Initial Eye Acceleration Research Articles

Properties of smooth pursuit and visual motion reaction time to second-order motion stimuli.

A large number of psychophysical and neurophysiological studies have demonstrated that smooth pursuit eye movements are tightly related to visual motion perception. This could be due to the fact that visual motion sensitive cortical areas such as meddle temporal (MT), medial superior temporal (MST) areas are involved in motion perception as well as pursuit initiation. Although the directional-discrimination and perceived target velocity tasks are used to evaluate visual motion perception, it is still uncertain whether the speed of visual motion perception, which is determined by visuomotor reaction time (RT) to a small target, is related to pursuit initiation. Therefore, we attempted to determine the relationship between pursuit latency/acceleration and the visual motion RT which was measured to the visual motion stimuli that moved leftward or rightward. The participants were instructed to fixate on a stationary target and press one of the buttons corresponding to the direction of target motion as soon as possible once the target starts to move. We applied five different visual motion stimuli including first- and second-order motion for smooth pursuit and visual motion RT tasks. It is well known that second-order motion induces lower retinal image motion, which elicits weaker responses in MT and MST compared to first-order motion stimuli. Our results showed that pursuit initiation including latency and initial eye acceleration were suppressed by second-order motion. In addition, second-order motion caused a delay in visual motion RT. The better performances in both pursuit initiation and visual motion RT were observed for first-order motion, whereas second-order (theta motion) induced remarkable deficits in both variables. Furthermore, significant Pearson’s correlation and within-subjects correlation coefficients were obtained between visual motion RT and pursuit latency/acceleration. Our findings support the suggestion that there is a common neuronal pathway involved in both pursuit initiation and the speed of visual motion perception.

Smooth pursuit eye movement deficits as a biomarker for psychotic features in bipolar disorder-Findings from the PARDIP study.

Smooth pursuit eye movement deficits are an established psychosis biomarker across schizophrenia, schizoaffective and psychotic bipolar disorder (BPwP). Whether smooth pursuit deficits are also seen in bipolar disorder without psychosis (BPwoP) is unclear. Here we present data from the Psychosis and Affective Research Domains and Intermediate Phenotypes (PARDIP) study comparing bipolar patients with and without psychotic features. Probands with BPwP (N=49) and BPwoP (N=36), and healthy controls (HC, N=71) performed eye tracking tasks designed to evaluate specific sensorimotor components relevant for pursuit initiation and pursuit maintenance. While BPwoP did not differ from either BPwP or HC on initial eye acceleration, they performed significantly better than BPwP on early (P<.01) and predictive (P=.02) pursuit maintenance measures, both without differing from HC. BPwP were impaired compared to HC on initial eye acceleration, and on early and predictive pursuit maintenance (all P<.01). In contrast to the three pursuit measures, BPwP and BPwoP were both impaired on general neurocognitive assessments in relation to HC (both P<.001), without a significant difference between the two bipolar patient groups. Our findings support the model that impairments of sensorimotor and cognitive processing as required for early and later predictive smooth pursuit maintenance are relatively specific to those bipolar patients with a history of psychosis. This suggests that the neural circuitry for developing feed-forward predictive models for accurate pursuit maintenance is associated with the occurrence of psychotic features in bipolar patients. In contrast, generalized neuropsychological impairments did not differentiate the two bipolar patient groups.

Visual and non-visual motion information processing during pursuit eye tracking in schizophrenia and bipolar disorder.

Despite many reports on visual processing deficits in psychotic disorders, studies are needed on the integration of visual and non-visual components of eye movement control to improve the understanding of sensorimotor information processing in these disorders. Non-visual inputs to eye movement control include prediction of future target velocity from extrapolation of past visual target movement and anticipation of future target movements. It is unclear whether non-visual input is impaired in patients with schizophrenia. We recorded smooth pursuit eye movements in 21 patients with schizophrenia spectrum disorder, 22 patients with bipolar disorder, and 24 controls. In a foveo-fugal ramp task, the target was either continuously visible or was blanked during movement. We determined peak gain (measuring overall performance), initial eye acceleration (measuring visually driven pursuit), deceleration after target extinction (measuring prediction), eye velocity drifts before onset of target visibility (measuring anticipation), and residual gain during blanking intervals (measuring anticipation and prediction). In both patient groups, initial eye acceleration was decreased and the ability to adjust eye acceleration to increasing target acceleration was impaired. In contrast, neither deceleration nor eye drift velocity was reduced in patients, implying unimpaired non-visual contributions to pursuit drive. Disturbances of eye movement control in psychotic disorders appear to be a consequence of deficits in sensorimotor transformation rather than a pure failure in adding cognitive contributions to pursuit drive in higher-order cortical circuits. More generally, this deficit might reflect a fundamental imbalance between processing external input and acting according to internal preferences.

Pursuit eye movements as an intermediate phenotype across psychotic disorders: Evidence from the B-SNIP study

Smooth pursuit eye tracking deficits are a promising intermediate phenotype for schizophrenia and possibly for psychotic disorders more broadly. The Bipolar-Schizophrenia Network on Intermediate Phenotypes (B-SNIP) consortium investigated the severity and familiality of different pursuit parameters across psychotic disorders. Probands with schizophrenia (N=265), schizoaffective disorder (N=178), psychotic bipolar disorder (N=231), their first-degree relatives (N=306, N=217, N=273, respectively) and healthy controls (N=305) performed pursuit tracking tasks designed to evaluate sensorimotor and cognitive/predictive aspects of pursuit. Probands from all diagnostic groups were impaired on all pursuit measures of interest compared to controls (p<0.001). Schizophrenia probands were more impaired than other proband groups on both early pursuit gain and predictive gain. Relatives with and without enhanced psychosis spectrum personality traits were impaired on initial eye acceleration, the most direct sensorimotor pursuit measure, but not on pursuit gain measures. This suggests that alterations in early sensorimotor function may track susceptibility to psychosis even in the absence of psychosis related personality traits. There were no differences in pursuit measures between relatives of the three proband groups. Familiality estimates of pursuit deficits indicate that early pursuit gain was more familial than predictive gain, which has been the most widely used measure in previous family studies of psychotic disorders. Thus, while disease-related factors may induce significant impairments of pursuit gain, especially in schizophrenia, the pattern of deficits in relatives and their familiality estimates suggest that alterations in sensorimotor function at pursuit onset may indicate increased susceptibility across psychotic disorders.

Cue-dependent memory-based smooth-pursuit in normal human subjects: importance of extra-retinal mechanisms for initial pursuit

Using a cue-dependent memory-based smooth-pursuit task previously applied to monkeys, we examined the effects of visual motion-memory on smooth-pursuit eye movements in normal human subjects and compared the results with those of the trained monkeys. These results were also compared with those during simple ramp-pursuit that did not require visual motion-memory. During memory-based pursuit, all subjects exhibited virtually no errors in either pursuit-direction or go/no-go selection. Tracking eye movements of humans and monkeys were similar in the two tasks, but tracking eye movements were different between the two tasks; latencies of the pursuit and corrective saccades were prolonged, initial pursuit eye velocity and acceleration were lower, peak velocities were lower, and time to reach peak velocities lengthened during memory-based pursuit. These characteristics were similar to anticipatory pursuit initiated by extra-retinal components during the initial extinction task of Barnes and Collins (J Neurophysiol 100:1135-1146, 2008b). We suggest that the differences between the two tasks reflect differences between the contribution of extra-retinal and retinal components. This interpretation is supported by two further studies: (1) during popping out of the correct spot to enhance retinal image-motion inputs during memory-based pursuit, pursuit eye velocities approached those during simple ramp-pursuit, and (2) during initial blanking of spot motion during memory-based pursuit, pursuit components appeared in the correct direction. Our results showed the importance of extra-retinal mechanisms for initial pursuit during memory-based pursuit, which include priming effects and extra-retinal drive components. Comparison with monkey studies on neuronal responses and model analysis suggested possible pathways for the extra-retinal mechanisms.

Visual Error Signals From the Pretectal Nucleus of the Optic Tract Guide Motor Learning for Smooth Pursuit

Smooth pursuit (SP) eye movements are used to maintain the image of a moving object on or near the fovea. Visual motion signals aid in driving SP and are necessary for its adaptation. The sources of visual error signals that support SP adaptation are incompletely understood but could involve neurons in cortical and brain stem areas with direction selective visual motion responses. Here we focus on the pretectal nucleus of the optic tract (NOT), which encodes retinal error information during SP. The aim of this study was to characterize the role of the NOT in SP adaptation. SP adaptation is typically produced using a double step of velocity ramp (double-step paradigm), where target speed either increases or decreases 100 ms after the beginning of a trial. In our study, we delivered a brief (200 ms) train of microelectrical stimulation (ES) in the left NOT to introduce directional error signals at the point in time where a second target speed would appear in a double-step paradigm. The target was extinguished coincidentally with the onset of the ES train. Initial eye acceleration (1st 100 ms) showed significant increases after 100 trials, which included left NOT stimulation during ongoing pursuit in an ipsiversive (leftward) direction. In contrast, initial eye acceleration showed significant decreases after repeated left NOT stimulation during contraversive (rightward) SP. Control studies performed using the same periodicity of NOT stimulation as in the preceding text but without accompanying SP did not induce changes in eye acceleration. In contrast, ES of the NOT paired with active SP produced gradual changes in eye acceleration similar to that observed in double-step paradigm. Therefore our findings support the suggestion that the NOT is an important source of visual error information for guiding motor learning during horizontal SP.

Lesions of the Cerebellar Nodulus and Uvula Impair Downward Pursuit

We studied sinusoidal (SIN) and step-ramp (SR) pursuit in two rhesus monkeys, before and after surgical lesions of the cerebellar nodulus and uvula (Nod/Uv). Eye movements were recorded using the magnetic field scleral search coil method. Pursuit targets were generated by an LCD projector and back-projected onto a tangent screen in an otherwise dark room. After the Nod/Uv lesions, both monkeys showed a reduced eye velocity during downward pursuit (SIN: 42% decrease in M1, 91% decrease in M2; SR: 37% decrease in M1, 85% decrease in M2). For SR, the decrease was seen only for the closed-loop response; initial eye acceleration did not change (P>0.05). Upward pursuit gains increased for SIN (M1: 9%, M2: 11%); they decreased for SR (M1: 27%, M2: 18%), but to a lesser degree than for downward pursuit. Horizontal pursuit was little changed in M1 but was reduced in one direction in M2, the animal with the larger lesion. The deficit in downward tracking was limited to foveal pursuit; ocular following of random-dot stimuli was retained, even when the target subtended only several degrees. Our findings support a critical role for the Nod/Uv in vertical pursuit, particularly for sustained downward pursuit. Finally, in both monkeys, the lesion increased spontaneous upward ocular drift in the dark (mean prelesion, 1.43 degrees/s; postlesion, 5.92 degrees/s), suggesting a role for the Nod/Uv in holding the eyes still and in the genesis of downbeat nystagmus.

Horizontal Smooth Pursuit Adaptation in Macaques After Muscimol Inactivation of the Dorsolateral Pontine Nucleus (DLPN)

The smooth pursuit (SP) system can adapt its response to developmental changes, injury, and behavioral context. Previous lesion and single-unit recording studies show that the macaque cerebellum plays a role in SP initiation, maintenance, and adaptation. The aim of this study was to determine the potential role of the DLPN in SP adaptation. The DLPN receives inputs from the cortical SP system and delivers eye and visual motion information to the dorsal/ventral paraflocculus and vermis of the cerebellum. We studied SP adaptation in two juvenile rhesus monkeys (Macaca mulatta), using double steps of target speed that step- up (10-30 degrees/s) or step-down (25-5 degrees/s). We used microinjection of muscimol (<or=2%; 0.15 microl) to reversibly inactivate the DLPN, unilaterally. After DLPN inactivation, initial ipsilesional SP acceleration (first 100 ms) was significantly reduced by 47-74% (P < 0.01; unpaired t-test) of control values in the single-speed step-ramp paradigm. Similarly, ipsilesional steady-state SP velocity was also reduced by 59-78% (P < 0.01; unpaired t-test) of control values. Contralesional SP was not impaired after DLPN inactivation. Control testing showed significant adaptive changes of initial SP eye acceleration after 100 trials in either step-up or step-down paradigms. After inactivation, during ipsilesional SP, adaptation was impaired in the step-up but not in the step-down paradigm. In contrast, during contralesional tracking, adaptive capability remained in the step-down but not in the step-up paradigm. Therefore SP adaptation could depend, in part, on direction sensitive eye/visual motion information provided by DLPN neurons to cerebellum.

Involvement of the Cerebellar Dorsal Vermis in Vergence Eye Movements in Monkeys

Frontal-eyed primates use both smooth pursuit in frontoparallel planes (frontal pursuit) and pursuit-in-depth (vergence pursuit) to track objects moving slowly in 3-dimensional (3D) space. To understand how 3D-pursuit signals represented in frontal eye fields are processed further by downstream pathways, monkeys were trained to pursue a spot moving in 3D virtual space. We characterized pursuit signals in Purkinje (P) cells in the cerebellar dorsal vermis and their discharge during vergence pursuit. In 41% of pursuit P-cells, 3D-pursuit signals were observed. However, the majority of vermal-pursuit P-cells (59%) discharged either for vergence pursuit (43%) or for frontal pursuit (16%). Moreover, the majority (74%) of vergence-related P-cells carried convergence signals, displaying both vergence eye position and velocity sensitivity during sinusoidal and step vergence eye movements. Preferred frontal-pursuit directions of vergence + frontal-pursuit P-cells were distributed in all directions. Most pursuit P-cells (73%) discharged before the onset of vergence eye movements; the median lead time was 16 ms. Muscimol infusion into the sites where convergence P-cells were recorded resulted in a reduction of peak convergence eye velocity, of initial convergence eye acceleration, and of frontal-pursuit eye velocity. These results suggest involvement of the dorsal vermis in conversion of 3D-pursuit signals and in convergence eye movements.

Smooth pursuit deficits in schizophrenia, affective disorder and obsessive-compulsive disorder.

In schizophrenia, affective disorders, and obsessive-compulsive disorder (OCD) dysfunction of frontal neuronal circuits has been suggested. Such impairments imply corresponding oculomotor deficits. Eye movement response to foveofugal and foveopetal step-ramp stimuli was recorded within the same study design in patients with schizophrenia (N= 16), affective disorder (N= 15), and OCD (N= 18) and compared with controls (N=23) using infra-red reflection oculography. In the foveofugal task steady-state velocity was lower in all patient groups compared with controls. Post-saccadic eye velocity was also decreased in patients with schizophrenia and affective disorder. In the foveopetal stimulus steady-state velocity was reduced in schizophrenic patients, only. Changes of saccadic latencies or position errors were not found in any of the patient groups. Also, pursuit latency was unchanged and initial eye acceleration was not decreased. Unaltered saccadic parameters indicate intact motion perception in cortical visual area V5. Therefore, the observed deficit of pursuit maintenance implies a dysfunction of frontal networks in all patient groups including the pursuit region of the frontal eye field (FEF). In patients with schizophrenia and affective disorder reduced post-saccadic pursuit initiation may indicate an impaired interaction between the pursuit and the saccadic system.

Eye movement abnormalities in essential tremor may indicate cerebellar dysfunction.

Experimental and clinical data indicate that the cerebellum is involved in the pathophysiology of advanced stages of essential tremor (ET). The aim of this study was to determine whether a dysfunction also affects cerebellar structures involved in eye movement control. Eye movements of 14 patients with ET and 11 age-matched control subjects were recorded using the scleral search-coil technique. Vestibular function was assessed by electro-oculography. Eight ET patients had clinical evidence of intention tremor (ET(IT)); six had a predominantly postural tremor (ET(PT)) without intention tremor. ET patients showed two major deficits that may indicate cerebellar dysfunction: (i) an impaired smooth pursuit initiation; and (ii) pathological suppression of the vestibulo-ocular reflex (VOR) time constant by head tilts ('otolith dumping'). In the step ramp smooth pursuit paradigm, the initial eye acceleration in the first 60 ms of pursuit generation was significantly reduced in ET patients, particularly in ET(IT) patients, by approximately 44% (mean 23.4 degrees/s(2)) compared with that of control subjects (mean 41.3 degrees/s(2)). Subsequent steady-state pursuit velocity and sinusoidal pursuit gain (e.g. 0.4 Hz: 0.90 versus 0.78) were also significantly decreased in ET patients, whereas pursuit latency was unaffected. The intention tremor score correlated with the pursuit deficit, e.g. ET(IT) patients were significantly more affected than ET(PT) patients. Gain and time constant (tau) of horizontal VOR were normal, but suppression of the VOR time constant by head tilt ('otolith dumping') was pathological in 41% of ET patients, particularly in ET(IT) patients. Saccades and gaze-holding function were not impaired. The deficit of pursuit initiation, its correlation with the intensity of intention tremor, and the pathological VOR dumping provide additional evidence of a cerebellar dysfunction in the advanced stage of ET, when intention tremor becomes part of the clinical symptoms, and point to a common pathomechanism. The oculomotor deficits may indicate an impairment of the caudal vermis in ET.

Motor scaling by viewing distance of early visual motion signals during smooth pursuit.

The geometry of gaze stabilization during head translation requires eye movements to scale proportionally to the inverse of target distance. Such a scaling has indeed been demonstrated to exist for the translational vestibuloocular reflex (TVOR), as well as optic flow-selective translational visuomotor reflexes (e.g., ocular following, OFR). The similarities in this scaling by a neural estimate of target distance for both the TVOR and the OFR have been interpreted to suggest that the two reflexes share common premotor processing. Because the neural substrates of OFR are partly shared by those for the generation of pursuit eye movements, we wanted to know if the site of gain modulation for TVOR and OFR is also part of a major pathway for pursuit. Thus, in the present studies, we investigated in rhesus monkeys whether initial eye velocity and acceleration during the open-loop portion of step ramp pursuit scales with target distance. Specifically, with visual motion identical on the retina during tracking at different distances (12, 24, and 60 cm), we compared the first 80 ms of horizontal pursuit. We report that initial eye velocity and acceleration exhibits either no or a very small dependence on vergence angle that is at least an order of magnitude less than the corresponding dependence of the TVOR and OFR. The results suggest that the neural substrates for motor scaling by target distance remain largely distinct from the main pathway for pursuit.

Gaze-, eye-, and head-movement dynamics during closed- and open-loop gaze pursuit.

Horizontal step-ramp stimuli were used to examine gaze-, eye-, and head-movement dynamics during head-unrestrained pursuit in two rhesus monkeys. In a first series of experiments, we characterized and compared head-restrained (HR) and -unrestrained (HU) pursuit responses to unpredictable, nonperiodic, constant velocity (20-80 degrees/s) stimuli. When the head was free to move, both monkeys used a combination of eye and head motion to initially fixate and then pursue the target. The pursuit responses (i.e., gaze responses) were highly stereotyped and nearly identical among the HR and HU conditions for a given step-ramp stimulus. In the HU condition, initial eye and initial head acceleration tended to increase as a function of target velocity but did not vary systematically with initial target eccentricity. In a second series of experiments, step-ramp stimuli (40 degrees/s) were presented, and, approximately 125 ms after pursuit onset, a constant retinal velocity error (RVE) was imposed for a duration of 300 ms. In each monkey, HR and HU gaze velocity was similarly affected by stabilizing the target with respect to the monkey's fovea (i.e., RVE = 0 degrees/s) and by moving the target with constant retinal velocity errors (i.e., RVE = +/- 10 degrees/s). In the HU condition, changes in both eye and head velocity trajectories contributed to the observed gaze velocity responses to imposed RVEs. We conclude that eye and head movements are not independently controlled during HU pursuit but rather are controlled, at least in part, by a shared upstream controller within the pursuit pathways.

Apparent motion produces multiple deficits in visually guided smooth pursuit eye movements of monkeys.

We used apparent motion targets to explore how degraded visual motion alters smooth pursuit eye movements. Apparent motion targets consisted of brief stationary flashes with a spatial separation (Deltax), temporal separation (Deltat), and apparent target velocity equal to Deltax/Deltat. Changes in pursuit initiation were readily observed when holding target velocity constant and increasing the flash separation. As flash separation increased, the first deficit observed was an increase in the latency to peak eye acceleration. Also seen was a paradoxical increase in initial eye acceleration. Further increases in the flash separation produced larger increases in latency and resulted in decreased eye acceleration. By varying target velocity, we were able to discern that the visual inputs driving pursuit initiation show both temporal and spatial limits. For target velocities above 4-8 degrees /s, deficits in the initiation of pursuit were seen when Deltax exceeded 0.2-0.5 degrees, even when Deltat was small. For target velocities below 4-8 degrees /s, deficits appeared when Deltat exceeded 32-64 ms, even when Deltax was small. Further experiments were designed to determine whether the spatial limit varied as retinal and extra-retinal factors changed. Varying the initial retinal position of the target for motion at 18 degrees /s revealed that the spatial limit increased as a function of retinal eccentricity. We then employed targets that increased velocity twice, once from fixation and again during pursuit. These experiments revealed that, as expected, the spatial limit is expressed in terms of the flash separation on the retina. The spatial limit is uninfluenced by either eye velocity or the absolute velocity of the target. These experiments also demonstrate that "initiation" deficits can be observed during ongoing pursuit, and are thus not deficits in initiation per se. We conclude that such deficits result from degradation of the retino-centric motion signals that drive pursuit eye acceleration. For large flash separations, we also observed deficits in the maintenance of pursuit: sustained eye velocity failed to match the constant apparent target velocity. Deficits in the maintenance of pursuit depended on both target velocity and Deltat and did not result simply from a failure of degraded image motion signals to drive eye acceleration. We argue that such deficits result from a low gain in the eye velocity memory that normally supports the maintenance of pursuit. This low gain may appear because visual inputs are so degraded that the transition from fixation to tracking is incomplete.

Primate translational vestibuloocular reflexes. III. Effects of bilateral labyrinthine electrical stimulation.

The effects of functional, reversible ablation and potential recruitment of the most irregular otolith afferents on the dynamics and sensitivity of the translational vestibuloocular reflexes (trVORs) were investigated in rhesus monkeys trained to fixate near and far targets. Translational motion stimuli consisted of either steady-state lateral and fore-aft sinusoidal oscillations or short-lasting transient lateral head displacements. Short-duration (usually <2 s) anodal (inhibitory) and cathodal (excitatory) currents (50-100 microA) were delivered bilaterally during motion. In the presence of anodal labyrinthine stimulation, trVOR sensitivity and its dependence on viewing distance were significantly decreased. In addition, anodal currents significantly increased phase lags. During transient motion, anodal stimulation resulted in significantly lower initial eye acceleration and more sluggish responses. Cathodal currents tended to have opposite effects. The main characteristics of these results were simulated by a simple model where both regularly and irregularly discharging afferents contribute to the trVORs. Anodal labyrinthine currents also were found to decrease eye velocity during long-duration, constant velocity rotations, although results were generally more variable compared with those during translational motion.

Vector Averaging Occurs Downstream from Learning in Smooth Pursuit Eye Movements of Monkeys

How are sensory-motor transformations organized in a cortical motor system? In general, sensory information is transformed through a variety of signal processing operations in the context of distinct coordinate frameworks. We studied the interaction of two distinct operations in pursuit eye movements, learning and vector-averaging, to gain insight into their underlying coordinate frameworks and their sequence in sensory-motor processing. Learning was induced in the initiation of pursuit eye movements by targets that moved initially at one speed for 100 msec and then increased or decreased to a sustained final speed. Vector averaging was studied by comparing the initial eye acceleration evoked by the simultaneous motion of two targets with that evoked by each target singly. Learning caused specific effects on the direction of the vector-averaged responses to two-target stimuli that included one target moving in the direction used to induce learning. Learned increases or decreases in eye acceleration caused the direction of the responses to two-targets to rotate toward or away from the learning direction. Learning also caused nonspecific changes in the responses to two-target stimuli. After any learning protocol, two-target responses usually became smaller, and their directions rotated away from the axis of the target motion used for learning. Quantitative analysis showed that the specific effects of learning were predicted most closely by a model in which vector averaging occurs downstream from the site(s) of learning. We suggest that the pursuit system creates parallel commands for potential movements to each of the targets in two-target stimuli, and that learning occurs in the coordinates of the potential movements.

Eye movements of rhesus monkeys directed towards imaginary targets.

Is the presence of foveal stimulation a necessary prerequisite for rhesus monkeys to perform visually guided eye movements? To answer this question, we trained two rhesus monkeys to direct their eyes towards imaginary targets defined by extrafoveal cues. Independent of the type of target, real or imaginary, the trajectory of target movement determined the type of eye movement produced: steps in target position resulted in saccades and ramps in target position resulted in smooth pursuit eye movements. There was a tendency for the latency of saccades as well as pursuit onset latency to be delayed in the case of an imaginary target in comparison to the real target. The initial eye acceleration during smooth pursuit initiation elicited by an imaginary target decreased in comparison to the acceleration elicited by a real target. The steady-state pursuit gain was quite similar during pursuit of an imaginary or a real target. Our results strengthen the notion that pursuit is not exclusively a foveal function.

The effect of a moving distractor on the initiation of smooth-pursuit eye movements.

As a step toward understanding the mechanism by which targets are selected for smooth-pursuit eye movements, we examined the behavior of the pursuit system when monkeys were presented with two discrete moving visual targets. Two rhesus monkeys were trained to select a small moving target identified by its color in the presence of a moving distractor of another color. Smooth-pursuit eye movements were quantified in terms of the latency of the eye movement and the initial eye acceleration profile. We have previously shown that the latency of smooth pursuit, which is normally around 100 ms, can be extended to 150 ms or shortened to 85 ms depending on whether there is a distractor moving in the opposite or same direction, respectively, relative to the direction of the target. We have now measured this effect for a 360 deg range of distractor directions, and distractor speeds of 5-45 deg/s. We have also examined the effect of varying the spatial separation and temporal asynchrony between target and distractor. The results indicate that the effect of the distractor on the latency of pursuit depends on its direction of motion, and its spatial and temporal proximity to the target, but depends very little on the speed of the distractor. Furthermore, under the conditions of these experiments, the direction of the eye movement that is emitted in response to two competing moving stimuli is not a vectorial combination of the stimulus motions, but is solely determined by the direction of the target. The results are consistent with a competitive model for smooth-pursuit target selection and suggest that the competition takes place at a stage of the pursuit pathway that is between visual-motion processing and motor-response preparation.

Activity of neurons in monkey superior colliculus during interrupted saccades.

1. Recent studies of the monkey superior colliculus (SC) have identified several types of cells in the intermediate layers (including burst, buildup, and fixation neurons) and the sequence of changes in their activity during the generation of saccadic eye movements. On the basis of these observations, several hypotheses about the organization of the SC leading to saccade generation have placed the SC in a feedback loop controlling the amplitude and direction of the impending saccade. We tested these hypotheses about the organization of the SC by perturbing the system while recording the activity of neurons within the SC. 2. We applied a brief high-frequency train of electrical stimulation among the fixation cells in the rostral pole of the SC. This momentarily interrupted the saccade in midflight: after the initial eye acceleration, the eye velocity decreased (frequently to 0) and then again accelerated. Despite the break in the saccade, these interrupted saccades were of about the same amplitude as normal saccades. The postinterruption saccades were usually initiated immediately after the termination of stimulation and occurred regardless of whether the saccade target was visible or not. The velocity-amplitude relationship of the preinterruption component of the saccade fell slightly above the main sequence for control saccades of that amplitude, whereas postinterruption saccades fell near the main sequence. 3. Collicular burst neurons are silent during fixation and discharge a robust burst of action potentials for saccades to a restricted region of the visual field that define a closed movement field. During the stimulation-induced saccadic interruption, these burst neurons all showed a pause in their high-frequency discharge. During an interrupted saccade to a visual target, the typical saccade-related burst was broken into two parts: the first part of the burst began before the initial preinterruption saccade; the second burst began before the postinterruption saccade. 4. We quantified three aspects of the resumption of activity of burst neurons following saccade interruption: 1) the total number of spikes in the pre- and postinterruption bursts, was very similar to the total number of spikes in the control saccade burst; 2) the increase in total duration of the burst (preinterruption period + interruption + postinterruption period) was highly correlated with the increase in total saccade duration (preinterruption saccade + interruption + postinterruption saccade); and 3) the time course of the postinterruption saccade and the resumed cell discharge both followed the same monotonic trajectory as the control saccade in most cells. 5. The same population of burst neurons was active for both the preinterruption and the postinterruption saccades, provided that the stimulation was brief enough to allow the postinterruption saccade to occur immediately. If the postinterruption saccade was delayed by > 100 ms, then burst neurons at a new and more rostral locus related to such smaller saccades became active in association with the smaller remaining saccade. We interpret this shift in active locations within the SC as a termination of the initial saccadic error command and the triggering of a new one. 6. Buildup neurons usually had two aspects to their discharge: a high-frequency burst for saccades of the optimal amplitude and direction (similar to burst neurons), and a low-frequency discharge for saccades of optimal direction whose amplitudes were equal to or greater than the optimal (different from burst neurons). The stimulation-induced interruption in saccade trajectory differentially affected these two components of buildup neuron discharge. The high-frequency burst component was affected in a manner very similar to the burst neurons.(ABSTRACT TRUNCATED)

The influence of structured visual backgrounds on smooth-pursuit initiation, steady-state pursuit and smooth-pursuit termination.

Smooth-pursuit eye movements were recorded in two rhesus monkeys in order to compare the influence of structured visual backgrounds on smooth-pursuit initiation, steady-state pursuit and pursuit termination. Different target trajectories were used in order to study smooth-pursuit initiation and termination. The influence of visual backgrounds on pursuit initiation was characterized by recording ocular responses elicited by step-ramp target displacements starting from straight ahead. Pursuit termination was characterized by analysing the transition from steady-state smooth-pursuit to fixation when a centripetally directed target ramp was terminated by a small target step in the direction of the ramp as soon as the target had come close to the straightahead position. The quantification of steady-state pursuit was based on ocular responses elicited by either paradigm. In accordance with previous work, we found that the onset of smooth-pursuit eye movements was delayed and initial eye acceleration reduced in the presence of a structured visual background. Likewise, mean eye velocity during steady-state pursuit was reduced by structured visual backgrounds. However, neither the latency nor the time course of smooth-pursuit termination was altered when the homogeneous background was replaced by a structured visual background. The lack of sensitivity of pursuit termination to the presence of visual structured backgrounds supports a previous contention that pursuit termination is mediated by a process which is different from the ones mediating smooth-pursuit initiation and steady-state pursuit. The absence of any noticeable effect of structured backgrounds on pursuit termination suggests that at least the fast component of the optokinetic reflex is suppressed during pursuit termination.