Capacity of Vertical VOR Adaptation in Squirrel Monkey

2002 ◽  
Vol 88 (6) ◽  
pp. 3194-3207 ◽  
Author(s):  
Y. Hirata ◽  
J. M. Lockard ◽  
S. M. Highstein
Keyword(s):  
Motor Learning ◽  
Head Movement ◽  
High Frequency ◽  
Low Frequency ◽  
Squirrel Monkeys ◽  
Head Motion ◽  
Vestibuloocular Reflex ◽  
Differential Adaptation ◽  
Vor Adaptation ◽  
Eye Velocity

Squirrel monkeys were trained using newly developed visual-vestibular mismatch paradigms to test the asymmetrical simultaneous induction of vertical vestibuloocular reflex (VOR) gain changes in opposite directions (high and low) either in the upward and downward directions or in response to high- and low-frequency stimuli. The first paradigm consists of sinusoidal head movement [ Asin(ω t)] and a full rectified sinusoidal optokinetic stimulus [±‖ A sin(ω t)‖], whereas the second paradigm consists of the sum of two sinusoids with different frequencies { A sin(ω1 t) + A sin(ω2 t) for head motion and ±[ Asin(ω1 t) − Asin(ω2 t)] for the optokinetic stimulus, ω1 = 0.1π, ω2 = 5π}. The first paradigm induced a half rectified sinusoidal eye-velocity trace, i.e., suppression of the VOR during upward head motion and enhancement during downward head motion or vise versa, whereas the second paradigm induced suppression of the VOR at the low-frequency ω1 and enhancement at the high-frequency ω2 or vise versa. After 4 h of exposure to these paradigms, VOR gains of up and down or high and low frequency were modified in opposite directions. We conclude that the monkey vertical VOR system is capable of up-down directionally differential adaptation as well as high-low frequency differential adaptation. However, experiments also suggest that these gain controls are not completely independent because the magnitudes of the gain changes during simultaneous asymmetrical training were less than those achieved by symmetrical training or training in only one of the two components, indicating an influence of the gain controls on each other. These results confine the adaptive site(s) responsible for vertical VOR motor learning to those that can process up and downward or low- and high-frequency head signal separately but not completely independently.

Vestibuloocular Reflex Dynamics During High-Frequency and High-Acceleration Rotations of the Head on Body in Rhesus Monkey

2002 ◽  
Vol 88 (1) ◽  
pp. 13-28 ◽  
Author(s):  
Marko Huterer ◽  
Kathleen E. Cullen
Keyword(s):  
Eye Movements ◽  
High Frequency ◽  
The Body ◽  
Whole Body ◽  
Head Motion ◽  
Similar Response ◽  
Vestibuloocular Reflex ◽  
Frequency Range ◽  
Response Dynamics ◽  
Passive Rotation

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.

Neural basis for motor learning in the vestibuloocular reflex of primates. I. Changes in the responses of brain stem neurons

1994 ◽  
Vol 72 (2) ◽  
pp. 928-953 ◽  
Author(s):  
S. G. Lisberger ◽  
T. A. Pavelko ◽  
D. M. Broussard
Keyword(s):  
Eye Movements ◽  
Motor Learning ◽  
Firing Rate ◽  
Brain Stem ◽  
Head Rotation ◽  
Head Motion ◽  
Vestibuloocular Reflex ◽  
Neural Basis ◽  
Ventral Paraflocculus ◽  
The Brain

1. We recorded from neurons in the brain stem of monkeys before and after they had worn magnifying or miniaturizing spectacles to cause changes in the gain of the vestibuloocular reflex (VOR). The gain of the VOR was estimated as eye speed divided by head speed during passive horizontal head rotation in darkness. Electrical stimulation in the cerebellum was used to identify neurons that receive inhibition at monosynaptic latencies from the flocculus and ventral paraflocculus (flocculus target neurons or FTNs). Cells were studied during smooth pursuit eye movements with the head stationary, fixation of different positions, cancellation of the VOR, and the VOR evoked by rapid changes in head velocity. 2. FTNs were divided into two populations according to their responses during pursuit with the head stationary. The two groups showed increased firing during smooth eye motion toward the side of recording (Eye-ipsiversive or E-i) or away from the side of recording (Eye-contraversive or E-c). A higher percentage of FTNs showed increased firing rate for contraversive pursuit when the gain of the VOR was high (> or = 1.6) than when the gain of the VOR was low (< or = 0.4). 3. Changes in the gain of the VOR had a striking effect on the responses during the VOR for the FTNs that were E-c during pursuit with the head stationary. Firing rate increased during contraversive VOR eye movements when the gain of the VOR was high or normal and decreased during contraversive VOR eye movements when the gain of the VOR was low. Changes in the gain of the VOR caused smaller changes in the responses during the VOR of FTNs that were E-i during pursuit with the head stationary. We argue that motor learning in the VOR is the result of changes in the responses of individual FTNs. 4. The responses of E-i and E-c FTNS during cancellation of the VOR depended on the gain of the VOR. Responses tended to be in phase with contraversive head motion when the gain of the VOR was low and in phase with ipsiversive head motion when the gain of the VOR was high. Comparison of the effect of motor learning on the responses of FTNs during cancellation of the VOR with the results of similar experiments on horizontal-gaze velocity Purkinje cells in the flocculus and ventral paraflocculus suggests that the brain stem vestibular inputs to FTNs are one site of motor learning in the VOR.(ABSTRACT TRUNCATED AT 400 WORDS)

Effect of Stimulus Duration on Localization of Direction of Noise Stimuli

1970 ◽  
Vol 13 (4) ◽  
pp. 826-838 ◽  
Author(s):  
Willard R. Thurlow ◽  
James R. Mergener
Keyword(s):  
Stimulus Duration ◽  
Head Movement ◽  
High Frequency ◽  
Thermal Noise ◽  
Low Frequency ◽  
Frequency Noise ◽  
Noise Sources ◽  
Minimum Duration ◽  
High Frequency Noise ◽  
Efficient Performance

Localization of the direction of bursts of thermal noise was measured for both high-frequency and low-frequency bands, as a function of duration of bursts. Durations of 0.3, 1, 2, and 5 sec were used. Subjects were free to move their heads to aid in localization. Subjects were not specially trained in sound localization. With increase in stimulus duration, perception of elevation was slightly improved for low-frequency noise, probably due to increased information from head movement. A minimum duration of the order of 2 sec appears necessary to allow subjects to achieve maximum performance (which still is not very good for these low-frequency stimuli). Perception of the elevation of the high-frequency noise sources we used was relatively good even at the briefest duration; however, variability of judgment was larger at the shorter durations. Perception of front-back source position was much improved for both low-frequency and high-frequency noise when stimulus duration was increased. The results are understandable in terms of the increased possibility for head movement with increase in stimulus duration. It appears that one should use a minimum stimulus duration of about 2 sec if one wishes subjects to approach their most efficient performance.

Neural basis for motor learning in the vestibuloocular reflex of primates. III. Computational and behavioral analysis of the sites of learning

1994 ◽  
Vol 72 (2) ◽  
pp. 974-998 ◽  
Author(s):  
S. G. Lisberger
Keyword(s):  
Motor Learning ◽  
Eye Movement ◽  
Computer Model ◽  
Visual Motion ◽  
Transfer Functions ◽  
Vestibular Nucleus ◽  
Vestibuloocular Reflex ◽  
Neural Basis ◽  
Ventral Paraflocculus ◽  
Eye Velocity

1. We have used a combination of eye movement recordings and computer modeling to study long-term adaptive modification (motor learning) in the vestibuloocular reflex (VOR). The eye movement recordings place constraints on possible sites for motor learning. The computer model abides by these constraints, as well as constraints provided by data in previous papers, to formalize a new hypothesis about the sites of motor learning. The model was designed to reproduce as much of the existing neural and behavioral data as possible. 2. Motor learning was induced in monkeys by fitting them with spectacles that caused the gain of the VOR (eye speed divided by head speed) to increase to values > 1.6 or to decrease to values < 0.4. We elicited pursuit by providing ramp motion of a small target at 30 degrees/s along the horizontal axis. Changes in the gain of the VOR caused only small and inconsistent changes in the eye acceleration in the first 100 ms after the onset of pursuit and had no effect on the eye velocity during tracking of steady target motion. Electrical stimulation in the flocculus and ventral paraflocculus with single pulses or trains of pulses caused smooth eye movement toward the side of stimulation after latencies of 9–11 ms. Neither the latency, the peak eye velocity, nor the initial eye acceleration varied as a consistent function of the gain of the VOR. 3. The computer model contained nodes that represented position-vestibular-pause cells (PVP-cells) and flocculus target neurons (FTNs) in the vestibular nucleus, and horizontal gaze-velocity Purkinje cells (HGVP-cells) in the cerebellar flocculus and ventral paraflocculus. Node FTN represented only the “E-c FTNs,” which show increased firing for eye motion away from the side of recording. The transfer functions in the model included dynamic elements (filters) as well as static elements (summing junctions, gain elements, and time delays). Except for the transfer functions that converted visual motion inputs into commands for smooth eye movement, the model was linear. 4. The performance of the model was determined both by computer simulation and, for the VOR in the dark, by analytic solution of linear equations. For simulation, we adjusted the parameters by hand to match the output of the model to the eye velocity of monkeys and to match the activity of the relevant nodes in the model to the firing of HGVP-cells, FTNs, and PVP-cells when the gain of the VOR was 0.4, 1.0, and 1.6.(ABSTRACT TRUNCATED AT 400 WORDS)

Memory retention of vestibuloocular reflex motor learning in squirrel monkeys

Neuroreport ◽  
2004 ◽  
Vol 15 (6) ◽  
pp. 1007-1011 ◽  
Author(s):  
Y. Kuki ◽  
Y. Hirata ◽  
P. M. Blazquez ◽  
S. A. Heiney ◽  
S. M. Highstein
Keyword(s):  
Motor Learning ◽  
Squirrel Monkeys ◽  
Vestibuloocular Reflex ◽  
Memory Retention

Characterization and adaptive modification of the goldfish vestibuloocular reflex by sinusoidal and velocity step vestibular stimulation

1992 ◽  
Vol 68 (6) ◽  
pp. 2003-2015 ◽  
Author(s):  
A. M. Pastor ◽  
R. R. de la Cruz ◽  
R. Baker
Keyword(s):  
Electrical Stimulation ◽  
Eye Movement ◽  
Constant Velocity ◽  
Directional Asymmetry ◽  
Vestibuloocular Reflex ◽  
Dynamic Component ◽  
Head Velocity ◽  
Vor Adaptation ◽  
Eye Velocity ◽  
Stimulation Of

1. The normal and adapted vestibuloocular reflex (VOR) of goldfish was characterized by means of sinusoidal, velocity step, and position step head rotations about the vertical axis. VOR adaptation was induced by short-term, 1- to 4-h, presentation of visual and vestibular stimuli that altered the ratio of eye to head velocity. 2. The VOR response measured with sinusoidal oscillations in the dark was close to ideal compensatory values over 2 decades (1/32-2 Hz). Gain approximated unity, and phase, in relation to the head, was nearly 180 degrees. The VOR was linear within the range of head velocity tested (4-64 degrees/s). 3. Head velocity steps from 1/8 to 1 Hz produced steplike eye velocity profiles that could be divided into an early acceleration-related "dynamic" component and a later constant-velocity "sustained" period frequently separated by a sag at approximately 0.1-0.15 s from the initiation of eye movement. The sustained response exhibited no decay during the constant-velocity component of the step. 4. Higher temporal resolution of the dynamic response showed the adducting eye movement to have a shorter latency, faster rise time, and larger peak gain than the abducting eye movement. The characteristics of this directional asymmetry were similar for position steps and electrical stimulation of the vestibular nerve. However, the asymmetry was not observed during sinusoidal head rotation, the sustained component of the step response, or after electrical stimulation of the VIth and IIIrd nerves. We conclude that this directional asymmetry is of central origin and may be largely due to the parallel vestibular and abducens internuclear neuron pathways onto medial rectus motoneurons. 5. The VOR adaptation process for both higher and lower eye velocity exhibited an exponential time course with time constants of 55 and 45 min, respectively. After continuous sinusoidal training for 4 h, VOR gain reached an asymptotic level 5% away from perfect suppression in the low-gain training, but 19% away from the actual performance in the high-gain paradigm. The time constant for VOR gain reversal was 5 h, and an asymptotic level 40% less than performance was reached within 10 h. 6. Adapted VOR gain was symmetrical for both directions of eye movement measured either during sinusoidal rotation or the sustained part of the velocity step. VOR adaptation also produced a comparable gain change in the nasal and temporal directions of the dynamic component, but this reflected the asymmetric characteristics observed in the preadapted condition.(ABSTRACT TRUNCATED AT 400 WORDS)

Combined eye-head gaze shifts in the primate. II. Interactions between saccades and the vestibuloocular reflex

1986 ◽  
Vol 56 (6) ◽  
pp. 1558-1570 ◽  
Author(s):  
R. D. Tomlinson ◽  
P. S. Bahra
Keyword(s):  
Head Movement ◽  
Rhesus Monkeys ◽  
Vertical Component ◽  
Horizontal Component ◽  
Vestibuloocular Reflex ◽  
Water Reward ◽  
Gaze Shifts ◽  
Gaze Shift ◽  
The Gaze ◽  
Eye Velocity

The mechanisms of eye-head coordination were studied in two alert juvenile rhesus monkeys. Animals were trained to follow a target light to obtain a water reward and the combined eye-head gaze shifts in response to target steps with a variably sized horizontal components were studied. During a certain random portion of the gaze shifts, a torque motor was used to perturb the head to investigate the operational state of the vestibuloocular reflex (VOR) during the saccadic gaze shift. The effects of perturbing the head were assessed during five different conditions: horizontal target steps ranging from 10 to 80 degrees in amplitude; oblique target steps where the vertical component was larger than the horizontal component; purely vertical target steps 10-40 degrees in amplitude; both horizontal and oblique target steps delivered while the animals' saccades had been slowed by the use of diazepam; and large spontaneous gaze shifts in response to both sounds and visual stimuli. Comparison of perturbed and unperturbed large-amplitude (greater than 40 degrees) gaze shifts indicate that the VOR is turned off for most of the duration of the movement. Nonetheless, there is an apparent interaction between the saccadic eye movement and the head movement, thus, as the head velocity increases, the eye velocity decreases so that gaze velocity remains nearly constant throughout the gaze shift. Since the VOR is turned off when this interaction occurs, it must represent an interaction between the actual eye and head movement motor programs themselves. Although the results were not quite as clear for small saccades (less than 20 degrees), experiments on animals whose saccades had been slowed either by the use of diazepam or by combining a small horizontal component with a large vertical component indicate that the VOR is left on during these smaller gaze shifts. During quite small gaze shifts (less than 10 degrees), the VOR is clearly functioning; however, as the size of the gaze shift is increased, this becomes less clear, and there appears to be a region where the VOR operates with a gain substantially less than normal before it enters the large gaze shift region where the VOR is turned off entirely.(ABSTRACT TRUNCATED AT 400 WORDS)

Vertical vestibuloocular reflex in cat: asymmetry and adaptation

1988 ◽  
Vol 59 (2) ◽  
pp. 279-298 ◽  
Author(s):  
L. H. Snyder ◽  
W. M. King
Keyword(s):  
Eye Movement ◽  
Head Movement ◽  
Time Course ◽  
Percentage Change ◽  
Slow Phase ◽  
High Temporal Resolution ◽  
Vestibuloocular Reflex ◽  
Movement Trajectory ◽  
Head Velocity ◽  
Eye Velocity

1. We studied eye velocity during the first 2 s of the vertical vestibuloocular reflex (VOR) elicited from cats placed on their sides (90 degrees roll position) and rotated about an earth vertical axis. Vestibular stimuli were presented in the dark and consisted of brief trapezoidal velocity profiles. Eye movements were recorded with a magnetic search coil, and eye velocity was analyzed with high temporal resolution. 2. The first 2 s of upward or downward eye velocity after the onset of head rotation was characterized and compared. Adaptive changes in VOR gain (eye/head velocity) were then induced, and upward and downward eye velocity responses were again compared. 3. The early time course of the vertical VOR was complex. After a latency of approximately 15 ms, eye velocity increased rapidly until it was equal in magnitude and opposite in direction to head velocity. The peak eye velocity decayed within less than 1 s to a plateau of slow-phase eye velocity (SPEV) equal to approximately -0.6 times the head velocity. Peak upward and downward eye velocity was symmetric. The transition from peak to plateau was more rapid for the downward VOR (slow phases downward) than for the upward VOR (slow phases upward). The plateau attained by upward SPEV was approximately 15% higher than the plateau attained by downward SPEV. 4. VOR gain adaptation was symmetric. The percentage change in adapted upward eye velocity equalled the percentage change in adapted downward eye velocity. Both peak and plateau SPEV adapted, but peak eye velocity adapted less than plateau eye velocity. VOR latency was unchanged by adaptation. 5. The trajectory of the VOR response to steps of head velocity could be divided into an invariant and a variant interval. The invariant interval consisted of the initial approximately 15 ms of the eye movement. Neither direction of head movement (upward vs. downward) nor adaptation of the VOR gain effected the eye movement trajectory during the invariant interval. The variant interval began approximately 30 ms after the onset of head movement and approximately 15 ms after the onset of eye movement. In unadapted animals, downward eye speed exceeded upward eye speed during the variant interval. In adapted animals, eye speed during the variant interval, but not during the invariant interval, diverged from eye speed in the unadapted state. We suggest that the initial invariant interval (approximately 15 ms) of the eye movement response trajectory may represent the direct response of the classically described three-neuron arc.(ABSTRACT TRUNCATED AT 400 WORDS)

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