine or prone position. Pitch (yaw) tilts from the supine or prone position toward upright (ear-down) position elicited a transient vertical (horizontal) VOR and shortened the time constant of the torsional postrotatory response while a horizontal (vertical) orthogonal component slowly built up. As a result the eye velocity vector gradually rotated in the pitch (yaw) plane until the orthogonal component reached a peak value. Subsequently residual postrotatory eye velocity decayed along a line parallel to gravity. 5. The time constant of the torsional postrotatory response in supine/prone positions was 16.5 +/- 6.8 s. After tilts from supine/prone positions toward upright position, time constants decreased and were minimal after tilts to upright position (2.7 +/- 0.7 s).(ABSTRACT TRUNCATED AT 400 WORDS)

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