Identification of loci involved in the memory of chronic motor learning of the vertical vestibuloocular reflex in squirrel monkeys

2006 ◽  
Vol 5 (4) ◽  
pp. 296-297 ◽  
Author(s):  
Yutaka Hirata ◽  
Pablo Blazquez ◽  
Stephen Highstein
Keyword(s):  
Motor Learning ◽  
Squirrel Monkeys ◽  
Vestibuloocular Reflex

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

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.

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)

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)

scholarly journals Acute Adaptation of the Vestibuloocular Reflex: Signal Processing by Floccular and Ventral Parafloccular Purkinje Cells

2001 ◽  
Vol 85 (5) ◽  
pp. 2267-2288 ◽  
Author(s):  
Y. Hirata ◽  
S. M. Highstein
Keyword(s):  
Purkinje Cells ◽  
Unit Activity ◽  
Single Unit ◽  
Cell Activity ◽  
Squirrel Monkeys ◽  
Efference Copy ◽  
Visual Signals ◽  
Vestibuloocular Reflex ◽  
Single Unit Activity ◽  
Gain Change

The gain of the vertical vestibuloocular reflex (VVOR), defined as eye velocity/head velocity was adapted in squirrel monkeys by employing visual-vestibular mismatch stimuli. VVOR gain, measured in the dark, could be trained to values between 0.4 and 1.5. Single-unit activity of vertical zone Purkinje cells was recorded from the flocculus and ventral paraflocculus in alert squirrel monkeys before and during the gain change training. Our goal was to evaluate the site(s) of learning of the gain change. To aid in the evaluation, a model of the vertical optokinetic reflex (VOKR) and VVOR was constructed consisting of floccular and nonfloccular systems divided into subsystems based on the known anatomy and input and output parameters. Three kinds of input to floccular Purkinje cells via mossy fibers were explicitly described, namely vestibular, visual (retinal slip), and efference copy of eye movement. The characteristics of each subsystem (gain and phase) were identified at different VOR gains by reconstructing single-unit activity of Purkinje cells during VOKR and VVOR with multiple linear regression models consisting of sensory input and motor output signals. Model adequacy was checked by evaluating the residual following the regressions and by predicting Purkinje cells' activity during visual-vestibular mismatch paradigms. As a result, parallel changes in identified characteristics with VVOR adaptation were found in the prefloccular/floccular subsystem that conveys vestibular signals and in the nonfloccular subsystem that conveys vestibular signals, while no change was found in other subsystems, namely prefloccular/floccular subsystems conveying efference copy or visual signals, nonfloccular subsystem conveying visual signals, and postfloccular subsystem transforming Purkinje cell activity to eye movements. The result suggests multiple sites for VVOR motor learning including both flocculus and nonflocculus pathways. The gain change in the nonfloccular vestibular subsystem was in the correct direction to cause VOR gain adaptation while the change in the prefloccular/floccular vestibular subsystem was incorrect (anti-compensatory). This apparent incorrect directional change might serve to prevent instability of the VOR caused by positive feedback via the efference copy pathway.

Horizontal Vestibuloocular Reflex Evoked by High-Acceleration Rotations in the Squirrel Monkey. III. Responses After Labyrinthectomy

2000 ◽  
Vol 83 (5) ◽  
pp. 2482-2496 ◽  
Author(s):  
David M. Lasker ◽  
Timothy E. Hullar ◽  
Lloyd B. Minor
Keyword(s):  
Squirrel Monkey ◽  
High Frequency ◽  
Squirrel Monkeys ◽  
Spontaneous Nystagmus ◽  
Vestibuloocular Reflex ◽  
Testing Session ◽  
High Acceleration ◽  
Unilateral Labyrinthectomy ◽  
Linear And Nonlinear ◽  
Sinusoidal Rotations

The horizontal angular vestibuloocular reflex (VOR) evoked by high-frequency, high-acceleration rotations was studied in four squirrel monkeys after unilateral labyrinthectomy. Spontaneous nystagmus was measured at the beginning and end of each testing session. During the period that animals were kept in darkness (4 days), the nystagmus at each of these times measured ∼20°/s. Within 18–24 h after return to the light, the nystagmus (measured in darkness) decreased to 2.8 ± 1.5°/s (mean ± SD) when recorded at the beginning but was 20.3 ± 3.9°/s at the end of the testing session. The latency of the VOR measured from responses to steps of acceleration (3,000°/s2 reaching a velocity of 150°/s) was 8.4 ± 0.3 ms for responses to ipsilesional rotations and 7.7 ± 0.4 ms for contralesional rotations. During the period that animals were kept in darkness after the labyrinthectomy, the gain of the VOR measured during the steps of acceleration was 0.67 ± 0.12 for contralesional rotations and 0.39 ± 0.04 for ipsilesional rotations. Within 18–24 h after return to light, the VOR gain for contralesional rotations increased to 0.87 ± 0.08, whereas there was only a slight increase for ipsilesional rotations to 0.41 ± 0.06. A symmetrical increase in the gain measured at the plateau of head velocity was noted after the animals were returned to light. The VOR evoked by sinusoidal rotations of 2–15 Hz, ±20°/s, showed a better recovery of gain at lower (2–4 Hz) than at higher (6–15 Hz) frequencies. At 0.5 Hz, gain decreased symmetrically when the peak amplitude was increased from 20 to 100°/s. At 10 Hz, gain was decreased for ipsilesional half-cycles and increased for contralesional half-cycles when velocity was raised from 20 to 50°/s. A model incorporating linear and nonlinear pathways was used to simulate the data. Selective increases in the gain for the linear pathway accounted for the recovery in VOR gain for 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 contribution of the nonlinear pathway. This pathway was driven into cutoff and therefore did not affect responses for rotations toward the lesioned side.

Neural basis for motor learning in the vestibuloocular reflex of primates. II. Changes in the responses of horizontal gaze velocity Purkinje cells in the cerebellar flocculus and ventral paraflocculus

1994 ◽  
Vol 72 (2) ◽  
pp. 954-973 ◽  
Author(s):  
S. G. Lisberger ◽  
T. A. Pavelko ◽  
H. M. Bronte-Stewart ◽  
L. S. Stone
Keyword(s):  
Motor Learning ◽  
Firing Rate ◽  
Purkinje Cells ◽  
Head Motion ◽  
Vestibuloocular Reflex ◽  
Head Velocity ◽  
Simple Spike ◽  
Horizontal Gaze ◽  
Ventral Paraflocculus ◽  
Spike Firing

1. We made extracellular recordings from Purkinje cells in the flocculus and ventral paraflocculus of awake monkeys before and after motor learning in the vestibuloocular reflex (VOR). Three samples were recorded 1) after miniaturizing spectacles had reduced the gain of the VOR (eye speed divided by head speed) to 0.4; 2) when the gain of the VOR was near 1.0; and 3) after magnifying spectacles had increased the gain of the VOR to 1.6. 2. We studied Purkinje cells that showed stronger modulation of simple-spike firing rate during horizontal than during vertical pursuit. These cells corresponded to the previously identified “horizontal gaze velocity Purkinje cells” or HGVP-cells. During pursuit of smooth target motion with the head stationary, HGVP-cells showed strong modulation of firing rate with increases for ipsiversive eye motion (toward the side of recording). When the monkey canceled his VOR by tracking a target that moved exactly with him during sinusoidal head rotation in the horizontal plane, HGVP-cells again showed strong modulation of firing rate with increases for ipsiversive head motion. 3. The responses of HGVP-cells during pursuit with the head stationary and during cancellation of the VOR reveal separate components of firing rate related to eye and head velocity. We used these two behavioral conditions to test for effects of motor learning on the head and eye velocity components of the simple-spike firing of HGVP-cells. Our data confirm the previous observation that motor learning causes the sensitivity to head velocity to be larger when the gain of the VOR is high and smaller when the gain of the VOR is low. Thus we agree with the previous conclusion that changes in the vestibular sensitivity of HGVP-cells, measured during sinusoidal head motion at low frequencies, are in the wrong direction to cause changes in the gain of the VOR. 4. To determine whether the simple-spike output from the HGVP-cells plays a role in the VOR after motor learning, we recorded simple-spike firing during the VOR evoked by transient, rapid changes in head velocity in darkness. When the gain of the VOR was low, firing rate increased during the VOR evoked by ipsiversive head motion and decreased during the VOR evoked by contraversive head motion. When the gain of the VOR was high, the direction selectivity of the responses was reversed.(ABSTRACT TRUNCATED AT 400 WORDS)

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