Apparent movement and appearance of periodic stripes during eye movements across a stroboscopically illuminated random dot pattern

When the eyes follow a small target moving across a stationary random dot pattern illuminated stroboscopically at 3--45 flashes . s-1, the structure of the random dot pattern is seen as moving in the direction of the eye pursuit movements (sigma-movement). At flash frequencies above 9.5 flashes . s-1, periodic stripes oriented perpendicularly to the direction of the pursuit eye movements appear and are also seen as moving in the direction of the eye pursuit movement. The period Ps of the apparent stripes depended on the flash frequency fs and the angular speed of the eyes Ve: Formula: see text. Apparent sigma-movement and apparent stripes were also seen when eye pursuit movements were initiated outside of the random dot pattern and they continued autonomously without a moving target across the pattern. The angular velocity of the sigma-pursuit movement across the random dot pattern depended on the flash frequency and the angular velocity of the initiating target. With the eyes stationary but a moving random dot pattern, the apparent stripes also appeared at flash frequencies fs greater than or equal to 9.5 flashes . s-1. Eq. (1) was valid when Ve was replaced by the target angular velocity Vs (k = 1).     

Sigma-optokinetic nystagmus in squirrel monkeys elicited by stationary stripe patterns illuminated by regular and random-interval flash sequences

 Eye position and angular velocity were measured in squirrel monkeys (Saimiri sciureus) by means of the electromagnetic scleral search-coil technique. Horizontal sigma-optokinetic nystagmus (sigma-OKN) was elicited by a stationary, stroboscopically illuminated, periodic, vertical-stripe pattern lining a vertical cylinder. The relationship between the mean slow-phase eye angular velocity, V_e, of sigma-OKN and the product of pattern period, P_s, and flash frequency, f_s, was determined. When V_e approximated k·P_s·f_s (deg·s^–1) and k was an integer ≥l, the sigma-paradigm was fulfilled. Sigma-OKN could be evoked in different ”modes”, whereby k approximated 1, 2,…n. The sigma-OKN properties of squirrel monkeys were similar to those measured for sigma-OKN in the ”stare” mode in man, with the exception of a long-lasting optokinetic afternystagmus (sigma-OKAN) appearing in the monkey. A considerable amount of temporal variability in flash sequence intervals (”temporal noise”), causing retinal error signals that interfered with the sigma-paradigm, was accepted by the visuo-motor system without interruption of sigma-OKN. This observation was explained by the operation of a short memory device for perception of visual motion. The internal gain, g_i, which relates the retinal ”error” displacement velocity, V_r, and V_e depended, in turn, on V_r according to a function resembling the known relationship between neuronal activity of NOT (nucleus of the optic tract) nerve cells and V_r. This observation may be taken as direct proof that sigma-OKN can be explained by a centrally preprogrammed relationship between the retinal velocity, V_r, and the OKN slow-phase eye velocity, V_e. It is stipulated that the sum of V_r and efference copy signals generated in cortical or subcortical gaze centers is the essential component controlling the perceived velocity of the sigma-movement, whereby a short-term integrator plays a role for squirrel monkey sigma-OKN. When the flash frequency, f_s, was modulated periodically according to a sinewave or ”triangular” function at a rate below 0.5 cycles·s^–1, V_e was found to respond with a corresponding modulation, provided the modulation amplitude did not exceed 50% of the mean flash rate. When the latter occurred, nonlinear responses could be observed. A similar response was found when the speed of ”real” optokinetic stimuli was varied sinusoidally. Under these experimental conditions, however, the amplitude of the V_e variation yielded up to 1.0 approximately linear responses. Received: 4 May 1998 / Accepted: 3 September 1998     

Sigma-movement and optokinetic nystagmus elicited by stroboscopically illuminated stereopatterns

Summary Sigma-movement is an apparent movement seen when a stationary periodic visual pattern of the period P_s is illuminated Stroboscopically at the flash frequency f_s and smooth gaze pursuit eye movements are performed across the pattern at an angular velocity V_e = P_s · f_s deg · s^–1. Sigma-movement leads to an optokinetic nystagmus (Sigma OKN) which in turn sustains Sigma-movement perception. (1) Sigma-movement was also seen in an apparent three-dimensional periodic stripe pattern generated by two periodic monocular stimulus patterns with a certain degree of horizontal binocular disparity. (2) Sigma-movement perception and Sigma-OKN were also elicited by a Stroboscopically illuminated, stationary, random dot stereostripe pattern. The periodicity P_s of this pattern is generated on the cyclopean retina (Julesz 1971). The equation described above was also valid. When the time delay t between left eye and right eye flashes was varied, the apparent depth of the random dot stereostripe pattern decreased with increasing t, but the Sigmaeffects were not affected. (3) Sigma-movement illusion and Sigma-pursuit movements can also be induced when real three-dimensional objects composed of periodic components are Stroboscopically illuminated and adequate gaze or eye pursuit movements are induced. Sigma-movement is related to gaze movement and is therefore elicitable by eye, head or body movements. (4) Sigma-movement is presumably caused by the interaction of efference copy signals (generated in a cortical gaze pursuit system) and afferent visual signals. The present data indicate that neuronal mechanisms for this interaction are located — at least in part — at or beyond the level of binocular fusion and stereopsis.Supported by grants of the Deutsche Forschungsgemeinschaft (Gr161)     

Pursuit eye movements and their neural control in the monkey

1. Single units in the 3. and 6. nerve nuclei were recorded, together with the stimulus and eye movements in trained macaques during pursuit eye movements. 2. The relationship between the impulse rate of an oculomotor motoneuron and the corresponding eye movements can be described by a first order differential equation only, if distinctions are made between the modes of the oculomotor system (e.g., fixation or pursuit) and between the agonist phase and the antagonist phase of the corresponding eye muscle. 3. The trained monkeys showed a frequency response during pursuit eye movements, which was comparable to that of humans and which clearly indicates the existence of a predictor mechanism. 4. After sudden stimulus disappearance in the pursuit mode, both the neural impulse rate and the eye movement performed smooth changes for more than 1s. These slow post-pursuit eye movements were related to the time course before stimulus disappearance. 5. Our findings lead to the hypothesis, that pursuit eye movements in primates, if elicited by small moving visual stimuli, are generated by means of a feedback system consisting of a predictor mechanism, the parameters of which are continuously corrected by an updating process in the afferent visual system.     

Combined eye-head gaze shifts to visual and auditory targets in humans

We studied the characteristics of combined eye-head gaze shifts in human subjects to determine whether they used similar strategies when looking at visual (V), auditory (A), and combined (V+A) targets located at several target eccentricities along the horizontal meridian. Subjects displayed considerable variability in the combinations of eye and head movement used to orient to the targets, ranging from those who always aligned their head close to the target, to those who relied predominantly on eye movements and only moved their head when the target was located beyond the limits of ocular motility. For a given subject, there was almost no variability in the amount of eye and head movement in the three target conditions (V, A, V+A). The time to initiate a gaze shift was influenced by stimulus modality and eccentricity. Auditory targets produced the longest latencies when located centrally (less than 20° eccentricity), whereas visual targets evoked the longest latencies when located peripherally (greater than 40° eccentricity). Combined targets (V+A) elicited the shortest latency reaction times at all eccentricities. The peak velocity of gaze shifts was also affected by target modality. At eccentricities between 10 and 30°, peak gaze velocity was greater for movements to visual targets than for movements to auditory targets. Movements to the combined target were of comparable speed with movements to visual targets. Despite the modality-specific differences in reaction latency and peak gaze velocity, the consistency of combinations of eye and head movement within subjects suggests that visual and auditory signals are remapped into a common reference frame for controlling orienting gaze shifts. A likely candidate is the deeper layers of the superior colliculus, because visual and auditory signals converge directly onto the neurons projecting to the eye and head premotor centers.     

Retinal ganglion cell synchronization by fixational eye movements improves feature estimation

Image movements relative to the retina are essential for the visual perception of stationary objects during fixation. Here we have measured fixational eye and head movements of the turtle, and determined their effects on the activity of retinal ganglion cells by simulating the movements on the isolated retina. We show that ganglion cells respond mainly to components of periodic eye movement that have amplitudes of roughly the diameter of a photoreceptor. Drift or small head movements have little effect. Driven cells that are located along contrast borders are synchronized, which reliably signals a preceding movement. In an artificial neural network, the estimation of spatial frequencies for various square wave gratings improves when timelocked to this synchronization. This could potentially improve stimulus feature estimation by the brain.     

Sensory-to-motor processing of the ocular-following response

The ocular-following response is a slow tracking eye movement that is elicited by sudden drifting movements of a large-field visual stimulus in primates. It helps to stabilize the eyes on the visual scene. Previous single unit recordings and chemical lesion studies have reported that the ocular-following response is mediated by a pathway that includes the medial superior temporal (MST) area of the cortex and the ventral paraflocculus (VPFL) of the cerebellum. Using a linear regression model, we systematically analyzed the quantitative relationships between the complex temporal patterns of neural activity at each level with sensory input and motor output signals (acceleration, velocity, and position) during ocular-following. The results revealed the following: (1) the temporal firing pattern of the MST neurons locally encodes the dynamic properties of the visual stimulus within a limited range. On the other hand, (2) the temporal firing pattern of the Purkinje cells in the cerebellum globally encodes almost the entire motor command for the ocular-following response. We conclude that the cerebellum is the major site of the sensory-to-motor transformation necessary for ocular-following, where population coding is integrated into rate coding.     

The Aubert-Fleischl phenomenon: A temporal frequency effect on perceived velocity in afferent motion perception

Apparent velocities of moving visual stimuli are known to be different depending on whether the subject pursues the stimulus (efferently controlled motion perception) or whether the eye is stationary and the image moves across the retina (afferent motion perception). Afferent motion perception of a periodic pattern or a moving single object causes overestimation of velocity (magnitude estimations) as compared to smooth pursuit. This socalled Aubert-Fleischl phenomenon is shown to depend on local temporal frequency stimulation on the retina caused by the repetitive passage of contrast borders of the moving periodic pattern. This is evidenced by the fact that for a given stimulus speed the amount of overestimation is a function of the spatial frequency of the pattern (or the angular subtend of a single moving object) and that the Aubert-Fleischl phenomenon is not observed if a single edge moves. Background characteristics seem not to influence the apparent velocity during smooth pursuit.     

Neuronal dynamics in the visual corticothalamic pathway revealed through binocular rivalry

Summary Single unit activity was recorded from principal cells in the A-laminae of the cat dorsal lateral geniculate nucleus (dLGN). A steady state pattern of afferent activation was induced by presenting a continuously drifting square wave grating of constant spatial frequency to the eye (the dominant eye) that provided the excitatory input to the recorded cell. Intermittently, a second grating stimulus was presented to the other, nondominant, eye. In most neurones nondominant eye stimulation led to inhibition of relay cell responses. The latency of this suppressive effect was unusually long (up to 1 s) and its intensity and duration depended critically on the similarity between the gratings that were presented to the two eyes. Typically suppression was strongest when the gratings differed in orientation, direction of movement and contrast and when the nondominant eye stimulus was moving rather than stationary. Ablation of visual cortex abolished these long latency and feature-dependent interferences. We conclude that the visual cortex and the corticothalamic projections are involved in the mediation of these interocular interactions. We interpret our results as support for the hypothesis that corticothalamic feedback modifies thalamic transmission as a function of the congruency between ongoing cortical activation patterns and afferent retinal signals.     

Activity of movement sensitive neurons of the cat's tectum opticum during spontaneous eye movements

Summary Activity of tectal movement specific neurons was recorded during spontaneous eye movements in total darkness and in presence of stationary visual stimuli. According to their reactions in presence or absence of stationary visual stimuli tectal units can be divided into four categories:1. Neurons which are silent or discharge independently of eye movements, when the animal stays in total darkness, but which fire in synchrony with eye movements when stationary stimuli are presented. 2. Neurons which remain unaffected when the animal makes eye movements in total darkness or in presence of a stationary pattern. 3. Neurons which fire in synchrony with eye movements in absence and in presence of stationary patterns. In a few of these neurons tested curarization of the animal led to a marked increase of spontaneous activity. 4. Neurons whose spontaneous and stimulus driven discharge is suppressed in synchrony with eye movements when the animal is exposed to total darkness or when it faces stationary patterns     

Ongoing eye movements constrain visual perception

Eye movements markedly change the pattern of retinal stimulation. To maintain stable vision, the brain possesses a variety of mechanisms that compensate for the retinal consequences of eye movements. However, eye movements may also be important for resolving the ambiguities often posed by visual inputs, because motor commands contain additional spatial information that is necessarily absent from retinal signals. To test this possibility, we used a perceptually ambiguous stimulus composed of four line segments, consistent with a shape whose vertices were occluded. In a passive condition, subjects fixated a spot while the shape translated along a certain trajectory. In several active conditions, the spot, occluder and shape translated such that when subjects tracked the spot, they experienced the same retinal stimulus as during fixation. We found that eye movements significantly promoted perceptual coherence compared to fixation. These results indicate that eye movement information constrains the perceptual interpretation of visual inputs.     

Eye- and head movements in freely moving rabbits.

1. Eye- and head movements were recorded in unrestrained, spontaneously behaving rabbits with a new technique, based upon phase detection of signals induced in implanted coils by a rotating magnetic field. 2. Movements of the eye in space were exclusively saccadic. In the intersaccadic intervals the eyes were stabilized in space, even during vigorous head movements. Most of this stability was maintained in darkness, except for the occurrence of slow drift. 3. Many saccades were initiated while the head was stationary. They were accompanied by a similar, but slower head rotation with approximately the same amplitude. The displacement of the eye in space was a pure step without appreciable under- or over-shoot. The deviation of the eye in the head was mostly transient. 4. Other saccades were started while the head was moving and were possibly fast phases of a vestibulo-ocular reflex. The time course of the eye movement in space was identical for all saccades, whether the head was moving prior to the saccade or not. Eye movements without any head movement were not observed. 5. Saccades were mostly large (average 20-6 +/- 12-4 degrees S.D.) and never smaller than 1 degree. The relations of maximal velocity and duration to amplitude were similar to those reported for man. 6. Visual pursuit of moving objects, when elicited, was only saccadic and never smooth. 7. It is concluded that the co-ordination and dynamics of the rabbit's head- and eye movements are similar to those of primates. In the absence of foveal specilization, the eye movements are restricted to a rather global redirection of the visual field, possibly in particular of the binocular area.     

The directional effects of passive eye movement on the directional visual responses of single units in the pigeon optic tectum

 We have investigated the visual responses of 184 single units located in the superficial layers of the optic tectum (OT) of the decerebrate, paralysed pigeon. Visual responses were similar to those reported in non-decerebrate preparations; most units responded best to moving visual stimuli, 18% were directionally selective (they had a clear preference for a particular direction of visual stimulus movement), 76% were plane-selective (they responded to movement in either direction in a particular plane). However, we also found that a high proportion of units showed some sensitivity to the orientation of visual stimuli. We examined the effects of extraocular muscle (EOM) afferent signals, induced by passive eye movement (PEM), on the directional visual responses of units. Visual responses were most modified by particular directions of eye movement, although there was no unique relationship between the direction of visual stimulus movement to which an individual unit responded best and the direction of eye movement that caused the greatest modification of that visual response. The results show that EOM afferent signals, carrying information concerning the direction of eye movement, reach the superficial layers of the OT in the pigeon and there modify the visual responses of units in a manner that suggests some role for these signals in the processing of visual information. Received: 17 June 1996 / Accepted: 29 April 1997     

Integration of retinal and motor signals of eye movements in striate cortex cells of the alert cat

Responses of saccade-depressed (SD) and saccade-excited (SE) cells in the striate cortex to eye movements of alert cats under presentation of a visual pattern were studied under reinforcement of the eye movements with rewards of water. These responses were compared to those on passive displacement of the visual pattern reproducing the movements of the retinal image occurring during eye movements while eye movements were suppressed by withdrawal of reinforcement. Passive displacement of the visual pattern produced in the SD cells depression closely resembled the depression occurring during eye movements under presentation of the visual pattern, in time course as well as in amplitude. Both the saccade depression and the depression due to passive movement of the visual pattern were nonselective to the direction of eye movements. Saccade excitation of the SE cells frequently contained two components occurring at 20 and 80 ms after the onsets of eye movements. Passive displacement of the visual pattern produced in the SE cells excitation comparable with the early component of the saccade excitation. These findings suggest that saccade depression in the SD cells and the early component of the saccade excitation in the SE cells are related to retinal reafference of eye movement. During presentation of visual patterns, saccade excitation in the SE cells was closely related to parameters of eye movements, such as direction, amplitude, duration, and velocity. The correlations were completely lost or strongly reduced in darkness. Lines of evidence were provided that the saccade excitation of the SE cells in darkness or the later component of the saccade excitation under presentation of a visual pattern represents efference copy signals of eye movement transferred to the striate cortex through the Clare-Bishop (CB) cortex. Excitation comparable with saccade excitation in darkness occurred in synchrony with activities of the oculomotor nuclei even after retrobulbar paralysis of eye movement, indicating that the excitation is related to efference copy signals rather than proprioceptive reafference of eye movement.(ABSTRACT TRUNCATED AT 400 WORDS)     

Evidence for corrective effects of afferent signals from the extraocular muscles on single units in the pigeon vestibulo-oculomotor system

The role of extraocular muscle (EOM) afferent feedback signals in the control of eye movement is still controversial. We recorded from 106 single units in the vestibular nuclei, oculomotor nuclei and reticular formation of 80 decerebrate, paralysed pigeons. EOM afferents were stimulated by passive eye movement (PEM) during vestibular stimulation by sinusoidal oscillation in the horizontal plane. We found that EOM afferent signals profoundly modified the vestibular responses of 91 (86%) of the single units recorded. As well as using PEM to simulate eye movements similar to saccades, we moved the eye in a manner which mimicked the slow phase of the vestibulo-ocular reflex (artificial VOR, AVOR). We have found evidence that, as well as providing signals closely related to the parameters of eye movement, PEM alters the vestibular responses of cells during AVOR in a manner which suggests that EOM afferent signals may play a corrective role in the moment-to-moment control of eye movement in the vestibulo-ocular reflex.     

Neural maps of head movement vector and speed in the optic tectum of the barn owl

1. This study investigates the contribution of the optic tectum in encoding the metric and kinetic properties of saccadic head movements. We describe the dependence of head movement components (size, direction, and speed) on parameters of focal electrical stimulation of the barn owl's optic tectum. The results demonstrate that both the site and the amount of activity can influence head saccade metrics and kinetics. 2. Electrical stimulation of the owl's optic tectum elicited rapid head movements that closely resembled natural head movements made in response to auditory and visual stimuli. The kinetics of these movements were similar to those of saccadic eye movements in primates. 3. The metrics and kinetics of head movements evoked from any given site depended strongly on stimulus parameters. Movement duration increased with stimulus duration, as did movement size. Both the size and the maximum speed of the movement increased to a plateau value with current strength and pulse rate. Movement direction was independent of stimulus parameters. 4. The initial position of the head influenced the size, direction, and speed of movements evoked from any given site: when the owl initially faced away from the direction of the induced saccade, the movement was larger and faster than when the owl initially faced toward the direction of the induced movement. 5. A characteristic movement of particular size, direction, and speed could be defined for each site by the use of stimulation parameters that elicited plateau movements with normal kinetic profiles and by having the head initially centered on the body. The size, direction, and speed of these characteristic movements varied systematically with the site of stimulation across the tectum. The map of head movement vector (size and direction) was aligned with the sensory representations of visual and auditory space, such that the movement elicited from a given site when the owl initially faced straight ahead brought the owl to face that region of space represented by the sensory responses of the neurons at the site of stimulation. 6. The results imply that both the site and the amount of neural activity in the optic tectum contribute to encoding the metrics and kinetics of saccadic movements. A comparison of the present findings with previous studies on saccadic eye movements in primates and combined eye and head movements in cats suggests striking similarities in the ways in which tectal activity specifies a redirection in gaze to such dissimilar motor effectors as the eyes and head.     

Eye and head coupled and dissociated movements during orientation to a double step visual target displacement

Summary Tight coupling between eye and head movements has been observed in response to a single visual target offset. On this basis, when the visual stimulus consists of two successive steps in the same (horizontal) direction, either increasing in eccentricity (staircase) or decreasing in eccentricity (pulse-step) gaze should be due to concomitant eye and head angular displacement. That is, the eyes and head should aim at each target displacement so that their combined movement matches target offset. We have tested this hypothesis in five healthy subjects. The measured variables were head and gaze offset, the interval between two consecutive saccades from onset to onset (I) and the response delay between onset of the second step and onset of the first gaze saccade (D). With both staircase and pulse-step stimuli, the eye saccade preceded the head movement, and the gaze response either had the stimulus profile pattern or consisted of one gaze saccade to the final target offset. In response to staircase stimuli, I decreased concomitantly with an increase in D; with pulse-step stimuli, as D increased, I decreased slightly in three subjects and decreased markedly in two subjects. Dissociation between the eye and head movements could clearly be demonstrated with pulse-step stimuli: the first gaze saccade to the target pulse displacement was accompanied by a head movement to the target step offset. We also observed cases in which the gaze saccade to the target step displacement was made simultaneously with the head movement to the target pulse offset. Our study extends previous observations in head fixed condition and illustrates that in the majority of cases, when the head is free and a visual pulse step stimulus is presented, both the saccadic and head systems have the ability to modify or cancel the initial neural command to move to the first target displacement. When this modification takes place in only one system, eye and head movements are dissociated.On leave from the Occupational Health and Rehabilitation Institute at Loewenstein Hospital, P.O. Box 3, Raanana 43 100, Israel     

Contribution of the frontal eye field to gaze shifts in the head-unrestrained monkey: effects of microstimulation

The role of the primate frontal eye field (FEF) has been inferred primarily from experiments investigating saccadic eye movements with the head restrained. Three recent reports investigating head-unrestrained gaze shifts disagree on whether head movements are evoked with FEF stimulation and thus whether the FEF participates in gaze movement commands. We therefore examined the eye, head, and overall gaze movement evoked by low-intensity microstimulation of the low-threshold region of the FEF in two head-unrestrained monkeys. Microstimulation applied at 200 or 350 Hz for 200 ms evoked large gaze shifts with substantial head movement components from most sites in the dorsomedial FEF, but evoked small, predominantly eye-only gaze shifts from ventrolateral sites. The size and direction of gaze and eye movements were strongly affected by the eye position before stimulation. Head movements exhibited little position dependency, but at some sites and initial eye positions, head-only movements were evoked. Stimulus-evoked gaze shifts and their eye and head components resembled those elicited naturally by visual targets. With stimulus train durations >200 ms, the evoked gaze shifts were more likely to be accomplished with a substantial head movement, which often continued for the entire stimulus duration. The amplitude, duration and peak velocity of the evoked head movement were more strongly correlated with stimulus duration than were those of the gaze or eye movements. We conclude that the dorsomedial FEF generates a gaze command signal that can produce eye, head, or combined eye-head movement depending on the initial orbital position of the eye.     

Enhanced activation of neurons in prelunate cortex before visually guided saccades of trained rhesus monkeys

Summary Single unit recording from trained rhesus monkeys demonstrate that the activity of the prelunate cortex is enhanced when a visual stimulus becomes a target of saccadic eye movement. As a rule, the enhancement is spatially selective: it does not occur if the animal makes an eye movement away from, rather than towards the stimulus. The results show that the prelunate cortex has access to an extraretinal signal which is activated in association with events preceding visually guided eye movements. Whether the signal reflects the initiation of eye movement or the animal's interest in the stimulus, which he usually selects to initiate an eye movement, remains uncertain.Supported by the Deutsche Forschungsgemeinschaft (DFG), Sonderforschungsbereich Hirnforschung und Sinnesphysiologie (SFB 70, Tp. B7)     

Short latency compensatory eye movement responses to transient linear head acceleration: a specific function of the otolith-ocular reflex

Summary Normal subjects were exposed to 0.26 g linear acceleration steps along the inter-aural axis whilst they fixated an earth stationary target at 110 cm distance. The stimulus evoked slow phase eye movements at a mean latency of 34 ms which attained the relative target velocity in 113 ms. In contrast, visual following with head fixed, of identical relative target motion, had significantly longer latencies and time to match target velocity. The short latency responses to linear acceleration were absent in an alabyrinthine subject. It is concluded that the otolith-ocular reflex is responsible for the short latency responses to linear head movement and functions to stabilise vision during sudden head movement before visually guided compensatory eye movements take effect.