Deviation of eyes and head in acute cerebral stroke.

BACKGROUND: It is a well-known phenomenon that some patients with acute left or right hemisphere stroke show a deviation of the eyes (Prévost's sign) and head to one side. Here we investigated whether both right- and left-sided brain lesions may cause this deviation. Moreover, we studied the relationship between this phenomenon and spatial neglect. In contrast to previous studies, we determined not only the discrete presence or absence of eye deviation with the naked eye through clinical inspection, but actually measured the extent of horizontal eye-in-head and head-on-trunk deviation. In further contrast, measurements were performed early after stroke onset (1.5 days on average). METHODS: Eye-in-head and head-on-trunk positions were measured at the bedside in 33 patients with acute unilateral left or right cerebral stroke consecutively admitted to our stroke unit. RESULTS: Each single patient with spatial neglect and right hemisphere lesion showed a marked deviation of the eyes and the head to the ipsilesional, right side. The average spontaneous gaze position in this group was 46 degrees right, while it was close to the saggital body midline (0 degrees ) in the groups with acute left- or right-sided stroke but no spatial neglect as well as in healthy subjects. CONCLUSION: A marked horizontal eye and head deviation observed approximately 1.5 days post-stroke is not a symptom associated with acute cerebral lesions per se, nor is a general symptom of right hemisphere lesions, but rather is specific for stroke patients with spatial neglect. The evaluation of the patient's horizontal eye and head position thus could serve as a brief and easy way helping to diagnose spatial neglect, in addition to the traditional paper-and-pencil tests.

Processing of second-order motion stimuli in primate middle temporal area and medial superior temporal area.

Two rhesus monkeys were subjects in a direction-discrimination task involving moving stimuli defined by either first- or second-order motion. Two different second-order motion stimuli were used: drift-balanced motion consisting of a rectangular field of stationary dots and theta motion consisting of the same rectangular field with dots moving in the direction opposite to that of the object. The two types of stimuli involved different segmentation cues between the moving object and the background: temporal structure of the luminance (flicker) in the case of drift-balanced motion and opposed motion in the case of the theta-motion stimulus. Our monkeys were able to correctly report the direction of each stimulus. Single-unit recordings from the middle temporal (MT) and medial superior temporal (MST) areas revealed that 16 out of 38 neurons (41%) from area MT and 34 out of 68 neurons (50%) from area MST responded in a directionally selective manner to the drift-balanced stimulus. The movement of an object defined by theta motion is not explicitly encoded in the neuronal activity in areas MT or MST. Our results do not support the hypothesis that the neuronal activity in these areas codes for the direction of stimulus movement independent of specific stimulus parameters. Furthermore, our results emphasize the relevance of different segmentation cues between figure and background. Therefore the notion that there are multiple sites responsible for the processing of second-order motion is strongly supported.

Cancellation of self-induced retinal image motion during smooth pursuit eye movements.

When our eyes are tracking a target that is moving in front of a structured background, global motion of equal speed is induced in the opposite direction. This effect has been termed reafference, which, astonishingly, does not significantly affect the execution of such pursuit eye movements. Employing brief and unexpected injections of full-field motion during ongoing human smooth pursuit, we demonstrate that the sensitivity for full-field motion is reduced strongly in the direction opposite to the eye movement, i.e. the direction of reafferent background motion. Our experiments further characterize this asymmetry in visual motion processing and provide a preliminary explanation for the accuracy of the pursuit system despite self-induced motion.

Image segmentation: a tug-of-war for the eyeball.

Separating objects from their background is one of the central abilities of the visual system. Recent evidence has revealed how populations of neurons, some of which have receptive fields with an antagonistic center-surround structure, and some of which do not, might contribute to this ability.

Initiation of smooth-pursuit eye movements to first-order and second-order motion stimuli.

Since normal human subjects can perform smooth-pursuit eye movements only in the presence of a moving target, the occurrence of these eye movements represents an ideal behavioural probe to monitor the successful processing of visual motion. It has been shown previously that subjects can execute smooth-pursuit eye movements to targets defined by luminance and colour, the first-order stimulus attributes, as well as to targets defined by derived, second-order stimulus attributes such as contrast, flicker or motion. In contrast to these earlier experiments focusing on steady-state pursuit, the present study addressed the course of pre-saccadic pursuit initiation (less than 100 ms), as this early time period is thought to represent open-loop pursuit, i.e. the eye movements are exclusively driven by visual inputs proceeding the onset of the eye movement itself. Eye movements of five human subjects tracking first- and second-order motion stimuli had been measured. The analysis of the obtained eye traces revealed that smooth-pursuit eye movements could be initiated to first-order as well as second-order motion stimuli, even before the execution of the first initial saccade. In contrast to steady-state pursuit, the initiation of pursuit was not exclusively determined by the movement of the target, but rather due to an interaction between dominant first-order and less-weighted second-order motion components. Based on our results, two conclusions may be drawn: first and specific for initiation of smooth-pursuit eye movements, we present evidence supporting the notion that initiation of pursuit reflects integration of all available visual motion information. Second and more general, our results further support the hypothesis that the visual system consists of more than one mechanism for the extraction of first-order and second-order motion.

Asymmetry in visual motion processing.

The smooth pursuit system is traditionally employed using a single small target moving on a homogeneous background. It still is not fully understood, however, how accurate tracking is sustained in the presence of a structured background, which will activate global motion processing in the opposite direction as a consequence of the ongoing eye movement. To further study this interaction, we used brief shifts of a textured background injected at various times during the initiation of smooth pursuit. While shifts opposite to the target direction did not alter smooth pursuit performance, those in the same direction resulted in a marked transient perturbation of the pursuit. These results suggest a simple yet limited mechanism that adjusts the sensitivity of global motion processing.

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.

Slow eye movements.

Monkeys and humans are able to perform different types of slow eye movements. The analysis of the eye movement parameters, as well as the investigation of the neuronal activity underlying the execution of slow eye movements, offer an excellent opportunity to study higher brain functions such as motion processing, sensorimotor integration, and predictive mechanisms as well as neuronal plasticity and motor learning. As an example, since there exists a tight connection between the execution of slow eye movements and the processing of any kind of motion, these eye movements can be used as a biological, behavioural probe for the neuronal processing of motion. Global visual motion elicits optokinetic nystagmus, acting as a visual gaze stabilization system. The underlying neuronal substrate consists mainly of the cortico-pretecto-olivo-cerebellar pathway. Additionally, another gaze stabilization system depends on the vestibular input known as the vestibulo-ocular reflex. The interactions between the visual and vestibular stabilization system are essential to fulfil the plasticity of the vestibulo-ocular reflex representing a simple form of learning. Local visual motion is a necessary prerequisite for the execution of smooth pursuit eye movements which depend on the cortico-pontino-cerebellar pathway. In the wake of saccades, short-latency eye movements can be elicited by brief movements of the visual scene. Finally, eye movements directed to objects in different planes of depth consist of slow movements also. Although there is some overlap in the neuronal substrates underlying these different types of slow eye movements, there are brain areas whose activity can be associated exclusively with the execution of a special type of slow eye movement.

Smooth-pursuit eye movements elicited by first-order and second-order motion.

The perception of the displacement of luminance-defined contours (i.e., first-order motion) is an important and well-examined function of the visual system. It can be explained, for example, by the operation of elementary motion detectors (EMDs), which cross-correlate the spatiotemporal luminance distribution. More recent studies using second-order motion stimuli, i.e., shifts of the distribution of features such as contrast, texture, flicker, or motion, extended classic concepts of motion perception by including nonlinear or hierarchical processing in the EMD. Smooth-pursuit eye movements can be used as a direct behavioral probe for motion processing. The ability of the visual system to extract motion signals from the spatiotemporal changes of the retinal image can be addressed by analyzing the elicited eye movements. We measured the eye movement response to moving objects defined by two different types of first-order motion and two different types of second-order motion. Our results clearly showed that the direction of smooth-pursuit eye movements was always determined by the direction of object motion. In particular, in the case of second-order motion stimuli, smooth-pursuit did not follow the retinal image motion. The latency of the initial saccades during pursuit of second-order stimuli was slightly but significantly increased, compared with the latency of saccades elicited by first-order motion. The processing of second-order motion in the peripheral visual field was less exact than the processing of first-order motion in the peripheral field. Steady state smooth-pursuit eye speed did not reflect the velocity of second-order motion as precisely as that of first-order motion, and the resulting retinal error was compensated by saccades. Interestingly, for slow second-order stimuli we observed that the eye could move faster than the target, leading to small, corrective saccades in the opposite direction to the ongoing smooth-pursuit eye movement. We conclude from our results that both visual perception and the control of smooth-pursuit eye movements have access to processing mechanisms extracting first- and second-order motion.

Visual responses of neurons from areas V1 and MT in a monkey with late onset strabismus: a case study.

One adult monkey (Macaca fascicularis) was investigated psychophysically and electrophysiologically after at least 5 years of late onset esotropic macrostrabismus (squint angle 52 deg). Behavioural tests revealed normal monocular visual and visuomotor functions. No indications of deep amblyopia or oculomotor asymmetry were found. The monkey used the left or right eye alternately at about equal frequencies. Single unit recordings from area VI disclosed a normal ocular dominance distribution. Most VI neurons from both hemispheres received binocular input. Thus, discordant visual information from corresponding retinal locations of the two eyes converged onto the cortical neurons. No evidence for anomalous retinal correspondence was found. Diplopia and confusion must therefore be avoided by suppression of vision through one eye to allow stable, unambiguous perception. Possible suppression was investigated by stimulating a neuron through the same eye when it was actively used for fixation in one set of trials, and when it was not used for fixation in another set of trials. Significant differences in these two stimulus conditions were found in 20/39 neurons from area VI and in 11/34 motion sensitive neurons recorded in the middle superior temporal area (MT). The normalized population activity in VI and MT was higher if cells were stimulated through the fixating eye. The data are discussed with respect to possible suppressive mechanisms helping to prevent double vision in strabismus and in binocular rivalry.

Responses of primate area MT during the execution of optokinetic nystagmus and afternystagmus.

The directional selectivity of the visual response properties was determined in 148 neurons, all located in area MT of three hemispheres of two macaque monkeys. The preferred direction of every neuron was obtained by analyzing the response obtained by a circular movement of the background while the monkeys fixated a stationary target. The distribution of the preferred directions was isotropic and showed no ipsiversive bias. MT neurons were excited in a directionally selective manner during the execution of optokinetic nystagmus, in a similar way to that produced by visual stimulation during fixation. The majority of neurons showed a sensitivity to the velocity of retinal image slip. Activity during the execution of optokinetic nystagmus could be traced back to residual retinal image slip in the direction of optokinetic stimulation. No dynamic effects of the neuronal activity during the build-up of eye velocity in early optokinetic nystagmus were observed. Obviously, the activity in area MT did not reflect the charging of the velocity storage mechanism. Accordingly, following the cessation of stimulation, the activity dropped to the level of spontaneous activity and did not parallel the execution of optokinetic afternystagmus. These results suggest that area MT is not part of the velocity storage mechanism and, furthermore, that the storage mechanism must be downstream of area MT in the processing of visual motion for the generation of the optokinetic nystagmus and afternystagmus.

Eye position effects in monkey cortex. I. Visual and pursuit-related activity in extrastriate areas MT and MST.

We studied the effect of eye position on visual and pursuit-related activity in neurons in the superior temporal sulcus of the macaque monkey. Altogether, 109 neurons from the middle temporal area (area MT) and the medial superior temporal area (area MST) were tested for influence of eye position on their stimulus-driven response in a fixation paradigm. In this paradigm the monitored eye position signal was superimposed onto the stimulus control signal while the monkey fixated at different locations on a screen. This setup guaranteed that an optimized stimulus was moved across the receptive field at the same retinal location for all fixation locations. For 61% of the MT neurons and 82% of the MST neurons the stimulus-induced response was modulated by the position of the eyes in the orbit. Directional selectivity was not influenced by eye position. One hundred sixty-eight neurons exhibited direction-specific responses during smooth tracking eye movements and were tested in a pursuit paradigm. Here the monkey had to track a target that started to move in the preferred direction with constant speed from five different locations on the screen in random order. Pursuit-related activity was modulated by eye position in 78% of the MT neurons as well as in 80% of the MST neurons tested. Neuronal activity varied linearly as a function of both horizontal and vertical eye position for most of the neurons tested in both areas, i.e., two-dimensional regression planes could be approximated to the responses of most of the neurons. The directions of the gradients of these regression planes correlated neither with the preferred stimulus direction tested in the fixation paradigm nor with the preferred tracking direction in the pursuit paradigm. Eighty-six neurons were tested with both the fixation and the pursuit paradigms. The directions of the gradients of the regression planes fit to the responses in both paradigms tended to correlate with each other, i.e., for more than two thirds of the neurons the angular difference between both directions was less than +/-90 degrees. The modulatory effect of the position of the eyes in the orbit proved to balance out at the population level for neurons in areas MT and MST, tested with the fixation as well as the pursuit paradigm. Results are discussed in light of the hypothesis of an ongoing coordinate transformation of the incoming sensory signals into a nonretinocentric representation of the visual field.

Inability of rhesus monkey area V1 to discriminate between self-induced and externally induced retinal image slip.

Retinal image slip can result from an eye movement across a stationary object or alternatively from motion of the object while the eyes are stationary. The ability to discriminate between these two kinds of retinal image slip is necessary for the perception of a stable visual world. In order to determine if this ability is already present in monkey visual area V1, we asked if single V1 units are able to differentiate between externally and self-induced retinal image slip. Externally induced retinal image slip was realized in the 'object motion' condition (OMC) by moving a behaviourally irrelevant visual stimulus ('object': a bar or a large random dot pattern) across the receptive field while the monkey fixated a small, stationary target. Conversely, self-induced retinal image slip of comparable size was evoked in the 'ego motion' condition (EMC) by asking the monkey to pursue the target, moving at the speed of the object in the OMC, while the object was kept stationary. We recorded 221 units from visual area V1, 51, (23%) of them directionally selective, and compared their responses to self-induced and externally induced retinal image slip. Many of them seemed to give some preference to externally induced retinal image slip. However, on closer examination it became clear that this seeming preference could be attributed to the fact that oculomotor performance was less precise in the EMC than in the OMC, causing a larger deviation from the optimal retinal image trajectory in the EMC. We show that the impact of eye position errors can be eliminated by the use of a position-invariant stimulus, such as large-field random dot patterns. We then show that the impact of both eye position errors and deviation of eye velocity from target velocity in the EMC can be eliminated by moving the stimulus in a given OMC trial according to an inverted replica of the eye movement trajectory in the preceding EMC trial, guaranteeing identical retinal stimulation in the OMC and the EMC. If identical retinal stimulation was ensured, none of the V1 units tested was able to differentiate between externally and self-induced retinal image slip. We conclude that V1 does not contribute to the perception of a world which is stable despite eye movements.

Responses of neurons of the nucleus of the optic tract and the dorsal terminal nucleus of the accessory optic tract in the awake monkey.

The nucleus of the optic tract (NOT) and the dorsal terminal nucleus of the accessory optic tract (DTN) are essential nuclei for the generation of slow-phase eye movements during horizontal optokinetic nystagmus. We recorded from 101 neurons (all directionally selective) in four NOT/DTN of three trained and behaving rhesus monkeys. Neuronal activity increased when stimuli moved ipsiversively with respect to the recording site and decreased below spontaneous activity when stimuli moved contraversively. While the monkey fixated a small spot, some NOT/DTN neurons did not respond at all to the retinal image slip of a whole-field random dot pattern; others showed a monotonic increase of activity to increasing velocities of that stimulus. The velocity range tested was up to 100 degrees/s. During the execution of optokinetic nystagmus, 39 of 73 cells tested showed a velocity-tuned response with an average optimum at 21 degrees/s retinal image slip. Following saccades during optokinetic nystagmus (quick phases), the NOT/DTN neuronal activity briefly attained the level of spontaneous activity, as predicted from the velocity selectivity during optokinetic nystagmus. Immediately upon cessation of optokinetic stimulation in the preferred direction, NOT/DTN activity returned to the spontaneous level and did not reflect the ongoing optokinetic afternystagmus in darkness. Most NOT/DTN neurons displayed direction selectivity also during smooth pursuit. Twenty-one of 50 cells tested (42%) always responded to the retinal slip of the target (target velocity cells), 16 cells (32%) responded to the retinal slip of the background (background velocity cells), and 13 cells (26%) did not respond at all during smooth pursuit. We conclude from our results that the NOT/DTN is an essential structure for the processing of the direction and speed of retinal image slip. This information is then used for the generation and maintenance of slow eye movements, preferentially during horizontal optokinetic nystagmus but also during pursuit eye movements.

Eye movements elicited by transparent stimuli.

A transparent motion condition occurs when two different motion vectors appear at the same region of an image. Such transparency during self-motion has shown demonstrable effects on perception and on the underlying neurophysiology in the cortical and subcortical structures of primates. Presumably such stimulus conditions also influence oculomotor behavior. We investigated smooth-pursuit performance, using a transparent stimulus consisting of two oppositely-moving patterns. We found slight reduction in the mean eye velocity tracking a transparent pattern, compared with that when tracking a unidirectional pattern. Additionally, we investigated the behavior of the optokinetic system to transparency, demonstrating that it elicits antagonistic optokinetic nystagmus, with distinctly reduced gain of the slow phases. Furthermore, we observed, during optokinetic stabilization of transparent stimuli, directional dominances demonstrating that subjects preferably followed one direction. Presenting a transparent stimulus with oppositely moving patterns and different velocities we found a general velocity dominance demonstrating that patterns with a certain velocity are preferred. Performing all experiments under dichoptic conditions produced results comparable with those found under transparent stimulus conditions.

Optokinetic and pursuit system: a case report.

Several studies have demonstrated the importance of the pretectal Nucleus of the Optic Tract (NOT) and the Dorsal Terminal Nucleus of the accessory optic system (DTN) for the generation of horizontal optokinetic nystagmus (OKN). Although single unit data from trained rhesus monkey NOT/DTN cells are available it is still unclear if there is a link between the pursuit and the optokinetic system at this level of motion analysis. In order to address the question whether the NOT/DTN is important for the optokinetic as well as the pursuit system an electrolytic lesion was placed where NOT/DTN activity was recorded previously. The monkey was tested on optokinetic and pursuit paradigms. Immediately following the lesion the monkey performed a spontaneous nystagmus with slow phases directed away from the lesioned side. This spontaneous nystagmus persisted even during optokinetic stimulation in the opposite direction. During the first week postlesion the spontaneous nystagmus disappeared and the monkey regained the ability to perform optokinetic nystagmus toward the lesioned side. The gain of the mean slow phase eye velocity was, however, largely reduced for this stimulus direction. The onset of OKN following the onset of optokinetic stimulation was not affected by the lesion. During smooth pursuit the mean eye velocity was more reduced for pursuit towards the lesioned side. The resulting position error was compensated by an increase in the number of catch-up saccades. In addition to the confirmation of the well-known directional deficits of the optokinetic system caused by a lesion of the pretectum, a directional deficit in the pursuit system was demonstrated.

Functional grouping of the cortico-pretectal projection.

The ascendency of the cerebral cortex in mammals naturally raises questions about the role of the archetypal subcortical centers we share in common with other phyla. Here we report a situation in which an ancient oculomotor control center, the nucleus of the optic tract, is not so much dominated by the cerebral cortex as served by it. We suggest that the organization of cortical output to subcortical centers may be helpful in understanding the function of the cerebral cortex.

Motion perception during saccades.

Although the retinal image is displaced by each saccade performed we do not perceive the visual environment moving concordant with the saccades. In this study experiments were designed in which additional movement of most of the visual scene was applied during saccades. The subjects perceived the intrasaccadic movement after the saccade. The perceived speed of this movement was decreased and the threshold amplitude was increased compared to perception during fixation. The intrasaccadic movement perception was based on a novel aftereffect of motion perception. The velocity of retinal slip did not affect the threshold. If the retinal slip speed during saccades was temporally reduced by an intrasaccadic movement parallel to the saccade, the threshold amplitude was identical to the threshold amplitude obtained by intrasaccadic movement opposite to the saccade increasing retinal slip speed. Horizontal intrasaccadic movements were detected at lower thresholds than vertical movements independent of saccade direction. In addition, the thresholds were not effected by the saccade amplitude suggesting that neither speed, duration, nor direction of eye movement related retinal slip affects the amount of suppression. Our results suggest that saccadic suppression is related to delayed central processing of retinal information during saccades. This processing does not involve saccade parameters such as direction and amplitude.

Responses of monkey nucleus of the optic tract neurons during pursuit and fixation.

We recorded 101 neurons in the nucleus of the optic tract (NOT) of 3 rhesus monkeys. The neurons were tested in a variety of oculomotor paradigms. This report focusses on the modulation of NOT neuronal activity during smooth pursuit eye movements. A small horizontally moving spot (less than 1 degrees) elicited a directionally specific response during fixation and revealed thereby the extent of the receptive fields. During pursuit NOT neurons are coding for target slip. If eye speed exceeds target speed the direction of retinal slip is reversed and in accordance with their directional sensitivity NOT neurons immediately change their activity. This result proves the slip transfer function as well as the independence from eye movement signals of NOT neurons. During pursuit across a structured background some neurons are still coding for target slip whereas other neurons are coding for background slip. These two groups of neurons can also be distinguished by their response during fixation. The response of a target slip neuron to a background movement is cancelled, whereas the response of a background neuron is not affected by fixation. There is no difference in size of receptive fields for these two groups of neurons. We conclude from our findings that directionally selective cells in the monkey NOT may provide input to the pursuit system as well as to the optokinetic system. This dichotomy may also be reflected in different efferent projections: to the nucleus reticularis tegmenti pontis and to the inferior olive, respectively. A similar notion was introduced by the late Maekawa for the rabbit's NOT.

Influence of mechanical disturbance on oculomotor behavior.

Using a binocular search coil technique, we measured oculomotor behavior during gentle pressing with a finger on the outer canthus of one eye. With a steadily pressed viewing eye, and the fellow eye occluded, the occluded eye deviates while the pressed eye does not. If the eye is rapidly pressed and released, the compensation of rotational force in the pressed eye becomes incomplete, so that both eyes move. At high frequencies of press (greater than 1 Hz) the pressed eye is deviated and the contralateral eye no longer moves. In darkness the pressed eye always rotates but the contralateral eye never does, demonstrating that any inflow from proprioceptors sensing rotation of the pressed eye does not affect oculomotor posture as measured in the fellow eye. With binocular viewing the results are more variable. On some trials neither eye moves, while on others both move. The results can be interpreted as a Hering's law controlled attempting to reconcile disparate inputs from the two eyes. The results confirm and extend, with objective measures, earlier conclusions from subjective experiments.