Pursuit Direction Research Articles

Farthest North Polar Bear (<i>Ursus maritimus</i>)

On 5 August 2001, while on a cruise with tourists from Longyearbyen, Svalbard, to the Geographic North Pole, we sighted a lone polar bear (Ursus maritimus) from the Russian icebreaker Yamal at a site we believe to be the northernmost record of this species. The adult bear was seen walking slowly on the ice toward the ship about 500 meters away. The location of the ship, as determined by the ship's Global Positioning System (GPS), was 89°46.5'N, 26°21.1'E, about 13 nautical miles from the Pole. No seals were seen in the area on that day, although on an earlier date (8 August 1993), one of us (JFS) sighted a ringed seal (Phoca hispida) in the water adjacent to the Yamal upon reaching the Pole. Many other sightings of polar bears were made on the August 2001 cruise, both prior to this date and also later, as the ship reached Franz Josef Land [Zemlya Frantsa-Iosifa], Russia, the next objective after the Pole. The voyage began at Longyearbyen on 1 August and ended there on 12 August 2001. ... Ice conditions in the area of the sighting on 5 August 2001 ranged from unbroken 10/10 multiyear sea ice to 8/10-9/10 broken multiyear ice. ... Winds and currents can ... be responsible for relatively rapid ice-cover changes in foraging habitats for polar bears, perhaps making it more opportunistic for them to move northward or in other directions in pursuit of prey. Whether those factors might have been instrumental in producing the conditions of our polar bear sighting only 13.5 nautical miles (15.5 statute miles/25 km) from the North Pole cannot be ascertained. Considering the water depth at the Geographic North Pole (4179 m, or 13 710'), with little likelihood of upwelling and generation of nutrients for seals and lower elements of the food chain, it is unlikely that seals and polar bears would normally venture this far north. However, Todd et al. (1992) noticed, as we did, light-brown algae frozen within some of the ice en route to the Pole, and they also mention sighting tracks of arctic fox (Alopex lagopus) in hard-packed snow at 89°11.15'N in July 1992. ...

Pursuit speed compensation in cortical area MSTd.

When we move forward the visual images on our retinas expand. Humans rely on the focus, or center, of this expansion to estimate their direction of self-motion or heading and, as long as the eyes are still, the retinal focus corresponds to the heading. However, smooth pursuit eye movements add visual motion to the expanding retinal image and displace the focus of expansion. In spite of this, humans accurately judge their heading during pursuit eye movements even though the retinal focus no longer corresponds to the heading. Recent studies in macaque suggest that correction for pursuit may occur in the dorsal aspect of the medial superior temporal area (MSTd); neurons in this area are tuned to the retinal position of the focus and they modify their tuning to partially compensate for the focus shift caused by pursuit. However, the question remains whether these neurons shift focus tuning more at faster pursuit speeds, to compensate for the larger focus shifts created by faster pursuit. To investigate this question, we recorded from 40 MSTd neurons while monkeys made pursuit eye movements at a range of speeds across simulated self- or object motion displays. We found that most MSTd neurons modify their focus tuning more at faster pursuit speeds, consistent with the idea that they encode heading and other motion parameters regardless of pursuit speed. Across the population, the median rate of compensation increase with pursuit speed was 51% as great as required for perfect compensation. We recorded from the same neurons in a simulated pursuit condition, in which gaze was fixed but the entire display counter-rotated to produce the same retinal image as during real pursuit. This condition yielded the result that retinal cues contribute to pursuit compensation; the rate of compensation increase was 30% of that required for accurate encoding of heading. The difference between these two conditions was significant (P < 0.05), indicating that extraretinal cues also contribute significantly. We found a systematic antialignment between preferred pursuit and preferred visual motion directions. Neurons may use this antialignment to combine retinal and extraretinal compensatory cues. These results indicate that many MSTd neurons compensate for pursuit velocity, pursuit direction as previously reported and pursuit speed, and further implicate MSTd as a critical stage in the computation of egomotion.

Spatial generalization of learning in smooth pursuit eye movements: implications for the coordinate frame and sites of learning.

We have examined the underlying coordinate frame for pursuit learning by testing how broadly learning generalizes to different retinal loci and directions of target motion. Learned changes in pursuit were induced using double steps of target speed. Monkeys tracked a target that stepped obliquely away from the point of fixation, then moved smoothly either leftward or rightward. In each experimental session, we adapted the response to targets moving in one direction across one locus of the visual field by changing target speed during the initial catch-up saccade. Learning occurred in both presaccadic and postsaccadic eye velocity. The changes were specific to the adapted direction and did not generalize to the opposite direction of pursuit. To test the spatial scale of learning, we examined the responses to targets that moved across different parts of the visual field at the same velocity as the learning targets. Learning generalized partially to motion presented at untrained locations in the visual field, even those across the vertical meridian. Experiments with two sets of learning trials showed interference between learning at different sites in the visual field, suggesting that pursuit learning is not capable of spatial specificity. Our findings are consistent with the previous suggestions that pursuit learning is encoded in an intermediate representation that is neither strictly sensory nor strictly motor. Our data add the constraint that the site or sites of pursuit learning must process visual information on a fairly large spatial scale that extends across the horizontal and vertical meridians.

Spatial Generalization of Learning in Smooth Pursuit Eye Movements: Implications for the Coordinate Frame and Sites of Learning

We have examined the underlying coordinate frame for pursuit learning by testing how broadly learning generalizes to different retinal loci and directions of target motion. Learned changes in pursuit were induced using double steps of target speed. Monkeys tracked a target that stepped obliquely away from the point of fixation, then moved smoothly either leftward or rightward. In each experimental session, we adapted the response to targets moving in one direction across one locus of the visual field by changing target speed during the initial catch-up saccade. Learning occurred in both presaccadic and postsaccadic eye velocity. The changes were specific to the adapted direction and did not generalize to the opposite direction of pursuit. To test the spatial scale of learning, we examined the responses to targets that moved across different parts of the visual field at the same velocity as the learning targets. Learning generalized partially to motion presented at untrained locations in the visual field, even those across the vertical meridian. Experiments with two sets of learning trials showed interference between learning at different sites in the visual field, suggesting that pursuit learning is not capable of spatial specificity. Our findings are consistent with the previous suggestions that pursuit learning is encoded in an intermediate representation that is neither strictly sensory nor strictly motor. Our data add the constraint that the site or sites of pursuit learning must process visual information on a fairly large spatial scale that extends across the horizontal and vertical meridians.

Role of arcuate frontal cortex of monkeys in smooth pursuit eye movements. I. Basic response properties to retinal image motion and position.

Anatomical and physiological studies have shown that the "frontal pursuit area" (FPA) in the arcuate cortex of monkeys is involved in the control of smooth pursuit eye movements. To further analyze the signals carried by the FPA, we examined the activity of pursuit-related neurons recorded from a discrete region near the arcuate spur during a variety of oculomotor tasks. Pursuit neurons showed direction tuning with a wide range of preferred directions and a mean full width at half-maximum of 129 degrees. Analysis of latency using the "receiver operating characteristic" to compare responses to target motion in opposite directions showed that the directional response of 58% of FPA neurons led the initiation of pursuit, while 19% led by 25 ms or more. Analysis of neuronal responses during pursuit of a range of target velocities revealed that the sensitivity to eye velocity was larger during the initiation of pursuit than during the maintenance of pursuit, consistent with two components of firing related to image motion and eye motion. FPA neurons showed correlates of two behavioral features of pursuit documented in prior reports. 1) Eye acceleration at the initiation of pursuit declines as a function of the eccentricity of the moving target. FPA neurons show decreased firing at the initiation of pursuit in parallel with the decline in eye acceleration. This finding is consistent with prior suggestions that the FPA plays a role in modulating the gain of visual-motor transmission for pursuit. 2) A stationary eccentric cue evokes a smooth eye movement opposite in direction to the cue and enhances the pursuit evoked by subsequent target motions. Many pursuit neurons in the FPA showed weak, phasic visual responses for stationary targets and were tuned for the positions about 4 degrees eccentric on the side opposite to the preferred pursuit direction. However, few neurons (12%) responded during the preparation or execution of saccades. The responses to the stationary target could account for the behavioral effects of stationary, eccentric cues. Further analysis of the relationship between firing rate and retinal position error during pursuit in the preferred and opposite directions failed to provide evidence for a large contribution of image position to the firing of FPA neurons. We conclude that FPA processes information in terms of image and eye velocity and that it is functionally separate from the saccadic frontal eye fields, which processes information in terms of retinal image position.

Volitional scaling of anticipatory ocular pursuit velocity using precues

Human subjects cannot normally perform smooth eye movements in the absence of a target. However, the repeated presentation of identical, transient target motion stimuli, preceded by warning cues, leads to the build up of anticipatory smooth pursuit (ASP) eye movements several hundred milliseconds prior to stimulus onset. The present study sought to investigate whether subjects are able to volitionally scale ASP speed, as well as select pursuit direction, in advance of target motion stimuli of random direction (left vs. right) and speed (10, 20, 30 and 40° /s), given stationary precues predictive of both these target parameters. The subjects’ success at this task is discussed in terms of their ability to volitionally scale the internal store of target velocity information postulated to drive ASP.

Enhancement of multiple components of pursuit eye movement by microstimulation in the arcuate frontal pursuit area in monkeys.

Periarcuate frontal cortex is involved in the control of smooth pursuit eye movements, but its role remains unclear. To better understand the control of pursuit by the "frontal pursuit area" (FPA), we applied electrical microstimulation when the monkeys were performing a variety of oculomotor tasks. In agreement with previous studies, electrical stimulation consisting of a train of 50-microA pulses at 333 Hz during fixation of a stationary target elicited smooth eye movements with a short latency (approximately 26 ms). The size of the elicited smooth eye movements was enhanced when the stimulation pulses were delivered during the maintenance of pursuit. The enhancement increased as a function of ongoing pursuit speed and was greater during pursuit in the same versus opposite direction of the eye movements evoked at a site. If stimulation was delivered during pursuit in eight different directions, the elicited eye velocity was fit best by a model incorporating two stimulation effects: a directional signal that drives eye velocity and an increase in the gain of ongoing pursuit eye speed in all directions. Separate experiments tested the effect of stimulation on the response to specific image motions. Stimulation consisted of a train of pulses at 100 or 200 Hz delivered during fixation so that only small smooth eye movements were elicited. If the stationary target was perturbed briefly during microstimulation, normally weak eye movement responses showed strong enhancement. If delivered at the initiation of pursuit, the same microstimulation caused enhancement of the presaccadic initiation of pursuit for steps of target velocity that moved the target either away from the position of fixation or in the direction of the eye movement caused by stimulation at the site. Stimulation in the FPA increased the latency of saccades to stationary or moving targets. Our results show that the FPA has two kinds of effects on the pursuit system. One drives smooth eye velocity in a fixed direction and is subject to on-line gain control by ongoing pursuit. The other causes enhancement of both the speed of ongoing pursuit and the responses to visual motion in a way that is not strongly selective for the direction of pursuit. Enhancement may operate either at a single site or at multiple sites. We conclude that the FPA plays an important role in on-line gain control for pursuit as well as possibly delivering commands for the direction and speed of smooth eye motion.

Oculocentric frames of reference for limb movement.

We have reviewed evidence that suggests that the target for limb motion is encoded in a retinocentric frame of reference. Errors in pointing that are elicited by an illusion that distorts the perceived motion of a target are strongly correlated with errors in gaze position. The modulations in the direction and speed of ocular smooth pursuit and of the hand show remarkable similarities, even though the inertia of the arm is much larger than that of the eye. We have suggested that ocular motion is constrained so that gaze provides an appropriate target signal for the hand. Finally, ocular and manual tracking deficits in patients with cerebellar ataxia are very similar. These deficits are also consistent with the idea that a gaze signal provides the target for hand motion; in some cases limb ataxia would be a consequence of optic ataxia rather than reflecting a deficit in the control of limb motion per se. These results, as well as neurophysiological data summarized here, have led us to revise a hypothesis we have previously put forth to account for the initial stages of sensorimotor transformations underlying targeted limb motions. In the original hypothesis, target location and initial arm posture were ultimately encoded in a common frame of reference tied to somatosensation, i.e. a body-centered frame of reference, and a desired change in posture was derived from the difference between the two. In our new scheme, a movement vector is derived from the difference between variables encoded in a retinocentric frame of reference. Accordingly, gaze, with its exquisite ability to stabilize a target image even under dynamic conditions, would be used as a reference signal. Consequently, this scheme would facilitate the processing of information under conditions in which the body and the target are moving relative to each other.

Pursuit affects precision of perceived heading for small viewing apertures

We investigated the interaction between extra-retinal rotation signals and retinal motion signals in heading perception during pursuit eye movement. For limited viewing aperture, the variability in perceived heading strongly depends on the pattern of motion directions. Heading towards a point outside the aperture generates nearly parallel aperture flow. This results in lower precision of perceived heading than heading that renders the radial pattern of flow visible. We ask if the precision is limited by the pattern of flow visible on the retina or that on the screen. During fixation, the two patterns are identical. They are decoupled during pursuit, since pursuit changes radial flow within the aperture on the screen into nearly parallel flow on the retina, and vice versa. The extra-retinal signal is known to reduce systematic errors in the direction of pursuit, thus compensating for the rotational flow during pursuit. We now ask if the extra-retinal signal also affects the precision of heading percepts. It might if at the spatial integration stage the rotational flow has been subtracted out already. A compensation beyond the integration stage, however, cannot undo the change in retinal motion directions so that an effect of pursuit on precision cannot be avoided. We measured the variable and systematic errors in perceived heading during fixation and pursuit for a frontal plane approach, while varying duration, dot lifetime and aperture size. We found precision is effected by pursuit as much as predicted from the pattern of retinal flow, while compensation is significantly greater than zero. This means that the interaction between the extra-retinal signal and visual motion signals takes place after spatial integration of local motion signals. Furthermore, compensation increased significantly with longer duration (0.5–3.0 s), but not with larger aperture size (10–50°). A larger aperture size did increase the eccentricity of perceived heading.

Smooth eye movements and spatial localisation

We asked subjects to align a target that flashed as their eyes rotated to the right in pursuit of a moving ring, with a target that flashed as their eyes rotated to the left in pursuit of the ring. Subjects systematically mislocalised the targets in the direction of pursuit. When the ring and flashes were the only structures that were visible, the alignment error was about 4 cm, corresponding to a timing error of about 100 ms. The timing error was independent of the position along the ring's path, but did depend to some extent on pursuit velocity. Adding a textured background reduced the mislocalisation considerably, presumably because it enabled subjects to localise the targets relative to the surrounding. There was almost no mislocalisation if the subject was not pursuing the ring. It is suggested that the mislocalisation arises because incoming retinal signals are combined directly with outgoing oculo-motor commands, with no attempt to account for any of the involved neuronal and muscular delays.

Distortion of Visual Space During Pursuit Eye Movements

We measured perceived positions of flash stimuli arranged two-dimensionally in the peripheral visual field during pursuit eye movement to examine the influence of displacement of the eye position on localization in the peripheral visual field. The horizontal mislocalization of the flash stimulus during the horizontal pursuit eye movement was found toward the pursuit direction. The magnitude of this mislocalization was asymmetrical around the central visual field, and the asymmetry depended on the pursuit direction. As the eye position changed, the magnitude of the horizontal mislocalization gradually decreased. It was also observed that the vertical mislocalization of the flash stimulus was constant regardless of the eye position displacement. These results show that the visual space during the horizontal pursuit eye movement is expanded horizontally and then gradually returns to the normal state. It is suggested that the visual space is dynamically distorted during the pursuit eye movement.

Shift in smooth pursuit initiation and MT and MST neuronal activity under different stimulus conditions.

The activity of neurons in extrastriate middle temporal (MT) and medial superior temporal (MST) areas were studied during the initiation of pursuit eye movements in macaque monkeys. The intersecting motion of two stimuli was used to test hypotheses about how these direction- and speed-sensitive neurons contribute to the generation of pursuit. The amplitude and direction of the initial saccade to the target and the initial speed and direction of pursuit were best predicted by a vector-average model of the underlying neuronal activity with relatively short time and spatial separation before a visual pursuit target and a distracter stimulus crossed in the visual field. The resulting eye movements were best described by a winner-take-all model when the time and spatial separation between the two stimuli was increased before the stimuli crossed. Neurons in MT and MST also shifted their activity from that best described by a vector average to a winner-take-all model under the same stimulus conditions. The changes in activity of neurons in both areas were generally similar to each other during these changes in pursuit initiation. Thus a slight alteration in the target motion produced a concurrent shift in both the neuronal processing and the movement execution. We propose that the differences in the oculomotor behavior can be accounted for by shifts in the overlap of active neuronal populations within MT and MST.

Fast and robust fixed-point algorithms for independent component analysis

Independent component analysis (ICA) is a statistical method for transforming an observed multidimensional random vector into components that are statistically as independent from each other as possible. In this paper, we use a combination of two different approaches for linear ICA: Comon's information-theoretic approach and the projection pursuit approach. Using maximum entropy approximations of differential entropy, we introduce a family of new contrast (objective) functions for ICA. These contrast functions enable both the estimation of the whole decomposition by minimizing mutual information, and estimation of individual independent components as projection pursuit directions. The statistical properties of the estimators based on such contrast functions are analyzed under the assumption of the linear mixture model, and it is shown how to choose contrast functions that are robust and/or of minimum variance. Finally, we introduce simple fixed-point algorithms for practical optimization of the contrast functions. These algorithms optimize the contrast functions very fast and reliably.

Oculomotor tracking in two dimensions.

Results from studies of oculomotor tracking in one dimension have indicated that saccades are driven primarily by errors in position, whereas smooth pursuit movements are driven primarily by errors in velocity. To test whether this result generalizes to two-dimensional tracking, we asked subjects to track a target that moved initially in a straight line then changed direction. We found that the general premise does indeed hold true; however, the study of oculomotor tracking in two dimensions provides additional insight. The first saccade was directed slightly in advance of target location at saccade onset. Thus its direction was related primarily to angular positional error. The direction of the smooth pursuit movement after the saccade was related linearly to the direction of target motion with an average slope of 0.8. Furthermore the magnitude and direction of smooth pursuit velocity did not change abruptly; consequently the direction of smooth pursuit appeared to rotate smoothly over time.

Human smooth pursuit direction discrimination.

The smooth pursuit system is usually studied using single moving objects as stimuli. However, the visual motion system can respond to stimuli that must be integrated spatially and temporally (Williams DG, Sekuler R. Vision Res 1984;24:55-62; Watamaniuk SNJ, Sekuler R, Williams DW. Vision Res 1989;29:47-59). For example, when each dot of a random-dot cinematogram (RDC) is assigned a new direction of motion each frame from a narrow distribution of directions, the whole field of dots appears to move in the average direction (Williams and Sekuler, 1984). We measured smooth pursuit eye movements generated in response to small (10 deg diameter) RDCs composed of 250 dynamic random dots. Smooth eye movements were assessed by analyzing only the first 130 ms of eye movements after pursuit initiation (open-loop period). Comparing smooth eye movements to RDCs and single spot targets, we find that both targets generate similar responses confirming that the signal supplied to the smooth pursuit system can result from a spatial integration of motion information. In addition, the change in directional precision of smooth eye movements to RDCs with different amounts of directional noise was similar to that found for psychophysical direction discrimination. These results imply that the motion processing system responsible for psychophysical performance may also provide input to the oculomotor system.

Neuronal Responses Related to Smooth Pursuit Eye Movements in the Periarcuate Cortical Area of Monkeys

To examine how the periarcuate area is involved in the control of smooth pursuit eye movements, we recorded 177 single neurons while monkeys pursued a moving target in the dark. The majority (52%, 92/177) of task-related neurons responded to pursuit but had little or no response to saccades. Histological reconstructions showed that these neurons were located mainly in the posterior bank of the arcuate sulcus near the sulcal spur. Twenty-seven percent (48/177) changed their activity at the onset of saccades. Of these, 36 (75%) showed presaccadic burst activity with strong preference for contraversive saccades. Eighteen (10%, 18/177) were classified as eye-position-related neurons, and 11% (19/177) were related to other aspects of the stimuli or response. Among the 92 neurons that responded to pursuit, 85 (92%) were strongly directional with uniformly distributed preferred directions. Further analyses were performed in these directionally sensitive pursuit-related neurons. For 59 neurons that showed distinct changes in activity around the initiation of pursuit, the median latency from target motion was 96 ms and that preceding pursuit was -12 ms, indicating that these neuron can influence the initiation of pursuit. We tested some neurons by briefly extinguishing the tracking target (n = 39) or controlling its movement with the eye position signal (n = 24). The distribution of the change in pursuit-related activity was similar to previous data for the dorsomedial part of the medial superior temporal neurons (, indicating that pursuit-related neurons in the periarcuate area also carry extraretinal signals. For 22 neurons, we examined the responses when the animals reversed pursuit direction to distinguish the effects of eye acceleration in the preferred direction from oppositely directed eye velocity. Almost all neurons discharged before eye velocity reached zero, however, only nine neurons discharged before the eyes were accelerated in the preferred direction. The delay in neuronal responses relative to the onset of eye acceleration in these trials might be caused by suppression from oppositely directed pursuit velocity. The results suggest that the periarcuate neurons do not participate in the earliest stage of eye acceleration during the change in pursuit direction, although most of them may participate in the early stages of pursuit initiation in the ordinary step-ramp pursuit trials. Some neurons changed their activity when the animals fixated a stationary target, and this activity could be distinguished easily from the strong pursuit-related responses. Our results suggest that the periarcuate pursuit area carries extraretinal signals and affects the premotor circuitry for smooth pursuit.

Latency of saccades during smooth-pursuit eye movement in man. Directional asymmetries.

To examine the effects of smooth-pursuit eye movements on the initiation of saccades, their latency was measured when subjects initially fixated or pursued a target. In half of the block of trials, the fixation or pursuit target was extinguished 200 ms before the saccade target was illuminated (gap trials). Reduction of the mean saccade latency in the gap trials (the "gap effect") was evident even when the subjects were pursuing a moving target, consistent with previous observations. The effect of pursuit direction on saccade latency was also examined. Saccades in the same direction as the preceding pursuit (forward saccades) had shorter latencies than those in the opposite direction (backward saccades). This asymmetry was observed in both the gap and nongap trials. Although the forward-backward asymmetry was much smaller than the "gap effect", it was statistically significant in six of eight cases. These results suggest that the preparation of saccades is affected by smooth-pursuit eye movements.

Encoding of Smooth Pursuit Direction and Eye Position by Neurons of Area MSTd of Macaque Monkey

The spike activity of neurons was recorded from the dorsal bank of the superior temporal sulcus (area MSTd) of alert behaving macaque monkeys performing visual fixation or target tracking tasks, with the aim of studying the tuning features of these neurons with both the direction of slow eye movement and the position of gaze. One hundred thirty-two neurons were tested for several fixation points and tracking directions. Many of them (43%) tuned to the direction of pursuit, regardless of the angle of gaze. Some (18%) showed a tonic discharge modulated by the static position of the eyes without pursuit direction specificity. A substantial number of cells (22%) were characterized by a discharge rate tuned to pursuit direction but influenced also by angle of gaze. Tuning curves for eye movement direction presented an average bandwidth of 130 degrees and turned out to be continuously overlapping, suggesting a sort of vector coding of smooth pursuit direction. Gaze fields of eye position (EP) neurons were mostly ramp-like, with center of ramps shifted away from the straight ahead, implying a form of scalar coding of gaze eccentricity. The different categories of cells were intermingled and close to each other, suggesting possible reciprocal interactions within the same cortical area. These results show that EP and pursuit direction are signaled mainly by separate neuronal elements in area MSTd. Moreover, some cells can integrate both signals. Taking into account the visual responses of MSTd neurons to large, textured, moving fields, it is suggested that this area could be the site of interaction between visuo-oculomotor signals related to visual motion detection, slow eye movement direction, and EP. This signal interaction may be important for integrative functions such as analysis of external or self-induced visual motion, cortical control of pursuit eye movements, and eye/head coordination.

Transitions between pursuit eye movements and fixation in the monkey: dependence on context.

1. We compared the visuomotor processing underlying the onset and offset of pursuit by recording the eye movements of three monkeys as they smoothly tracked a target that was initially at rest, started to move suddenly at a constant velocity along the horizontal meridian, and then stopped. We presented this sequence of target motions in two different contexts. In the first context the target sometimes stopped after 500 ms, but on other interleaved trials the target either continued moving at a constant velocity, slowed down, speeded up, or reversed direction. In the second context the target always stopped, but the duration of the preceding constant velocity was randomized from 500 to 700 ms. 2. The dynamics of the eye velocity during the offset of pursuit were markedly different in the two experiments. When the target stopped only sometimes, the decrease in eye velocity at the offset of pursuit often overshot zero, producing a brief, small reversal in the direction of pursuit before eye speed settled to zero. When the target always stopped, the decrease in eye velocity at the offset of pursuit followed a more gradual transition toward zero with no overshoot. Thus the eye velocity profiles obtained in the first experiment contradict, whereas those obtained in the second experiment confirm, previous characterizations of the offset of pursuit as an exponential decay toward zero eye speed. 3. To investigate the basis of the different eye velocity profiles obtained in the two experiments, we probed the state of transmission along the visuomotor pathways for pursuit with the use of small perturbations in the motion of the target. We used perturbations consisting of 1 degree step changes in target position superimposed on the constant velocity motion of the target, on the basis of previous findings that such perturbations elicit saccades during fixation but smooth changes in eye speed during maintained pursuit. Single perturbations were imposed at regularly spaced intervals on separate interleaved trials during the onset, maintenance, and offset of pursuit. 4. Perturbations imposed during the onset and maintenance of pursuit had similar effects regardless of whether the target stopped only sometimes or always. In both experiments, perturbations that stepped the target in the direction opposite to the constant velocity of the target produced decreases in eye speed; perturbations in the same direction produced negligible or inconsistent changes in eye speed. The changes in eye speed caused by perturbations were largest for those perturbations introduced within the first 100 ms after the start of target motion, before the onset of the smooth eye movement, and became progressively smaller as target motion continued. The largest changes in eye speed were therefore caused by those perturbations imposed during periods of large retinal slip and by those perturbations whose direction opposed that slip. 5. Perturbations imposed during the offset of pursuit had different effects depending on whether the target stopped only sometimes or always. When the target stopped only sometimes, forward perturbations produced large increases in eye speed, whereas backward perturbations produced negligible or inconsistent changes in eye speed. Thus the visuomotor processing underlying the offset of pursuit in this experiment strongly resembled that underlying the onset of pursuit: in both cases, those perturbations in the direction opposing large retinal slip produced the largest effects. In contrast, when the target always stopped, neither forward nor backward perturbations imposed during the offset of pursuit produced large changes in eye speed. This indicates that the visuomotor processing underlying the offset of pursuit in this experiment was different from the processing underlying the onset of pursuit. 6. Perturbations also produced changes in the frequency of saccades, although these effects were less consistent than the changes in pursuit eye speed

Participation of the caudal fastigial nucleus in smooth-pursuit eye movements. I. Neuronal activity.

1. We recorded single-unit activity from neurons of an output of the cerebellum, the fastigial nucleus, in two rhesus macaques while the monkeys tracked small moving targets with their eyes. Many neurons in the caudal part of the fastigial nucleus exhibited a modulation in their discharge rates when smooth-pursuit eye movements were elicited by either sinusoidal or step-ramp motions of a small target. 2. The pursuit direction that elicited the most vigorous modulation in unit firing to sinusoidal target motion could be horizontal, vertical, or oblique. Most often, the preferred direction was in the contralateral and/or downward direction (50 of 69 neurons) or in the ipsilateral and/or upward direction (13 of 69). 3. For units whose preferred smooth-pursuit directions were either contralateral/downward or ipsilateral/upward during sinusoidal pursuit, peak firing as measured by the phase shift of periodic modulation at 0.5-0.8 Hz occurred near the time of peak velocity. The discharge of 80% of the neurons with contralateral/downward preferred directions preceded eye velocity by an average of -27 degrees; thus these neurons discharged maximally during eye acceleration. In contrast, neurons with ipsilateral/upward preferred directions lagged peak velocity by an average of +10.5 degrees and therefore discharged during eye deceleration. 4. The average eye velocity sensitivity for sinusoidal pursuit between 0.5 and 0.8 Hz was 0.83 +/- 0.57 (SD) spikes/s per degrees/s. We also tested 36 units during pursuit at a variety of frequencies in their preferred directions and found that firing rates increased monotonically with peak eye velocity. However, the firing rate saturated at velocities ranging from 20 to 60 degrees/s for different units. 5. When a monkey tracked a step-ramp target motion, three discharge patterns emerged in the 27 units tested. Just over half of the units discharged a burst of spikes that preceded (average lead of 27.4 +/- 17 ms) and lasted throughout the initial third of the eye acceleration; the burst was followed by a subsequent steady firing that continued after the eye had accelerated to its steady velocity. Fewer neurons discharged a burst that began late in the acceleration and was followed by steady firing. Occasional neurons showed only a gradual increase in firing rate during acceleration followed by a steady discharge. 6. Thirty of the 31 fastigial smooth-pursuit units tested also were modulated during sinusoidal yaw and/or pitch oscillations while the animals fixated a spot that rotated with them.(ABSTRACT TRUNCATED AT 400 WORDS)