Latency of cross-axis vestibulo-ocular reflex induced by pursuit training in monkeys

To examine the latency of smooth pursuit induced, short-term modifications of the vestibulo-ocular reflex (VOR), Japanese monkeys were rewarded for tracking a vertically moving target spot synchronized with horizontal whole body rotation. Eye movements induced by equivalent rotation in complete darkness were examined before and after training. Before training, the horizontal trapezoidal rotation (peak acceleration approximately 78%/s2) resulted in a collinear VOR with a mean latency of 15.3 ms, and no orthogonal component in any of the three monkeys tested. After training, the collinear VOR remained unchanged but an orthogonal, cross-axis VOR developed. It had a mean latency of 42.4 ms with gain (eye/chair) of 0.19, followed by a decaying phase that had a mean time constant of 80 ms. These results suggest that the cross-axis VOR induced by pursuit-vestibular interaction is different from previously reported cross-axis VOR induced by optokinetic-vestibular interaction.     

Prediction in the timing of pursuit eye movement initiation revealed by cross-axis vestibular–pursuit training in monkeys

The smooth-pursuit system interacts with the vestibular system to maintain the image of a moving target on the fovea. Efficient tracking performance requires information about the velocity and the initiation of target motion. Previous studies in monkeys have shown that training with orthogonal pursuit and whole body rotation results in adapted eye movement direction during chair rotation. In addition, the latency of the pursuit shortens and initial eye velocity increases in a task-dependent manner. To examine whether these adapted eye movements are predictive pursuit, we studied whether our monkeys could predict the timing of smooth eye movement initiation during chair rotation. Two young Japanese monkeys were rotated horizontally in a trapezoidal waveform (20°/s, ±10°) with random inter-trial intervals. A laser spot was moved vertically with the same trajectory at a constant delay ranging from 100 to 700 ms after the onset of the chair motion. The monkeys were required to pursue the spot. After this training, the latencies of pursuit eye movements following the onset of chair motion were examined in the presence of the target motion. The target was also briefly (for 500–700 ms) extinguished at 80 ms after the onset of chair rotation. Pursuit eye movements after training were initiated before the onset of target motion and the latencies were proportional to the delays used for training. The latencies and response magnitudes of pursuit with or without target blanking were similar. The auditory–pursuit training did not induce an initial pursuit response similar to that induced by vestibular–pursuit training. These results indicate that smooth eye movements during the chair rotation after the vestibular–pursuit training included a predictive pursuit component. The monkeys’ estimate of the delays revealed by the latencies of pursuit was shorter by 22–36% than the actual delays.     

Latency of vestibular responses of pursuit neurons in the caudal frontal eye fields to whole body rotation

The smooth pursuit system and the vestibular system interact to keep the retinal target image on the fovea by matching the eye velocity in space to target velocity during head and/or whole body movement. The caudal part of the frontal eye fields (FEF) in the fundus of the arcuate sulcus contains pursuit-related neurons and the majority of them respond to vestibular stimulation induced by whole body movement. To understand the role of FEF pursuit neurons in the interaction of vestibular and pursuit signals, we examined the latency and time course of discharge modulation to horizontal whole body rotation during different vestibular task conditions in head-stabilized monkeys. Pursuit neurons with horizontal preferred directions were selected, and they were classified either as gaze-velocity neurons or eye/head-velocity neurons based on the previous criteria. Responses of these neurons to whole body step-rotation at 20 degrees/s were examined during cancellation of the vestibulo-ocular reflex (VOR), VOR x1, and during chair steps in complete darkness without a target (VORd). The majority of pursuit neurons tested (approximately 70%) responded during VORd with latencies <80 ms. These initial responses were basically similar in the three vestibular task conditions. The shortest latency was 20 ms and the modal value was 24 ms. These responses were also similar between gaze-velocity neurons and eye/head-velocity neurons, indicating that the initial responses (<80 ms) were vestibular responses induced by semicircular canal inputs. During VOR cancellation and x1, discharge of the two groups of neurons diverged at approximately 90 ms following the onset of chair rotation, consistent with the latencies associated with smooth pursuit. The shortest latency to the onset of target motion during smooth pursuit was 80 ms and the modal value was 95 ms. The time course of discharge rate difference of the two groups of neurons between VOR cancellation and x1 was predicted by the discharge modulation associated with smooth pursuit. These results provide further support for the involvement of the caudal FEF in integration of vestibular inputs and pursuit signals.     

Visual tracking in monkeys: evidence for short-latency suppression of the vestibuloocular reflex

1. Monkeys normally use a combination of smooth head and eye movements to keep the eyes pointed at a slowly moving object. The visual inputs from target motion evoke smooth pursuit eye movements, whereas the vestibular inputs from head motion evoke a vestibuloocular reflex (VOR). Our study asks how the eye movements of pursuit and the VOR interact. Is there a linear addition of independent commands for pursuit and the VOR? Or does the interaction of visual and vestibular stimuli cause momentary, "parametric" modulation of transmission through VOR pathways? 2. We probed for the state of the VOR and pursuit by presenting transient perturbations of target and/or head motion under different steady-state tracking conditions. Tracking conditions included fixation at straight-ahead gaze, in which both the head and the target were stationary; "times-zero (X0) tracking," in which the target and head moved in the same direction at the same speed; and "times-two (X2) tracking," in which the target and head moved in opposite directions at the same speed. 3. Comparison of the eye velocities evoked by changes in the direction of X0 versus X2 tracking revealed two components of the tracking response. The earliest component, which we attribute to the VOR, had a latency of 14 ms and a trajectory that did not depend on initial tracking conditions. The later component had a latency of 70 ms or less and a trajectory that did depend on tracking conditions. 4. To probe the latency of pursuit eye movements, we imposed perturbations of target velocity imposed during X0 and X2 tracking. The resulting changes in eye velocity had latencies of at least 100 ms. We conclude that the effects of initial tracking conditions on eye velocity at latencies of less than 70 ms cannot be caused by visual feedback through the smooth-pursuit system. Instead, there must be another mechanism for short-latency control over the VOR; we call this component of the response "short-latency tracking." 5. Perturbations of head velocity or head and target velocity during X0 and X2 tracking showed that short-latency tracking depended only on the tracking conditions at the time the perturbation was imposed. The VOR appeared to be suppressed when the initial conditions were X0 tracking. 6. The magnitude of short-latency tracking depended on the speed of initial head and target movement. During X0 tracking at 15 deg/s, short-latency tracking was modest. When the initial speed of head and target motion was 60 deg/s, the amplitude of short-latency tracking was quite large and its latency became as short as 36 ms.(ABSTRACT TRUNCATED AT 400 WORDS)     

The initial vestibulo-ocular reflex and its visual enhancement and cancellation in humans

The gain (ratio of eye velocity to head velocity) of the initial horizontal vestibulo-ocular reflex (VOR) was calculated in 12 normal subjects over 350 ms during impulsive, unpredictable whole body rotation under three conditions: (1) darkness; (2) visual enhancement of the VOR, while the subjects fixated a stationary target; and (3) visual cancellation of the reflex, while subjects fixated a target that rotated with the head. The gain of the initial 80 ms of compensatory eye movement increased significantly during visual fixation in 5 subjects and decreased during attempted VOR cancellation in 3 subjects, when compared with VOR gain in darkness. Compensatory vestibular smooth eye movements were slowed, becoming curved at the onset of VOR cancellation, at mean latencies ranging from 78 to 149 ms in individual subjects (group mean 128 ms). At about 190 ms, quick phases moved the eyes in the same direction as head and target motion. The subsequent vestibular eye movements were about 50% slower than the initial smooth eye movements, indicating more effective cancellation. Visual enhancement of the VOR can occur prior to the onset of pursuit, providing evidence that fixation and smooth pursuit are distinct ocular motor systems. Visual cancellation of the VOR also begins prior to smooth pursuit initiation and becomes more effective after the latency of smooth pursuit.     

Activity of smooth pursuit-related neurons in the monkey periarcuate cortex during pursuit and passive whole-body rotation

Smooth pursuit and vestibularly induced eye movements interact to maintain the accuracy of eye movements in space (i.e., gaze). To understand the role played by the frontal eye fields in pursuit-vestibular interactions, we examined activity of 110 neurons in the periarcuate areas of head-stabilized Japanese monkeys during pursuit eye movements and passive whole-body rotation. The majority (92%) responded with the peak of their modulation near peak stimulus velocity during suppression of the vestibuloocular reflex (VOR) when the monkeys tracked a target that moved with the same amplitude and phase and in the same plane as the chair. We classified pursuit-related neurons (n = 100) as gaze- velocity if their peak modulation occurred for eye (pursuit) and head (VOR suppression) movements in the same direction; the amplitude of modulation during one less than twice that of the other; and modulation was lower during target-stationary-in-space condition (VOR x1) than during VOR suppression. In addition, we examined responses during VOR enhancement (x2) in which the target moved with equal amplitude as, but opposite direction to, the chair. Gaze-velocity neurons responded maximally for opposite directions during VOR x2 and suppression. Based on these criteria, the majority of pursuit-related neurons (66%) were classified as gaze-velocity with preferred directions uniformly distributed. Because the majority of the remaining cells (32/34) also responded during VOR suppression, they were classified as eye/head-velocity neurons. Thirteen preferred pursuit and VOR suppression in the same direction; 13 in the opposite direction, and 6 showed biphasic modulation during VOR suppression. Eye- and gaze-velocity sensitivity of the two groups of cells were similar; mean (+/- SD) was 0.53 +/- 0.30 and 0.50 +/- 0.44 spikes/s per degrees /s, respectively. Gaze-velocity (but not eye/head-velocity) neurons showed significant correlation between eye- and gaze-velocity sensitivity, and both groups maintained their responses when the tracking target was extinguished briefly. The majority of pursuit-related neurons (28/43 = about 65%) responded to chair rotation in complete darkness. When the monkeys fixated a stationary target, more than half of cells tested (21/40) discharged in proportion to the velocity of retinal motion of a second laser spot (mean velocity sensitivity = 0.20 +/- 0.16 spikes/s per degrees /s). Preferred directions of individual cells to the second spot were similar to those during pursuit. Visual responses to the second spot movement were maintained even when it was extinguished briefly. These results indicate that both retinal image- and gaze-velocity signals are carried by single periarcuate pursuit-related neurons, suggesting that these signals can provide target-velocity-in-space and gaze-velocity commands during pursuit-vestibular interactions.     

Discharge of pursuit neurons in the caudal part of the frontal eye fields during cross-axis vestibular-pursuit training in monkeys

Previous studies in monkeys have shown that pursuit training during orthogonal whole body rotation results in task-dependent, predictive pursuit eye movements. We examined whether pursuit neurons in the frontal eye fields (FEF) are involved in predictive pursuit induced by vestibular-pursuit training. Two monkeys were rotated horizontally at 20°/s for 0.5 s either rightward or leftward with random inter-trial intervals. This chair motion trajectory was synchronized with orthogonal target motion at 20°/s for 0.5 s either upward or downward. Monkeys were rewarded for pursuing the target. Vertical pursuit eye velocities and discharge of 23 vertical pursuit neurons to vertical target motion were compared before training and during the last 5 min of the 25–45 min training. The latencies of discharge modulation of 61% of the neurons (14/23) shortened after vestibular-pursuit training in association with a shortening of pursuit latency. However, their discharge modulation occurred after 100 ms following the onset of pursuit eye velocity. Only four neurons (4/23 = 17%) discharged before the eye movement onset. A significant change was not observed in eye velocity and FEF pursuit neuron discharge during pursuit alone after training without vestibular stimulation. Vestibular stimulation alone without a target after training induced no clear response. These results suggest that the adaptive change in response to pursuit prediction was induced by vestibular inputs in the presence of target pursuit. FEF pursuit neurons are unlikely to be involved in the initial stage of generating predictive eye movements. We suggest that they may participate in the maintenance of predictive pursuit.     

Latency of adaptive vergence eye movements induced by vergence-vestibular interaction training in monkeys

Clear vision of objects that move in depth toward or away from an observer requires vergence eye movements. The vergence system must interact with the vestibular system to maintain the object images on the foveae of both eyes during head movement. Previous studies have shown that training with sinusoidal vergence-vestibular interaction improves the frequency response of vergence eye movements during pitch rotation: vergence eye velocity gains increase and phase-lags decrease. To further understand the changes in eye movement responses in this adaptation, we examined latencies of vergence eye movements before and after vergence-vestibular training. Two head-stabilized Japanese monkeys were rewarded for tracking a target spot moving in depth that required vergence eye movements of 10°/s. This target motion was synchronized with pitch rotation at 20°/s. Both target and chair moved in a trapezoidal waveform interspersed with random inter-trial intervals. Before training, pitch rotation in complete darkness without a target did not induce vergence eye movements. Mean latencies of convergence and divergence eye movements induced by vergence target motion alone were 182 and 169 ms, respectively. After training, mean latencies of convergence and divergence eye movements to a target synchronized with pitch rotation shortened to 65 and 53 ms, and vergence eye velocity gains (relative to vergence target velocity) at the normal latencies were 0.68 and 1.53, respectively. Pitch rotation alone without a target induced vergence eye movements with similar latencies after training. These results indicate that vestibular information can be used effectively to initiate vergence eye movements following vergence-vestibular training.     

Purkinje cells of the cerebellar dorsal vermis: simple-spike activity during pursuit and passive whole-body rotation

To track a slowly moving object during whole body rotation, smooth-pursuit and vestibularly induced eye movements must interact to maintain the accuracy of eye movements in space (i.e., gaze), and gaze movement signals must eventually be converted into eye movement signals in the orbit. To understand the role played by the cerebellar vermis in pursuit-vestibular interactions, in particular whether the output of the vermis codes gaze-velocity or eye-velocity, we examined simple-spike activity of 58 Purkinje (P-) cells in lobules VI-VII of head-stabilized Japanese monkeys that were trained to elicit smooth-pursuit eye movements and cancel their vestibuloocular reflex (VOR) during passive whole body rotation around horizontal, vertical, or oblique axes. All pursuit-sensitive vermal P-cells also responded during VOR cancellation, and the majority of them had peak modulation near peak stimulus velocity. The directions of maximum modulation during these two tasks were distributed in all directions with a downward preponderance. Using standard criteria, 40% of pursuit-sensitive vermal P-cells were classified as gaze-velocity. Other P-cells were classified either as eye/head-velocity group I (36%) that had similar preferred directions during pursuit and VOR cancellation but that had larger responses during VOR x1 when gaze remained stationary, or as eye/head-velocity group II (24%) that had oppositely directed or orthogonal eye and head movement sensitivity during pursuit and VOR cancellation. Eye/head-velocity group I P-cells contained cells whose activity was correlated with eye velocity. Modulation of many P-cells of the three groups during VOR x1 could be accounted for by the linear addition of their modulations during pursuit and VOR cancellation. When monkeys fixated a stationary target, over half of the P-cells tested, including gaze-velocity P-cells, discharged in proportion to the velocity of retinal motion of a second spot. These observations are in a striking contrast to our previous results for floccular vertical P-cells. Because we used identical tasks, these differences suggest that the two cerebellar regions are involved in very different kinds of processing of pursuit-vestibular interactions.     

Role of the cerebellar flocculus region in the coordination of eye and head movements during gaze pursuit

The contribution of the flocculus region of the cerebellum to horizontal gaze pursuit was studied in squirrel monkeys. When the head was free to move, the monkeys pursued targets with a combination of smooth eye and head movements; with the majority of the gaze velocity produced by smooth tracking head movements. In the accompanying study we reported that the flocculus region was necessary for cancellation of the vestibuloocular reflex (VOR) evoked by passive whole body rotation. The question addressed in this study was whether the flocculus region of the cerebellum also plays a role in canceling the VOR produced by active head movements during gaze pursuit. The firing behavior of 121 Purkinje (Pk) cells that were sensitive to horizontal smooth pursuit eye movements was studied. The sample included 66 eye velocity Pk cells and 55 gaze velocity Pk cells. All of the cells remained sensitive to smooth pursuit eye movements during combined eye and head tracking. Eye velocity Pk cells were insensitive to smooth pursuit head movements. Gaze velocity Pk cells were nearly as sensitive to active smooth pursuit head movements as they were passive whole body rotation; but they were less than half as sensitive ( approximately 43%) to smooth pursuit head movements as they were to smooth pursuit eye movements. Considered as a whole, the Pk cells in the flocculus region of the cerebellar cortex were <20% as sensitive to smooth pursuit head movements as they were to smooth pursuit eye movements, which suggests that this region does not produce signals sufficient to cancel the VOR during smooth head tracking. The comparative effect of injections of muscimol into the flocculus region on smooth pursuit eye and head movements was studied in two monkeys. Muscimol inactivation of the flocculus region profoundly affected smooth pursuit eye movements but had little effect on smooth pursuit head movements or on smooth tracking of visual targets when the head was free to move. We conclude that the signals produced by flocculus region Pk cells are neither necessary nor sufficient to cancel the VOR during gaze pursuit.     

Role of the cerebellar flocculus region in cancellation of the VOR during passive whole body rotation

A series of studies were carried out to investigate the role of the cerebellar flocculus and ventral paraflocculus in the ability to voluntarily cancel the vestibuloocular reflex (VOR). Squirrel monkeys were trained to pursue moving visual targets and to fixate a head stationary or earth stationary target during passive whole body rotation (WBR). The firing behavior of 187 horizontal eye movement-related Purkinje (Pk) cells in the flocculus region was recorded during smooth pursuit eye movements and during WBR. Half of the Pk cells encountered were eye velocity Pk cells whose firing rates were related to eye movements during smooth pursuit and WBR. Their sensitivity to eye velocity during WBR was reduced when a visual target was not present, and their response to unpredictable steps in WBR was delayed by 80-100 ms, which suggests that eye movement sensitivity depended on visual feedback. They were insensitive to WBR when the VOR was canceled. The other half of the Purkinje cells encountered were sensitive to eye velocity during pursuit and to head velocity during VOR cancellation. They resembled the gaze velocity Pk cells previously described in rhesus monkeys. The head velocity signal tended to be less than half as large as the eye velocity-related signal and was observable at a short ( approximately 40 ms) latency when the head was unpredictably accelerated during ongoing VOR cancellation. Gaze and eye velocity type Pk cells were found to be intermixed throughout the ventral paraflocculus and flocculus. Most gaze velocity Pk cells (76%) were sensitive to ipsilateral eye and head velocity, but nearly half (48%) of the eye velocity Pk cells were sensitive to contralateral eye velocity. Thus the output of flocculus region is modified in two ways during cancellation of the VOR. Signals related to both ipsilateral and contralateral eye velocity are removed, and in approximately half of the cells a relatively weak head velocity signal is added. Unilateral injections of muscimol into the flocculus region had little effect on the gain of the VOR evoked either in the presence or absence of visual targets. However, ocular pursuit velocity and the ability to suppress the VOR by fixating a head stationary target were reduced by approximately 50%. These observations suggest that the flocculus region is an essential part of the neural substrate for both visual feedback-dependent and nonvisual mechanisms for canceling the VOR during passive head movements.     

Enhancement of the vestibulo-ocular reflex by prior eye movements.

We investigated the effect of visually mediated eye movements made before velocity-step horizontal head rotations in eleven normal human subjects. When subjects viewed a stationary target before and during head rotation, gaze velocity was initially perturbed by approximately 20% of head velocity; gaze velocity subsequently declined to zero within approximately 300 ms of the stimulus onset. We used a curve-fitting procedure to estimate the dynamic course of the gain throughout the compensatory response to head rotation. This analysis indicated that the median initial gain of compensatory eye movements (mainly because of the vestibulo-ocular reflex, VOR) was 0. 8 and subsequently increased to 1.0 after a median interval of 320 ms. When subjects attempted to fixate the remembered location of the target in darkness, the initial perturbation of gaze was similar to during fixation of a visible target (median initial VOR gain 0.8); however, the period during which the gain increased toward 1.0 was >10 times longer than that during visual fixation. When subjects performed horizontal smooth-pursuit eye movements that ended (i.e., 0 gaze velocity) just before the head rotation, the gaze velocity perturbation at the onset of head rotation was absent or small. The initial gain of the VOR had been significantly increased by the prior pursuit movements for all subjects (P < 0.05; mean increase of 11%). In four subjects, we determined that horizontal saccades and smooth tracking of a head-fixed target (VOR cancellation with eye stationary in the orbit) also increased the initial VOR gain (by a mean of 13%) during subsequent head rotations. However, after vertical saccades or smooth pursuit, the initial gaze perturbation caused by a horizontal head rotation was similar to that which occurred after fixation of a stationary target. We conclude that the initial gain of the VOR during a sudden horizontal head rotation is increased by prior horizontal, but not vertical, visually mediated gaze shifts. We postulate that this "priming" effect of a prior gaze shift on the gain of the VOR occurs at the level of the velocity inputs to the neural integrator subserving horizontal eye movements, where gaze-shifting commands and vestibular signals converge.     

A non-visual mechanism for voluntary cancellation of the vestibulo-ocular reflex

Summary Squirrel monkeys were trained to cancel their vestibulo-ocular reflex (VOR) by fixating a visual target that was head stationary during passive vestibular stimulation. The monkeys were seated on a vestibular turntable, and their heads were restrained. A small visual target (0.2°) was projected from the vestibular turntable onto a tangent screen. The monkeys' ability to suppress their VOR by fixating a head stationary target while the turntable was moving was compared to their ability to pursue the target when it was moved in the same manner.Squirrel monkeys were better able to suppress their VOR when the turntable was moved at high velocities than they were able to pursue targets that were moving at high velocities. The gaze velocity gain during VOR cancellation began to decrease when the head velocity was above 80°/s, and was greater than 0.6 when the head velocity was above 150°/s. However, gaze velocity gain during smooth pursuit decreased significantly when the target velocity was greater than 60°/s, and was less than 0.4 when the target velocity was 150°/s or more.The latency of VOR suppression was significantly shorter than the latency of smooth pursuit while the monkey was cancelling its VOR. When an unpredictable step change in head acceleration was generated while the monkey was cancelling its VOR, the VOR evoked by the head acceleration step began to be suppressed shortly after the initiation of the step ( 30 ms). On the other hand, the latency of the smooth pursuit eye movement elicited when the visual target was accelerated in the same manner during VOR cancellation was 100 ms. The comparison between these two results suggests that the monkeys did not use visual information related to target motion to suppress their VOR at an early latency.The monkeys' ability to suppress the VOR evoked by an unexpected change in head acceleration depended on the size of the head acceleration step. The VOR evoked by unexpected step changes in head acceleration was progressively less suppressed at an early latency as the size of the acceleration step increased, and was not suppressed at an early latency when the step change in head acceleration was greater than 500°/s².During smooth pursuit eye movements, unexpected step changes in head acceleration evoked a VOR that was suppressed at an early latency ( 50 ms) if the head movement was in the same direction as the ongoing smooth pursuit eye movement. The amount of early VOR suppression increased as the pursuit eye velocity increased.We conclude that squirrel monkeys utilize a fast, non-visual mechanism for cancelling their VOR while they are fixating a visual target and their head is moving. This non-visual mechanism appears to be turned on when the head is moving and the monkey is fixating a head stationary target. The mechanism probably utilizes a voluntarily gated vestibular signal to cancel the signals in VOR pathways at the level of the extraocular motorneurons. Although the VOR cancellation mechanism is not capable of completely suppressing the VOR evoked by large unexpected changes in head acceleration, we suggest that it is capable of suppressing the VOR generated by most voluntary head movements during combined eye and head gaze pursuit and that the function of this gated VOR cancellation system is to extend the range and accuracy of eye-head tracking movements.     

Experimental tests of a superposition hypothesis to explain the relationship between the vestibuloocular reflex and smooth pursuit during horizontal combined eye-head tracking in humans.

1. We used a modeling approach to test the hypothesis that, in humans, the smooth pursuit (SP) system provides the primary signal for cancelling the vestibuloocular reflex (VOR) during combined eye-head tracking (CEHT) of a target moving smoothly in the horizontal plane. Separate models for SP and the VOR were developed. The optimal values of parameters of the two models were calculated using measured responses of four subjects to trials of SP and the visually enhanced VOR. After optimal parameter values were specified, each model generated waveforms that accurately reflected the subjects' responses to SP and vestibular stimuli. The models were then combined into a CEHT model wherein the final eye movement command signal was generated as the linear summation of the signals from the SP and VOR pathways. 2. The SP-VOR superposition hypothesis was tested using two types of CEHT stimuli, both of which involved passive rotation of subjects in a vestibular chair. The first stimulus consisted of a "chair brake" or sudden stop of the subject's head during CEHT; the visual target continued to move. The second stimulus consisted of a sudden change from the visually enhanced VOR to CEHT ("delayed target onset" paradigm); as the vestibular chair rotated past the angular position of the stationary visual stimulus, the latter started to move in synchrony with the chair. Data collected during experiments that employed these stimuli were compared quantitatively with predictions made by the CEHT model. 3. During CEHT, when the chair was suddenly and unexpectedly stopped, the eye promptly began to move in the orbit to track the moving target. Initially, gaze velocity did not completely match target velocity, however; this finally occurred approximately 100 ms after the brake onset. The model did predict the prompt onset of eye-in-orbit motion after the brake, but it did not predict that gaze velocity would initially be only approximately 70% of target velocity. One possible explanation for this discrepancy is that VOR gain can be dynamically modulated and, during sustained CEHT, it may assume a lower value. Consequently, during CEHT, a smaller-amplitude SP signal would be needed to cancel the lower-gain VOR. This reduction of the SP signal could account for the attenuated tracking response observed immediately after the brake. We found evidence for the dynamic modulation of VOR gain by noting differences in responses to the onset and offset of head rotation in trials of the visually enhanced VOR.(ABSTRACT TRUNCATED AT 400 WORDS)     

Pursuit responses to target steps during ongoing tracking

Brief smooth eye-velocity responses to target position steps have been reported during smooth pursuit. We investigated position-error responses in eight healthy human subjects, comparing the effects of a step-ramp change in target position when imposed on steady-state smooth pursuit, vestibuloocular reflex (VOR) slow phases, or fixation. During steady-state pursuit or VOR, the target performed a step-ramp movement in the same or in the opposite direction relative to ongoing eye movements. When the step was directed backward relative to steady-state smooth pursuit, eye velocity transiently decreased (1.3 +/- 0.4 degrees /s; average peak change in amplitude +/- SD), beginning about 100 ms after the step. The amplitude of position-error responses varied inversely with the step size. In contrast, there was little or no response in trials with forward steps during steady-state smooth pursuit, when step-ramps were imposed on VOR or when smooth pursuit began from fixation. We hypothesize that during ongoing smooth tracking when a sudden shift in target position is detected the pursuit system compares the direction of ongoing eye velocity with the relative positional error on the retina. In the case of different relative directions between ongoing tracking and a new target eccentricity, a position-error response toward the new target is initiated. Such a mechanism might help the smooth pursuit system to respond better to changes in target direction. These experimental findings were simulated by a mathematical model of smooth pursuit by implementing direction-dependent behavior with a position-error gating mechanism.     

Directional asymmetry in smooth ocular tracking in the presence of visual background in young and adult primates

The smooth pursuit system moves the eyes in space accurately while compensating for visual inputs from the moving background and/or vestibular inputs during head movements. To understand the mechanisms underlying such interactions, we examined the influence of a stationary textured visual background on smooth pursuit tracking and compared the results in young and adult humans and monkeys. Six humans (three children, three adults) and six macaque monkeys (five young, one adult) were used. Human eye movements were recorded using infrared oculography and evoked by a sinusoidally moving target presented on a computer monitor. Scleral search coils were used for monkeys while they tracked a target presented on a tangent screen. The target moved in a sinusoidal or trapezoidal fashion with or without whole body rotation in the same plane. Two kinds of backgrounds, homogeneous and stationary textured, were used. Eye velocity gains (eye velocity/target velocity) were calculated in each condition to compare the influence of the textured background. Children showed asymmetric eye movements during vertical pursuit across the textured (but not the homogeneous) background; upward pursuit was severely impaired, and consisted mostly of catch-up saccades. In contrast, adults showed no asymmetry during pursuit across the different backgrounds. Monkeys behaved similarly; only slight effects were observed with the textured background in a mature monkey, whereas upward pursuit was severely impaired in young monkeys. In addition, VOR cancellation was severely impaired during upward eye and head movements, resulting in residual downward VOR in young monkeys. From these results, we conclude that the directional asymmetry observed in young primates may reflect a different neural organization of the vertical, particularly upward, pursuit system in the face of conflicting visual and vestibular inputs that can be associated with pursuit eye movements. Apparently, proper compensation matures later. Electronic Publication     

Oculo-manual coordination control: respective role of visual and non-visual information in ocular tracking of self-moved targets

We evaluated the role of visual and non-visual information in the control of smooth pursuit movements during tracking of a self-moved target. Previous works have shown that self-moved target tracking is characterised by shorter smooth pursuit latency and higher maximal velocity than eye-alone tracking. In fact, when a subject tracks a visual target controlled by his own arm, eye movement and arm movement are closely synchronised. In the present study, we showed that, in a condition where the direction of motion of a self-moved visual target was opposite to that of the arm (same amplitude, same velocity, but opposite direction of movement), the resulting smooth pursuit eye movements occurred with low latency, and continued for about 140 ms in the direction of the arm movement rather than in the direction of the actual visual target movement. After 140 ms, the eye movement direction reversed through a combination of smooth pursuit and saccades. Subsequently, while arm and visual target still moved in opposite directions, smooth pursuit occurred in pace with the visual target motion. Subjects were also submitted to a series of 60 tracking trials, for which the arm-to-target motion relationship was systematically reversed. Under these conditions subjects were able to initiate early smooth pursuit in the actual direction of the visual target. Overall, these results confirm that non-visual information produced by the arm motor system can trigger and control smooth pursuit. They also demonstrate the plasticity of the neuronal network handling eye-arm coordination control.     

Signals that modulate gain control for smooth pursuit eye movements in monkeys

The generation of primate smooth pursuit eye movements involves two processes. One process transforms the direction and speed of target motion into a motor command and the other regulates the strength, or "gain," of the visual-motor transformation. We have conducted a behavioral analysis to identify the signals that modulate the internal gain of pursuit. To test whether the modulatory signals are related to eye velocity in the orbit or in the world (gaze velocity), we used brief perturbations of target motion to probe the gain of pursuit during tracking conditions that used head rotation to dissociate eye and gaze velocity. We found that the responses to perturbations varied primarily as a function of gaze velocity. To further understand the gaze velocity signals that control internal pursuit gain, we used adaptive modification of the gain of the vestibulo-ocular reflex (VOR) to dissociate physical gaze velocity from the component of gaze velocity that is driven by visual inputs. After VOR adaptation, perturbation responses were altered; the smallest perturbation responses now occurred during tracking conditions that required nonzero physical gaze velocity. However, perturbation responses during tracking conditions that mimicked the modified VOR were still enhanced relative to those obtained during fixation. We conclude that the signals that modulate the internal gain of pursuit are modified by VOR adaptation so that they are rendered intermediate between physical and visually driven gaze velocity. Similar changes in the gaze velocity signal have been reported in the cerebellar floccular complex following adaptive modification of the VOR and could be present in other brain areas that carry putative gaze velocity signals.     

Visual and vergence eye movement-related responses of pursuit neurons in the caudal frontal eye fields to motion-in-depth stimuli

The caudal parts of the frontal eye fields (FEF) contain smooth-pursuit related neurons. Previous studies show that most FEF pursuit neurons carry visual signals in relation to frontal spot motion and discharge before the initiation of smooth-pursuit. It has also been demonstrated that most FEF pursuit neurons discharge during vergence tracking. Accurate vergence tracking requires information about target motion-in-depth. To further understand the role of the FEF in vergence tracking and to determine whether FEF pursuit neurons carry visual information about target motion-in-depth, we examined visual and vergence eye movement-related responses of FEF pursuit neurons to sinusoidal spot motion-in-depth. During vergence tracking, most FEF pursuit neurons exhibited both vergence eye position and velocity sensitivity. Phase shifts (re target velocity) of most neurons remained virtually constant up to 1.5 Hz. About half of FEF pursuit neurons exhibited visual responses to spot motion-in-depth. The preferred directions for visual responses of most neurons were similar to those during vergence tracking. Visual responses of most of these neurons exhibited sensitivity to the velocity of spot motion-in-depth. Phase shifts of most of the responding neurons remained virtually constant up to 2.0 Hz. Neurons that exhibited visual responses in-depth were mostly separate from neurons that showed visual responses in the frontal plane. To further examine whether FEF pursuit neurons could participate in initiation of vergence tracking, we examined latencies of neuronal responses with respect to vergence eye movements induced by step target motion-in-depth. About half of FEF pursuit neurons discharged before the onset of vergence eye movements with lead times longer than 20 ms. These results together with previous observations suggest that the caudal FEF carries visual signals appropriate to be converted into motor commands for pursuit in depth and frontal plane.     

Directional asymmetry in vertical smooth-pursuit and cancellation of the vertical vestibulo-ocular reflex in juvenile monkeys

Young primates exhibit asymmetric eye movements during vertical smooth-pursuit across a textured background such that upward pursuit has low velocity and requires many catch-up saccades. The asymmetric eye movements cannot be explained by the un-suppressed optokinetic reflex resulting from background visual motion across the retina during pursuit, suggesting that the asymmetry reflects most probably, a low gain in upward eye commands (Kasahara et al. in Exp Brain Res 171:306–321, 2006). In this study, we examined (1) whether there are intrinsic differences in the upward and downward pursuit capabilities and (2) how the difficulty in upward pursuit is correlated with the ability of vertical VOR cancellation. Three juvenile macaques that had initially been trained only for horizontal (but not vertical) pursuit were trained for sinusoidal pursuit in the absence of a textured background. In 2 of the 3 macaques, there was a clear asymmetry between upward and downward pursuit gains and in the time course of initial gain increase. In the third macaque, downward pursuit gain was also low. It did not show consistent asymmetry during the initial 2 weeks of training. However, it also exhibited a significant asymmetry after 4 months of training, similar to the other two monkeys. After 6 months of training, these two monkeys (but not the third) still exhibited asymmetry. As target frequency increased in these two monkeys, mean upward eye velocity saturated at ∼15°/s, whereas horizontal and downward eye velocity increased up to ∼40°/s. During cancellation of the VOR induced by upward whole body rotation, downward eye velocity of the residual VOR increased as the stimulus frequency increased. Gain of the residual VOR during upward rotation was significantly higher than that during horizontal and downward rotation. The time course of residual VOR induced by vertical whole body step-rotation during VOR cancellation was predicted by addition of eye velocity during pursuit and VOR x1. These results support our view that the directional asymmetry reflects the difference in the organization of the cerebellar floccular region for upward and downward directions and the preeminent role of pursuit in VOR cancellation.