A quantitative synchronization model for smooth pursuit target tracking

We propose a quantitative model for human smooth pursuit tracking of a continuously moving visual target which is based on synchronization of an internal expectancy model of the target position coupled to the retinal target signal. The model predictions are tested in a smooth circular pursuit eye tracking experiment with transient target blanking of variable duration. In subjects with a high tracking accuracy, the model accounts for smooth pursuit and repeatedly reproduces quantitatively characteristic patterns of the eye dynamics during target blanking. In its simplest form, the model has only one free parameter, a coupling constant. An extended model with a second parameter, a time delay or memory term, accounts for predictive smooth pursuit eye movements which advance the target. The model constitutes an example of synchronization of a complex biological system with perceived sensory signals. Cognitive and Neurobiological Research Consortium in Traumatic Brain Injury (CNRC-TBI).     

Effects of Attention to Auditory Motion on Cortical Activations during Smooth Pursuit Eye Tracking

Background

In contrast to traditional views that consider smooth pursuit as a relatively automatic process, evidence has been reported for the importance of attention for accurate pursuit performance. However, the exact role that attention might play in the maintenance of pursuit remains unclear.

Methodology/Principal Findings

We analysed the neuronal activity associated with healthy subjects executing smooth pursuit eye movements (SPEM) during concurrent attentive tracking of a moving sound source, which was either in-phase or in antiphase to the executed eye movements. Assuming that attentional resources must be allocated to the moving sound source, the simultaneous execution of SPEM and auditory tracking in diverging directions should result in increased load on common attentional resources. By using an auditory stimulus as a distractor rather then a visual stimulus we guaranteed that cortical activity cannot be caused by conflicts between two simultaneous visual motion stimuli. Our results revealed that the smooth pursuit task with divided attention led to significantly higher activations bilaterally in the posterior parietal cortex and lateral and medial frontal cortex, presumably containing the parietal, frontal and supplementary eye fields respectively.

Conclusions

The additional cortical activation in these areas is apparently due to the process of dividing attention between the execution of SPEM and the covert tracking of the auditory target. On the other hand, even though attention had to be divided the attentional resources did not seem to be exhausted, since the identification of the direction of the auditory target and the quality of SPEM were unaffected by the congruence between visual and auditory motion stimuli. Finally, we found that this form of task-related attention modulated not only the cortical pursuit network in general but also affected modality specific and supramodal attention regions.     

Memory and prediction in natural gaze control

In addition to stimulus properties and task factors, memory is an important determinant of the allocation of attention and gaze in the natural world. One way that the role of memory is revealed is by predictive eye movements. Both smooth pursuit and saccadic eye movements demonstrate predictive effects based on previous experience. We have previously shown that unskilled subjects make highly accurate predictive saccades to the anticipated location of a ball prior to a bounce in a virtual racquetball setting. In this experiment, we examined this predictive behaviour. We asked whether the period after the bounce provides subjects with visual information about the ball trajectory that is used to programme the pursuit movement initiated when the ball passes through the fixation point. We occluded a 100 ms period of the ball''s trajectory immediately after the bounce, and found very little effect on the subsequent pursuit movement. Subjects did not appear to modify their strategy to prolong the fixation. Neither were we able to find an effect on interception performance. Thus, it is possible that the occluded trajectory information is not critical for subsequent pursuit, and subjects may use an estimate of the ball''s trajectory to programme pursuit. These results provide further support for the role of memory in eye movements.     

Tuning Properties of MT and MSTd and Divisive Interactions for Eye-Movement Compensation

The primate brain intelligently processes visual information from the world as the eyes move constantly. The brain must take into account visual motion induced by eye movements, so that visual information about the outside world can be recovered. Certain neurons in the dorsal part of monkey medial superior temporal area (MSTd) play an important role in integrating information about eye movements and visual motion. When a monkey tracks a moving target with its eyes, these neurons respond to visual motion as well as to smooth pursuit eye movements. Furthermore, the responses of some MSTd neurons to the motion of objects in the world are very similar during pursuit and during fixation, even though the visual information on the retina is altered by the pursuit eye movement. We call these neurons compensatory pursuit neurons. In this study we develop a computational model of MSTd compensatory pursuit neurons based on physiological data from single unit studies. Our model MSTd neurons can simulate the velocity tuning of monkey MSTd neurons. The model MSTd neurons also show the pursuit compensation property. We find that pursuit compensation can be achieved by divisive interaction between signals coding eye movements and signals coding visual motion. The model generates two implications that can be tested in future experiments: (1) compensatory pursuit neurons in MSTd should have the same direction preference for pursuit and retinal visual motion; (2) there should be non-compensatory pursuit neurons that show opposite preferred directions of pursuit and retinal visual motion.     

Cursive writing with smooth pursuit eye movements

The eyes never cease to move: ballistic saccades quickly turn the gaze toward peripheral targets, whereas smooth pursuit maintains moving targets on the fovea where visual acuity is best. Despite the oculomotor system being endowed with exquisite motor abilities, any attempt to generate smooth eye movements against a static background results in saccadic eye movements [1, 2]. Although exceptions to this rule have been reported [3-5], volitional control over smooth eye movements is at best rudimentary. Here, I introduce a novel, temporally modulated visual display, which, although static, sustains smooth eye movements in arbitrary directions. After brief training, participants gain volitional control over smooth pursuit eye movements and can generate digits, letters, words, or drawings at will. For persons deprived of limb movement, this offers a fast, creative, and personal means of linguistic and emotional expression.     

A model of visually-guided smooth pursuit eye movements based on behavioral observations

We report a model that reproduces many of the behavioral properties of smooth pursuit eye movements. The model is a negative-feedback system that uses three parallel visual motion pathways to drive pursuit. The three visual pathways process image motion, defined as target motion with respect to the moving eye, and provide signals related to image velocity, image acceleration, and a transient that occurs at the onset of target motion. The three visual motion signals are summed and integrated to produce the eye velocity output of the model. The model reproduces the average eye velocity evoked by steps of target velocity in monkeys and humans and accounts for the variation among individual responses and subjects. When its motor pathways are expanded to include positive feedback of eye velocity and a switch, the model reproduces the exponential decay in eye velocity observed when a moving target stops. Manipulation of this expanded model can mimic the effects of stimulation and lesions in the arcuate pursuit area, the middle temporal visual area (MT), and the medial superior temporal visual area (MST).     

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. Received: 24 October 1994/Accepted in revised form: 16 December 1994     

Sensory and behavioral properties of neurons in posterior parietal cortex of the awake, trained monkey.

Neurons in posterior parietal cortex of the awake, trained monkey respond to passive visual and/or somatosensory stimuli. In general, the receptive fields of these cells are large and nonspecific. When these neurons are studied during visually guided hand movements and eye movements, most of their activity can be accounted for by passive sensory stimulation. However, for some visual cells, the response to a stimulus is enhanced when it is to be the target for a saccadic eye movement. This enhancement is selective for eye movements into the visual receptive field since it does not occur with eye movements to other parts of the visual field. Cells that discharge in association with a visual fixation task have foveal receptive fields and respond to the spots of light used as fixation targets. Cells discharging selectively in association with different directions of tracking eye movements have directionally selective responses to moving visual stimuli. Every cell in our sample discharging in association with movement could be driven by passive sensory stimuli. We conclude that the activity of neurons in posterior parietal cortex is dependent on and indicative of external stimuli but not predictive of movement.     

Complex predictive eye pursuit in monkey: a model system for cerebellar studies of skilled movement

Smooth pursuit eye movements provide a good model system for cerebellar studies of complex motor control in monkeys. First, the pursuit system exhibits predictive control along complex trajectories and this control improves with training. Second, the flocculus/paraflocculus region of the cerebellum appears to generate this control. Lesions impair pursuit and neural activity patterns are closely related to eye motion during complex pursuit. Importantly, neural responses lead eye motion during predictive pursuit and lag eye motion during non-predictable target motions that require visual control. The idea that flocculus/paraflocculus predictive control is non-visual is also supported by a lack of correlation between neural activity and retinal image motion during pursuit. Third, biologically accurate neural network models of the flocculus/paraflocculus allow the exploration and testing of pursuit mechanisms. Our current model can generate predictive control without visual input in a manner that is compatible with the extensive experimental data available for this cerebellar system. Similar types of non-visual cerebellar control are likely to facilitate the wide range of other skilled movements that are observed.     

Manuo-ocular coordination in target tracking. II. Comparing the model with human behavior

Several studies have shown that humans track a moving visual target with their eyes better if the movement of this target is directly controlled by the observer's hand. The improvement in performance has been attributed to coordination control between the arm motor system and the smooth pursuit (SP) system. In such a task, the SP system shows characteristics that differ from those observed during eye-alone tracking: latency (between the target-arm and the eye motion onsets) is shorter, maximum SP velocity is higher and the maximum target motion frequency at which the SP can function effectively is also higher. The aim of this article is to qualitatively evaluate the behavior of a dynamical model simulating the oculomotor system and the arm motor system when both are involved in tracking visual targets. The evaluation is essentially based on a comparison of the behavior of the model with the behavior of human subjects tracking visual targets under different conditions. The model has been introduced and quantitatively evaluated in a companion paper. The model is based on an exchange of internal information between the two sensorimotor systems, mediated by sensory signals (vision, arm muscle proprioception) and motor signals (arm motor command copy). The exchange is achieved by a specialized structure of the central nervous system, previously identified as a part of the cerebellum. Computer simulation of the model yielded results that fit the behavior of human subjects observed during previously reported experiments, both qualitatively and quantitatively. The parallelism between physiology and human behavior on the one hand, and structure and simulation of the model on the other hand, is discussed. Received: 6 March 1997 / Accepted in revised form: 15 July 1997     

Anticipatory Smooth Eye Movements in Autism Spectrum Disorder

Smooth pursuit eye movements are important for vision because they maintain the line of sight on targets that move smoothly within the visual field. Smooth pursuit is driven by neural representations of motion, including a surprisingly strong influence of high-level signals representing expected motion. We studied anticipatory smooth eye movements (defined as smooth eye movements in the direction of expected future motion) produced by salient visual cues in a group of high-functioning observers with Autism Spectrum Disorder (ASD), a condition that has been associated with difficulties in either generating predictions, or translating predictions into effective motor commands. Eye movements were recorded while participants pursued the motion of a disc that moved within an outline drawing of an inverted Y-shaped tube. The cue to the motion path was a visual barrier that blocked the untraveled branch (right or left) of the tube. ASD participants showed strong anticipatory smooth eye movements whose velocity was the same as that of a group of neurotypical participants. Anticipatory smooth eye movements appeared on the very first cued trial, indicating that trial-by-trial learning was not responsible for the responses. These results are significant because they show that anticipatory capacities are intact in high-functioning ASD in cases where the cue to the motion path is highly salient and unambiguous. Once the ability to generate anticipatory pursuit is demonstrated, the study of the anticipatory responses with a variety of types of cues provides a window into the perceptual or cognitive processes that underlie the interpretation of events in natural environments or social situations.     

Effects of vestibular and support afferentation upon visual pursuit in microgravity

Evaluation of the accuracy of eye turns (saccades) to fix a jerky pointed stimulus, and smooth pursuit of slow linear and sinusoidal movements of both pointed and optokinetic stimuli was performed in 31 cosmonauts on flight days 2-3, 5-8, 30, and once in one or two months of mission. An additional investigation of the eye pursuit function involved 10 cosmonauts, who, after testing during free floating, fulfilled stimulus tracking following a cycle of active head rotation, and 14 cosmonauts who received support afferentation. It was found that at the beginning of adaptation and periodically in the course of long mission, the systems of slow pursuit tracking adopted the strategy of saccadic approximation whereby gaze fixation was achieved through a sequence of macro- or microsaccadic movements. It was demonstrated that these disturbances, practically in all investigated cosmonauts, were consequent to the vestibular deprivation developing in microgravity. Vestibular afferentation produced by active head rotation improved characteristics of visual pursuit. Support deprivation also affects pursuit tracking by cosmonauts who form the concept of space orientation based on perception of their head and leg position. With support afferentation, these cosmonauts demonstrated improved visual pursuit characteristics.     

Different programming modes of human saccadic eye movements as a function of stimulus eccentricity: Indications of a functional subdivision of the visual field

1. Voluntary saccadic eye movements were made toward flashes of light on the horizontal meridian, whose duration and distance from the point of fixation were varied; eye movements were measured using d.c.-electrooculography.—2. Targets within 10°–15° eccentricity are usually reached by one saccadic eye movement. When the eyes turn toward targets of more than 10°–15° eccentricity, the first saccadic eye movement falls short of the target by an angle usually not exceeding 10°. The presence of the image of the target off the fovea (visual error signal) subsequent to such an undershoot elicits, after a short interval, corrective saccades (usually one) which place the image of the target on the fovea. In the absence of a visual error signal, the probability of occurrence of corrective saccades is low, but it increases with greater target eccentricities. These observations suggest that there are different, eccentricity-dependent modes of programming saccadic eye movements.—3. Saccadic eye movements appear to be programmed in retinal coordinates. This conclusion is based on the observations that, irrespective of the initial position of the eyes in the orbit, a) there are different programming modes for eye movements to targets within and beyond 10°–15° from the fixation point, and b_ the maximum velocity of saccadic eye movements is always reached at 25° to 30° target eccentricity. —4. Distributions of latency and intersaccadic interval (ISI) are frequently multimodal, with a separation between modes of 30 to 40 msec. These observations suggest that saccadic eye movements are produced by mechanisms which, at a frequency of 30 Hz, process visual information. —5. Corrective saccades may occur after extremely short intervals (30 to 60 msec) regardless of whether or not a visual error signal is present; the eyes may not even come to a complete stop during these very short intersaccadic intervals. It is suggested that these corrective saccades are triggered by errors in the programming of the initial saccadic eye movements, and not by a visual error signal. —6. The exitence of different, eccentricity-dependent programming modes of saccadic eye movements, is further supported by anatomical, physiological, psychophysical, and neuropathological observations that suggest a dissociation of visual functions dependent on retinal eccentricity. Saccadic eye movements to targets more eccentric than 10°–15° appear to be executed by a mechanism involving the superior colliculus (perhaps independent of the visual cortex), whereas saccadic eye movements to less eccentric targets appear to depend on a mechanism involving the geniculo-cortical pathway (perhaps in collaboration with the superior colliculus).     

Visual localization during eye tracking on steady background and during steady fixation on moving background

Experiments were performed to clarify the role of the background motion on the retina in the phenomenon of mislocation of brief visual stimuli during smooth eye tracking. It was found that these visual stimuli were mislocated also relative to a moving background during steady eye fixation. The magnitude of mislocation during pursuit eye movements and during steady fixation was influenced by the stimulus intensity, the background/eye velocity and the place of stimulus presentation in respect to the background; the influence having the same features in both cases. However, the magnitudes of mislocation under the two conditions were quantitatively different. The validity of a hypothesis that the eye movement itself plays no role in the process of localization, and, that this process is based on retinal information only, is considered.     

Eye and head movements to visual and auditory targets

Coordinated eye-head movements evoked by the presentation of visual, auditory and combined audio-visual targets were studied in 24 human subjects. At 60 deg located targets latencies of eye and head movements were shorter for auditory than for visual stimuli. Latencies were shorter for bisensory than for monosensory targets. The eye and head latencies were differently influenced by the modality of the stimulus when the eccentricity of the target was changed, but not by the variation of the stimulus duration. The different responses of the eye and the head depending on target modality and target eccentricity can be partially attributed to perceptual and central processing mechanisms, and are important to answer the question about the initial event in coordinated eye-head orientation.     

Visual-manual tracking and vestibular function during a seven-day dry immersion

A seven-day dry immersion experiment provided the opportunity to study the effects of decreased proprioceptive tactile and support afferentations on the vestibular function and visual-manual tracking. Before and after immersion, six subjects participated in a video oculographic evaluation of the static torsion otolith-cervicoocular reflex (OCOR) in response to head tilt by 30° in the frontal plane and dynamic vestibular-cervicoocular reactions to head longitudinal rotations at 0.125 Hz. In addition, the hand-eye motor coordination of tracking a jerky (sinusoidal) or smooth (linear) movement of point targets along the horizontal or vertical lines was evaluated on the basis of the data of electrooculography and records of manipulations with the joystick during immersion. A computerized test was performed in virtual glasses displaying images of visual stimuli and hand motor acts. The computed parameters included the reaction’s latent time, amplitude, speed and time of eye and hand movements, and gains of optooculomotor reactions and manual tracking as a ratio of eye/hand to visual stimulus speed. Testing was carried out before the experiment, after 3 h of immersion, on days 3 and 6 of staying in the bath, in the initial hours after immersion and on the third day of recovery. It was shown that removal of support and minimization of proprioceptive afferentation had a profound effect on the ocular tracking rather than pursuing the visual stimulus by hand. The accuracy of manual tracking was better in comparison with the eye tracking in all subjects. This was the first observation of changes in the peripheral vestibular system in two out of six subjects, i.e., inversion of the static torsion OCOP and positional nystagmus against a background of converted reflex, which did not change the parameters of the visual-manual tracking.     

Frame of reference transformations in motion perception during smooth pursuit eye movements

Smooth pursuit eye movements change the retinal image velocity of objects in the visual field. In order to change from a retinocentric frame of reference into a head-centric one, the visual system has to take the eye movements into account. Studies on motion perception during smooth pursuit eye movements have measured either perceived speed or perceived direction during smooth pursuit to investigate this frame of reference transformation, but never both at the same time. We devised a new velocity matching task, in which participants matched both perceived speed and direction during fixation to that during pursuit. In Experiment 1, the velocity matches were determined for a range of stimulus directions, with the head-centric stimulus speed kept constant. In Experiment 2, the retinal stimulus speed was kept approximately constant, with the same range of stimulus directions. In both experiments, the velocity matches for all directions were shifted against the pursuit direction, suggesting an incomplete transformation of the frame of reference. The degree of compensation was approximately constant across stimulus direction. We fitted the classical linear model, the model of Turano and Massof (2001) and that of Freeman (2001) to the velocity matches. The model of Turano and Massof fitted the velocity matches best, but the differences between de model fits were quite small. Evaluation of the models and comparison to a few alternatives suggests that further specification of the potential effect of retinal image characteristics on the eye movement signal is needed.     

Control and modulation of canal driven vestibulo-ocular reflex.

It has been well known that the canal driven vestibulo-ocular reflex (VOR) is controlled and modulated through the central nervous system by external sensory information (e.g. visual, otolithic and somatosensory inputs) and by mental conditions. Because the origin of retinal image motion exists both in the subjects (eye, head and body motions) and in the external world (object motion), the head motion should be canceled and/or the object should be followed by smooth eye movements. Human has developed a lot of central nervous mechanisms for smooth eye movements (e.g. VOR, optokinetic reflex and smooth pursuit eye movements). These mechanisms are thought to work for the purpose of better seeing. Distinct mechanism will work in appropriate self motion and/or object motion. As the results, whole mechanisms are controlled in a purpose-directed manner. This can be achieved by a self-organizing holistic system. Holistic system is very useful for understanding human oculomotor behavior.     

Frontal cortical control of smooth-pursuit

To maintain optimal clarity of objects moving slowly in three dimensional space, frontal eyed-primates use both smooth-pursuit and vergence (depth) eye movements to track precisely those objects and maintain their images on the foveae of left and right eyes. The caudal parts of the frontal eye fields contain neurons that discharge during smooth-pursuit. Recent results have provided a new understanding of the roles of the frontal eye field pursuit area and suggest that it may control the gain of pursuit eye movements, code predictive visual signals that drive pursuit, and code commands for smooth eye movements in a three dimensional coordinate frame.     

Characterization of Information-Based Learning Benefits with Submovement Dynamics and Muscular Rhythmicity

For skill advancement, motor variability must be optimized based on target information during practice sessions. This study investigated structural changes in kinematic variability by characterizing submovement dynamics and muscular oscillations after practice with visuomotor tracking under different target conditions. Thirty-six participants were randomly assigned to one of three groups (simple, complex, and random). Each group practiced tracking visual targets with trajectories of varying complexity. The velocity trajectory of tracking was decomposed into 1) a primary contraction spectrally identical to the target rate and 2) an intermittent submovement profile. The learning benefits and submovement dynamics were conditional upon experimental manipulation of the target information. Only the simple and complex groups improved their skills with practice. The size of the submovements was most greatly reduced by practice with the least target information (simple > complex > random). Submovement complexity changed in parallel with learning benefits, with the most remarkable increase in practice under a moderate amount of target information (complex > simple > random). In the simple and complex protocols, skill improvements were associated with a significant decline in alpha (8–12 Hz) muscular oscillation but a potentiation of gamma (35–50 Hz) muscular oscillation. However, the random group showed no significant change in tracking skill or submovement dynamics, except that alpha muscular oscillation was reduced. In conclusion, submovement and gamma muscular oscillation are biological markers of learning benefits. Effective learning with an appropriate amount of target information reduces the size of submovements. In accordance with the challenge point hypothesis, changes in submovement complexity in response to target information had an inverted-U function, pertaining to an abundant trajectory-tuning strategy with target exactness.