Uwe J. Ilg

The neural basis of smooth-pursuit eye movements.

Smooth-pursuit eye movements are used to stabilize the image of a moving object of interest on the fovea, thus guaranteeing its high-acuity scrutiny. Such movements are based on a phylogenetically recent cerebro-ponto-cerebellar pathway that has evolved in parallel with foveal vision. Recent work has shown that a network of several cerebrocortical areas directs attention to objects of interest moving in three dimensions and reconstructs the trajectory of the target in extrapersonal space, thereby integrating various sources of multimodal sensory and efference copy information, as well as cognitive influences such as prediction. This cortical network is the starting point of a set of parallel cerebrofugal projections that use different parts of the dorsal pontine nuclei and the neighboring rostral nucleus reticularis tegmenti pontis as intermediate stations to feed two areas of the cerebellum, the flocculus-paraflocculus and the posterior vermis, which make mainly complementary contributions to the control of smooth pursuit.

Posterior parietal cortex neurons encode target motion in world-centered coordinates.

The motion areas of posterior parietal cortex extract information on visual motion for perception as well as for the guidance of movement. It is usually assumed that neurons in posterior parietal cortex represent visual motion relative to the retina. Current models describing action guided by moving objects work successfully based on this assumption. However, here we show that the pursuit-related responses of a distinct group of neurons in area MST of monkeys are at odds with this view. Rather than signaling object image motion on the retina, they represent object motion in world-centered coordinates. This representation may simplify the coordination of object-directed action and ego motion-invariant visual perception.

The neural basis of smooth pursuit eye movements in the rhesus monkey brain

Smooth pursuit eye movements are performed in order to prevent retinal image blur of a moving object. Rhesus monkeys are able to perform smooth pursuit eye movements quite similar as humans, even if the pursuit target does not consist in a simple moving dot. Therefore, the study of the neuronal responses as well as the consequences of micro-stimulation and lesions in trained monkeys performing smooth pursuit is a powerful approach to understand the human pursuit system. The processing of visual motion is achieved in the primary visual cortex and the middle temporal area. Further processing including the combination of retinal image motion signals with extra-retinal signals such as the ongoing eye and head movement occurs in subsequent cortical areas as the medial superior temporal area, the ventral intraparietal area and the frontal and supplementary eye field. The frontal eye field especially contributes anticipatory signals which have a substantial influence on the execution of smooth pursuit. All these cortical areas send information to the pontine nuclei, which in turn provide the input to the cerebellum. The cerebellum contains two pursuit representations: in the paraflocculus/flocculus region and in the posterior vermis. While the first representation is most likely involved in the coordination of pursuit and the vestibular-ocular reflex, the latter is involved in the precise adjustments of the eye movements such as adaptation of pursuit initiation. The output of the cerebellum is directed to the moto-neurons of the extra-ocular muscles in the brainstem.

Deviation of eyes and head in acute cerebral stroke

BackgroundIt is a well-known phenomenon that some patients with acute left or right hemisphere stroke show a deviation of the eyes (Prévosts 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).MethodsEye-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.ResultsEach 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° right, while it was close to the saggital body midline (0°) in the groups with acute left- or right-sided stroke but no spatial neglect as well as in healthy subjects.ConclusionA marked horizontal eye and head deviation observed ~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 patients 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.

Single-neuron evidence for a contribution of the dorsal pontine nuclei to both types of target-directed eye movements, saccades and smooth-pursuit

The primate dorsolateral pontine nucleus (DLPN) is a key link in a cerebro‐cerebellar pathway for smooth pursuit eye movements, a pathway assumed to be anatomically segregated from tegmental circuits subserving saccades. However, the existence of afferents from several cerebrocortical and subcortical centres for saccades suggests that the DLPN and neighbouring parts of the dorsal pontine nuclei (DPN) might contribute to saccades as well. In order to test this hypothesis, we recorded from the DPN of two monkeys trained to perform smooth pursuit eye movements as well as visually and memory‐guided saccades. Out of 281 neurons isolated from the DPN, 138 were responsive in oculomotor tasks. Forty‐five were exclusively activated in saccade paradigms, 68 exclusively by smooth pursuit and 25 neurons showed responses in both. Pursuit‐related responses reflected sensitivity to eye position, velocity or combinations of velocity and position with minor contributions of acceleration in many cases. When tested in the memory‐guided saccades paradigm, 65 out of 70 neurons activated in saccade paradigms showed significant saccade‐related bursts and 20 significant activity in the memory period. Our finding of saccade‐related activity in the DPN in conjunction with the existence of strong anatomical input from saccade‐related cerebrocortical areas suggests that the DPN serves as a precerebellar relay for both pursuit and saccade‐related information originating from cerebral cortex, in addition to the classical tecto‐tegmental circuitry for saccades.

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.

Visual Stability and the Motion Aftereffect: A Psychophysical Study Revealing Spatial Updating

Eye movements create an ever-changing image of the world on the retina. In particular, frequent saccades call for a compensatory mechanism to transform the changing visual information into a stable percept. To this end, the brain presumably uses internal copies of motor commands. Electrophysiological recordings of visual neurons in the primate lateral intraparietal cortex, the frontal eye fields, and the superior colliculus suggest that the receptive fields (RFs) of special neurons shift towards their post-saccadic positions before the onset of a saccade. However, the perceptual consequences of these shifts remain controversial. We wanted to test in humans whether a remapping of motion adaptation occurs in visual perception. The motion aftereffect (MAE) occurs after viewing of a moving stimulus as an apparent movement to the opposite direction. We designed a saccade paradigm suitable for revealing pre-saccadic remapping of the MAE. Indeed, a transfer of motion adaptation from pre-saccadic to post-saccadic position could be observed when subjects prepared saccades. In the remapping condition, the strength of the MAE was comparable to the effect measured in a control condition (33±7% vs. 27±4%). Contrary, after a saccade or without saccade planning, the MAE was weak or absent when adaptation and test stimulus were located at different retinal locations, i.e. the effect was clearly retinotopic. Regarding visual cognition, our study reveals for the first time predictive remapping of the MAE but no spatiotopic transfer across saccades. Since the cortical sites involved in motion adaptation in primates are most likely the primary visual cortex and the middle temporal area (MT/V5) corresponding to human MT, our results suggest that pre-saccadic remapping extends to these areas, which have been associated with strict retinotopy and therefore with classical RF organization. The pre-saccadic transfer of visual features demonstrated here may be a crucial determinant for a stable percept despite saccades.

Anticipatory smooth-pursuit eye movements in man and monkey

A fundamental problem in the generation of goal-directed behaviour is caused by the inevitable latency of biological sensory systems. Behaviour which is fully synchronised with the triggering sensory event can only be executed if the occurrence of this event can be predicted based on prior information. Smooth-pursuit eye movements are a classical and well-established example of goal-directed behaviour. The execution of these eye movements is thought to be very closely linked to the processing of visual motion signals. Here, we show that healthy human subjects as well as trained rhesus monkeys are able to initiate smooth-pursuit eye movements in anticipation of a moving target. These anticipatory pursuit eye movements are scaled to the velocity of the expected target. Furthermore, we can exclude the possibility that anticipatory pursuit is simply an after-pursuit of the previous trial. Visually-guided pursuit is only marginally affected by the presence of a structured background. However, the presence of a structured background severely impedes the ability to perform anticipatory pursuit. More generally, our data provide additional evidence that the cognitive oculomotor repertoires of human and monkeys are similar, at least with respect of smooth-pursuit in the prediction of an appearing target.

Flicker in the visual background impairs the ability to process a moving visual stimulus

For the detection of a moving object, segregating the object from the background is a necessary first step. This segregation can be achieved by detection of differences in the spatial, temporal and spatio‐temporal properties of the object and background. Here we investigate how flicker influences the perception of a moving object in man and monkey, and we examine the neuronal responses in extrastriate medial temporal and medial superior temporal areas (MT and MST) of two rhesus monkeys. The performance of humans and monkeys in a direction discrimination task was impaired in the presence of flicker in the background compared to the static background condition. A similar effect was found in recordings from 155 single units in areas MT and MST during the discrimination task. The discriminability (d′) of the neuronal responses in preferred and nonpreferred directions was reduced by 33% on average in the presence of a flicker background compared to the static background. This reduction in discriminability was not caused by differences in variance of the neuronal activity for the two background conditions, but was due to a reduction of the difference between the activities in preferred and nonpreferred direction. This reduction in directional selectivity could be traced back to two different mechanisms: in 32 out of 155 neurons (21%), the decrease resulted from an increase in the response to the stimulus moving in the nonpreferred direction; in 62 out of 155 neurons (40%), the reduction in directional selectivity was due to a decrease in the response to the preferred direction. These results give deeper insights into how moving stimuli are processed in the presence of background flicker as present in natural visual scenes.

The effects of video game play on the characteristics of saccadic eye movements

Video game play has become a common leisure activity all around the world. To reveal possible effects of playing video games, we measured saccades elicited by video game players (VGPs) and non-players (NVGPs) in two oculomotor tasks. First, our subjects performed a double-step task. Second, we asked our subjects to move their gaze opposite to the appearance of a visual target, i.e. to perform anti-saccades. As expected on the basis of previous studies, VGPs had significantly shorter saccadic reaction times (SRTs) than NVGPs for all saccade types. However, the error rates in the anti-saccade task did not reveal any significant differences. In fact, the error rates of VGPs were actually slightly lower compared to NVGPs (34% versus 40%, respectively). In addition, VGPs showed significantly higher saccadic peak velocities in every saccade type compared to NVGP. Our results suggest that faster SRTs in VGPs were associated with a more efficient motor drive for saccades. Taken together, our results are in excellent agreement with earlier reports of beneficial video game effects through the general reduction in SRTs. Our data clearly provides additional experimental evidence for an higher efficiency of the VGPs on the one hand and refutes the notion of a reduced impulse control in VGPs on the other.