Neuronal Substrates of Motor Learning in the Velocity Storage Generated During Optokinetic Stimulation in the Squirrel Monkey

2007 ◽  
Vol 97 (2) ◽  
pp. 1114-1126 ◽  
Author(s):  
Pablo M. Blazquez ◽  
Maria A. Davis-Lopez de Carrizosa ◽  
Shane A. Heiney ◽  
Stephen M. Highstein
Keyword(s):  
Motor Learning ◽  
Brain Stem ◽  
High Gain ◽  
Velocity Storage ◽  
Optokinetic Stimulation ◽  
Optokinetic Response ◽  
Head Velocity ◽  
Velocity Sensitivity ◽  
Before And After ◽  
Eye Velocity

Chronic motor learning in the vestibuloocular reflex (VOR) results in changes in the gain of this reflex and in other eye movements intimately associated with VOR behavior, e.g., the velocity storage generated by optokinetic stimulation (OKN velocity storage). The aim of the present study was to identify the plastic sites responsible for the change in OKN velocity storage after chronic VOR motor learning. We studied the neuronal responses of vertical eye movement flocculus target neurons (FTNs) during the optokinetic afternystagmus (OKAN) phase of the optokinetic response (OKR) before and after VOR motor learning. Our findings can be summarized as follows. 1) Chronic VOR motor learning changes the horizontal OKN velocity storage in parallel with changes in VOR gain, whereas the vertical OKN velocity storage is more complex, increasing with VOR gain increases, but not changing following VOR gain decreases. 2) FTNs contain an OKAN signal having opposite directional preferences after chronic high versus low gain learning, suggesting a change in the OKN velocity storage representation of FTNs. 3) Changes in the eye-velocity sensitivity of FTNs during OKAN are correlated with changes in the brain stem head-velocity sensitivity of the same neurons. And 4) these changes in eye-velocity sensitivity of FTNs during OKAN support the new behavior after high gain but not low gain learning. Thus we hypothesize that the changes observed in the OKN velocity storage behavior after chronic learning result from changes in brain stem pathways carrying head velocity and OKN velocity storage information, and that a parallel pathway to vertical FTNs changes its OKN velocity storage representation following low, but not high, gain VOR motor learning.

Precerebellar Hindbrain Neurons Encoding Eye Velocity During Vestibular and Optokinetic Behavior in the Goldfish

2006 ◽  
Vol 96 (3) ◽  
pp. 1370-1382 ◽  
Author(s):  
James C. Beck ◽  
Paul Rothnie ◽  
Hans Straka ◽  
Susan L. Wearne ◽  
Robert Baker
Keyword(s):  
Firing Rate ◽  
Eye Movement ◽  
Time Course ◽  
Mossy Fiber ◽  
Vestibular Stimulation ◽  
Neuronal Firing ◽  
Velocity Storage ◽  
Head Velocity ◽  
Motor Error ◽  
Eye Velocity

Elucidating the causal role of head and eye movement signaling during cerebellar-dependent oculomotor behavior and plasticity is contingent on knowledge of precerebellar structure and function. To address this question, single-unit extracellular recordings were made from hindbrain Area II neurons that provide a major mossy fiber projection to the goldfish vestibulolateral cerebellum. During spontaneous behavior, Area II neurons exhibited minimal eye position and saccadic sensitivity. Sinusoidal visual and vestibular stimulation over a broad frequency range (0.1–4.0 Hz) demonstrated that firing rate mirrored the amplitude and phase of eye or head velocity, respectively. Table frequencies >1.0 Hz resulted in decreased firing rate relative to eye velocity gain, while phase was unchanged. During visual steps, neuronal discharge paralleled eye velocity latency (∼90 ms) and matched both the build-up and the time course of the decay (∼19 s) in eye velocity storage. Latency of neuronal discharge to table steps (40 ms) was significantly longer than for eye movement (17 ms), but firing rate rose faster than eye velocity to steady-state levels. The velocity sensitivity of Area II neurons was shown to equal (±10%) the sum of eye- and head-velocity firing rates as has been observed in cerebellar Purkinje cells. These results demonstrate that Area II neuronal firing closely emulates oculomotor performance. Conjoint signaling of head and eye velocity together with the termination pattern of each Area II neuron in the vestibulolateral lobe presents a unique eye-velocity brain stem-cerebellar pathway, eliminating the conceptual requirement of motor error signaling.

Dorsal Y group in the squirrel monkey. I. Neuronal responses during rapid and long-term modifications of the vertical VOR

1995 ◽  
Vol 73 (2) ◽  
pp. 615-631 ◽  
Author(s):  
A. M. Partsalis ◽  
Y. Zhang ◽  
S. M. Highstein
Keyword(s):  
Eye Movement ◽  
Neuronal Response ◽  
Head Rotation ◽  
High Gain ◽  
Optokinetic Stimulation ◽  
Linear Interaction ◽  
Full Field ◽  
Head Velocity ◽  
Visual Vestibular Interaction ◽  
Y Cells

1. The activity of 113 Y group neurons was recorded extracellularly in 5 alert squirrel monkeys. Sixty-two cells were recorded in naive animals, and 51 cells were recorded after adaptation of the vestibuloocular reflex (VOR) with the use of telescopic lenses. The animals were lying on their right side, so that head rotation was in the vertical (pitch) plane and optokinetic stimulation elicited vertical eye movement. The responses of most cells, as well as the concurrent eye movement, were studied during 1) the VOR, elicited in darkness or in light by sinusoidal head rotation, 2) visual following, elicited by sinusoidal rotation of a full-field optokinetic drum around the stationary animal, and 3) paradigms of visual-vestibular interaction, elicited by combined sinusoidal vestibular and optokinetic stimulation. Stimulation parameters for both head and drum velocity were usually 0.5 Hz, 35 degrees/s peak velocity. 2. Y group cells respond vigorously during visual following and during suppression of the VOR (produced by in-phase rotation of the head and the optokinetic drum); the response is approximately in-phase with eye velocity during visual following, and approximately in-phase with head velocity during suppression of the VOR. During the VOR in darkness, Y cells usually exhibit only slight modulation. The results suggest a linear interaction of visual following and vestibular signals on Y cells during vertical visual-vestibular interaction. Taking into account the excitatory projection of Y cells to superior rectus and inferior oblique motoneurons, a causal role of the Y group in rapid modification of VOR gain during visual-vestibular interaction is suggested. 3. Nine Y neurons from two animals were recorded continuously, for periods ranging from 30 min to 5 h, while the VOR was being adapted to higher or lower gain. Progressive changes of the gain of the VOR in darkness were evident after approximately 30 min from the initiation of head rotation under visual-vestibular mismatch. Consistent changes of the gain and/or phase of the neuronal response during the VOR in darkness were noted in all cases. The phase of the neuronal response gradually approximated head velocity phase during adaptation of the VOR to low gain, increases in the neuronal gain thereafter ensued; the opposite changes were observed during adaptation of the VOR to high gain. 4. Sixteen Y cells were recorded from 1 animal chronically adapted to high VOR gain with the use of magnifying lenses, and 35 cells were recorded from 2 animals chronically adapted to low VOR gain with the use of miniaturizing lenses.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Negative optokinetic afternystagmus in larval zebrafish demonstrates set-point adaptation

2019 ◽  
Vol 9 (1) ◽  
Author(s):  
Ting-Feng Lin ◽  
Mohammad Mohammadi ◽  
Ahmed M. Fathalla ◽  
Duygu Pul ◽  
Dennis Lüthi ◽  
...  
Keyword(s):  
Motor Learning ◽  
Light Extinction ◽  
Slow Phase ◽  
Optokinetic Stimulation ◽  
Zebrafish Model ◽  
Set Point ◽  
Larval Zebrafish ◽  
Optokinetic Afternystagmus ◽  
Sensorimotor Memory ◽  
Eye Velocity

AbstractMotor learning is essential to maintain accurate behavioral responses. We used a larval zebrafish model to study ocular motor learning behaviors. During a sustained period of optokinetic stimulation in 5-day-old wild-type zebrafish larvae the slow-phase eye velocity decreased over time. Then interestingly, a long-lasting and robust negative optokinetic afternystagmus (OKAN) was evoked upon light extinction. The slow-phase velocity, the quick-phase frequency, and the decay time constant of the negative OKAN were dependent on the stimulus duration and the adaptation to the preceding optokinetic stimulation. Based on these results, we propose a sensory adaptation process during continued optokinetic stimulation, which, when the stimulus is removed, leads to a negative OKAN as the result of a changed retinal slip velocity set point, and thus, a sensorimotor memory. The pronounced negative OKAN in larval zebrafish not only provides a practical solution to the hitherto unsolved problems of observing negative OKAN, but also, and most importantly, can be readily applied as a powerful model for studying sensorimotor learning and memory in vertebrates.

Compensatory and Orienting Eye Movements Induced By Off-Vertical Axis Rotation (OVAR) in Monkeys

2002 ◽  
Vol 88 (5) ◽  
pp. 2445-2462 ◽  
Author(s):  
Keisuke Kushiro ◽  
Mingjia Dai ◽  
Mikhail Kunin ◽  
Sergei B. Yakushin ◽  
Bernard Cohen ◽  
...  
Keyword(s):  
Eye Movements ◽  
Vertical Axis ◽  
Velocity Storage ◽  
Eye Position ◽  
Rotational Axis ◽  
Vestibuloocular Reflex ◽  
Time Constants ◽  
Head Velocity ◽  
Axis Rotation ◽  
Eye Velocity

Nystagmus induced by off-vertical axis rotation (OVAR) about a head yaw axis is composed of a yaw bias velocity and modulations in eye position and velocity as the head changes orientation relative to gravity. The bias velocity is dependent on the tilt of the rotational axis relative to gravity and angular head velocity. For axis tilts <15°, bias velocities increased monotonically with increases in the magnitude of the projected gravity vector onto the horizontal plane of the head. For tilts of 15–90°, bias velocity was independent of tilt angle, increasing linearly as a function of head velocity with gains of 0.7–0.8, up to the saturation level of velocity storage. Asymmetries in OVAR bias velocity and asymmetries in the dominant time constant of the angular vestibuloocular reflex (aVOR) covaried and both were reduced by administration of baclofen, a GABAB agonist. Modulations in pitch and roll eye positions were in phase with nose-down and side-down head positions, respectively. Changes in roll eye position were produced mainly by slow movements, whereas vertical eye position changes were characterized by slow eye movements and saccades. Oscillations in vertical and roll eye velocities led their respective position changes by ≈90°, close to an ideal differentiation, suggesting that these modulations were due to activation of the orienting component of the linear vestibuloocular reflex (lVOR). The beating field of the horizontal nystagmus shifted the eyes 6.3°/ g toward gravity in side down position, similar to the deviations observed during static roll tilt (7.0°/ g). This demonstrates that the eyes also orient to gravity in yaw. Phases of horizontal eye velocity clustered ∼180° relative to the modulation in beating field and were not simply differentiations of changes in eye position. Contributions of orientating and compensatory components of the lVOR to the modulation of eye position and velocity were modeled using three components: a novel direct otolith-oculomotor orientation, orientation-based velocity modulation, and changes in velocity storage time constants with head position re gravity. Time constants were obtained from optokinetic after-nystagmus, a direct representation of velocity storage. When the orienting lVOR was combined with models of the compensatory lVOR and velocity estimator from sequential otolith activation to generate the bias component, the model accurately predicted eye position and velocity in three dimensions. These data support the postulates that OVAR generates compensatory eye velocity through activation of velocity storage and that oscillatory components arise predominantly through lVOR orientation mechanisms.

Cerebellar role in adaptation of the goldfish vestibuloocular reflex

1994 ◽  
Vol 72 (3) ◽  
pp. 1383-1394 ◽  
Author(s):  
A. M. Pastor ◽  
R. R. de la Cruz ◽  
R. Baker
Keyword(s):  
Dynamic Response ◽  
Brain Stem ◽  
Purkinje Cells ◽  
Constant Velocity ◽  
Time Course ◽  
Vertical Axis ◽  
Vestibular Stimulation ◽  
Vestibuloocular Reflex ◽  
Head Velocity ◽  
Eye Velocity

1. The time course of eye velocity responses elicited by head velocity steps was compared in normal, adapted, and cerebellectomized goldfish. Vestibuloocular reflex (VOR) adaptation was induced by combined visual and vestibular stimulation that altered the ratio of eye to head velocity (VOR gain) toward values either higher or lower than the control amplitude. The velocity step consisted of alternating periods of head rotation at a constant velocity of 16 degrees/s zero-to-peak around the vertical axis. 2. The VOR produced by head velocity steps consisted of an early acceleration-related component, the dynamic response, separated from a sustained period of constant velocity, the plateau, by a sag that occurred around 125-150 ms. Latency of the VOR averaged 18 ms for the adducting eye and 20 ms for abducting eye independent of the initial VOR gain. Adapted dynamic VOR responses diverged from the control records at the earliest detectable latency after both high and low VOR gain training. This result demonstrates modification in the shortest latency brain stem VOR pathway, presumably, the three-neuron reflex arc. 3. After acute cerebellectomy the adapted dynamic response was unaltered for approximately 50 ms in the low-gain and 70 ms in the high-gain VOR states. Not less than 30% of the altered velocity was retained throughout the remaining dynamic and sustained component. These results demonstrate that the vestibulocerebellum is not necessary for the maintenance of the earliest adapted eye velocity. Hence brain stem pathways are sufficient for the expression of the modified VOR. 4. Purkinje cells identified by simple and complex spikes were recorded extracellularly in the area of the vestibulocerebellum, where electrical stimulation produced conjugate ipsiversive horizontal eye movements. Independent eye and head velocity sensitivities were determined in response to visual world motion and VOR suppression, respectively. The two signals either added, canceled, or were both present in Purkinje cells throughout the range of eye velocity induced by vertical axis visual-vestibular stimulation. 5. Latency of Purkinje cell discharge to either a vestibular or visual velocity step exhibited means of 43 and 70 ms, respectively.(ABSTRACT TRUNCATED AT 400 WORDS)

scholarly journals Normal Performance and Expression of Learning in the Vestibulo-Ocular Reflex (VOR) at High Frequencies

2005 ◽  
Vol 93 (4) ◽  
pp. 2028-2038 ◽  
Author(s):  
Ramnarayan Ramachandran ◽  
Stephen G. Lisberger
Keyword(s):  
Phase Shift ◽  
Harmonic Distortion ◽  
Head Movements ◽  
High Frequencies ◽  
Head Velocity ◽  
Ocular Reflex ◽  
Before And After ◽  
Vestibulo Ocular Reflex ◽  
Eye Velocity ◽  
Normal Performance

The rotatory vestibulo-ocular reflex (VOR) keeps the visual world stable during head movements by causing eye velocity that is equal in amplitude and opposite in direction to angular head velocity. We have studied the performance of the VOR in darkness for sinusoidal angular head oscillation at frequencies ranging from 0.5 to 50 Hz. At frequencies of ≥25 Hz, the harmonic distortion of the stimulus and response were estimated to be <14 and 22%, respectively. We measured the gain of the VOR (eye velocity divided by head velocity) and the phase shift between eye and head velocity before and after adaptation with altered vision. Before adaptation, VOR gains were close to unity for frequencies ≤20 Hz and increased as a function of frequency reaching values of 3 or 4 at 50 Hz. Eye velocity was almost perfectly out of phase with head velocity for frequencies ≤12.5 Hz, and lagged perfect compensation increasingly as a function of frequency. After adaptive modification of the VOR with magnifying or miniaturizing optics, gain showed maximal changes at frequencies <12.5 Hz, smaller changes at higher frequencies, and no change at frequencies larger than 25 Hz. Between 15 and 25 Hz, the phase of eye velocity led the unmodified VOR by as much as 50° when the gain of the VOR had been decreased, and lagged when the gain of the VOR had been increased. We were able to reproduce the main features of our data with a two-pathway model of the VOR, where the two pathways had different relationships between phase shift and frequency.

The effect of d-amphetamine on optokinetic nystagmus in the guinea pig

1999 ◽  
Vol 9 (2) ◽  
pp. 127-133
Author(s):  
V.V. Marlinsky ◽  
M. Reber ◽  
J. Kröller
Keyword(s):  
Guinea Pig ◽  
Optokinetic Nystagmus ◽  
Regression Line ◽  
Velocity Storage ◽  
Mean Values ◽  
Amphetamine Administration ◽  
Before And After ◽  
The Mean ◽  
Eye Velocity ◽  
The Relationship

The effect of d-amphetamine oral administration in doses of 1–2.5 mg/kg on horizontal optokinetic nystagmus (OKN) and afternystagmus (OKAN) was investigated in the guinea pig. Eye movements were recorded by means of the electromagnetic search-coil technique. After amphetamine administration the range of stimulus velocities effective for eliciting OKN was 10–20 deg/s higher than before treatment. The mean values and the fluctuations of the eye velocity during slow nystagmus phases before and after treatment did not differ. Aministration of amphetamine led to 2–8 s increase in OKAN duration. The OKAN prolongation did not depend on stimulation velocity. The dependency of OKAN duration on stimulation velocity was well approximated by a linear regression. The slope of the regression line was 0.160 ± 0.022 before and 0.177 ± 0.028 after treatment. Similarity in the coefficients indicates that amphetamine did not alter the relationship between the velocity of optokinetic stimulus and the duration of afternystagmus. Constant prolongation of OKAN over the whole range of stimulation velocities could reflect a constant shift in activity of neurons representing the velocity storage. The effects observed on OKN gain curves and the increase in OKAN duration did not display a clear dependency on the dosages of d-amphetamine used in the experiments. We assume that the effects of treatment reflected a general increase in attentiveness and motility of animals resulting from the arousal action of amphetamine.

The effect of habituation and plane of rotation on vestibular perceptual responses

2000 ◽  
Vol 10 (4-5) ◽  
pp. 193-200
Author(s):  
E.A. Grunfeld ◽  
T. Okada ◽  
K. Jáuregui-Renaud ◽  
A.M. Bronstein
Keyword(s):  
Angular Velocity ◽  
Median Time ◽  
Time Constant ◽  
Vertical Axis ◽  
Head Position ◽  
Velocity Storage ◽  
Optokinetic Stimulation ◽  
Axis Of Rotation ◽  
Before And After ◽  
Head Roll

A technique was applied to assess vestibular sensation without reference to external spatial, position cues. The stimuli were stopping responses to velocity-steps of 90 deg/s in the dark. Subjects indicated their perceived angular velocity by turning a flywheel connected to a tachogenerator. Two separate experiments were conducted. In one, subjects were rotated in yaw about an earth-vertical axis before and after prolonged rotational or visual (optokinetic) stimuli. In the second experiment, subjects were rotated in roll supine, with either the head (`roll centred') or the feet (`roll eccentric') on the axis of rotation. The two aims of the paper were to (i) examine the effect of repetitive vestibular and optokinetic stimulation on the time constant of decay of vestibular sensation in yaw; (ii) to compare vestibular sensation responses to rotation in roll both with and without the addition of a Z-axis centrifugal force. The pre-habituation sensation response in yaw decayed exponentially with a median time constant of 12.8 s. The duration of the sensation responses were significantly reduced following both prolonged vestibular and optokinetic stimulation. The reduction in vestibular responses following prolonged visual and vestibular stimuli, 1) is likely to occur in velocity storage mechanisms mediating ocular and perceptual responses, 2) may represent a mechanism for reducing the disorientating consequences of visual-vestibular conflict and 3) supports the use of optokinetic stimuli as a treatment for vestibular patients. The time constant of the sensation responses in roll was shorter and not significantly influenced by head position: 5.7 s in the head-centred position compared to 4.7 s in the eccentric head position. Therefore, perceptual as well as ocular responses to rotation in roll are determined primarily by cupula dynamics and not influenced by velocity storage.

Chronic Changes in Inputs to Dorsal Y Neurons Accompany VOR Motor Learning

2006 ◽  
Vol 95 (3) ◽  
pp. 1812-1825 ◽  
Author(s):  
Pablo M Blazquez ◽  
Yutaka Hirata ◽  
Stephen M. Highstein
Keyword(s):  
Motor Learning ◽  
Brain Stem ◽  
Purkinje Cells ◽  
Intact Animal ◽  
High Gain ◽  
Parallel Pathways ◽  
Gain Adaptation ◽  
Vor Adaptation ◽  
The Brain

Gain changes in the vestibuloocular reflex (VOR) during visual-vestibular mismatch stimulation serve as a model system for motor learning. The cerebellar flocculus and its target neurons in the brain stem (FTN) are candidates for the storage of these novel VOR gains. We have recently studied the changes in vertical flocculus Purkinje cells after chronic VOR motor learning. Recently we recorded Y neurons (a vertical type of FTNs) after chronic VOR motor learning and compared these records with vertical floccular Purkinje cells to document any changes in inputs to FTNs and understand how Y neurons and the vertical Purkinje cells fit into a general model for the vertical VOR. Analysis illustrates that the changes observed in Purkinje cells are not transferred to Y neurons, suggesting that the gain of their synaptic interconnection was modified. We quantified changes in both populations and employed simulations to study changes in parallel pathways to FTNs and to extract the role of the flocculus in VOR adaptation. Low-gain adaptation results in more drastic changes than its high-gain counterpart, causing increases in head velocity sensitivity in parallel pathways. Simulations suggest that cerebellar and brain stem plasticity both participate in novel VOR gain storage and that results obtained following floccular lesion are the product of different mechanisms than those operating in the intact animal.

scholarly journals Occurrence of long-term depression in the cerebellar flocculus during adaptation of optokinetic response

eLife ◽  
2018 ◽  
Vol 7 ◽  
Author(s):  
Takuma Inoshita ◽  
Tomoo Hirano
Keyword(s):  
Motor Learning ◽  
Visual Image ◽  
Cellular Mechanism ◽  
Optokinetic Stimulation ◽  
Wild Type ◽  
Long Term Depression ◽  
Optokinetic Response ◽  
Cerebellar Flocculus ◽  
In The Wild

Long-term depression (LTD) at parallel fiber (PF) to Purkinje cell (PC) synapses has been considered as a main cellular mechanism for motor learning. However, the necessity of LTD for motor learning was challenged by demonstration of normal motor learning in the LTD-defective animals. Here, we addressed possible involvement of LTD in motor learning by examining whether LTD occurs during motor learning in the wild-type mice. As a model of motor learning, adaptation of optokinetic response (OKR) was used. OKR is a type of reflex eye movement to suppress blur of visual image during animal motion. OKR shows adaptive change during continuous optokinetic stimulation, which is regulated by the cerebellar flocculus. After OKR adaptation, amplitudes of quantal excitatory postsynaptic currents at PF-PC synapses were decreased, and induction of LTD was suppressed in the flocculus. These results suggest that LTD occurs at PF-PC synapses during OKR adaptation.

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