The Influence of Eye Movement on the Perceived Stability of the Environment

ABSTRACT The world we see is stable, in spite of retinal image shifts induced by head and eye movements. This is because of complex sensorimotor integrations between the oculomotor and sensory systems: visual, vestibular, and proprioceptive. Eye movements are the response of the motor system to sensory input. They are of two types: those induced by a visual input, and compensatory eye rotations responding to a vestibular signal. Visual input alerts the brain to a feature of interest in the environment, and the motor system acts accordingly to bring the image of the object onto the region of sharpest acuity, or to maintain it there if the eyes are following a moving object. To localize the target correctly, the motor system needs additional information about eye position. It appears that this information is utilized during both saccadic and smooth pursuit eye movements. The source of this input is not known. Primates have demonstrated accurate localization of targets presented visually, after ablation of the striate cortex. The superior colliculus may be involved in localizing a target before the eyes move to fixate it. This structure may also be responsible for distinguishing between real and self-induced stimulus movements. The oculomotor system interacts with the vestibular system to produce compensatory eye movements. The vestibulo-ocular reflex arc (VOR) serves to initiate rotation of the eyes, in the event of a head or body movement, to maintain an unchanged subjective straight-ahead direction. The operation of this reflex is not fully understood. An impairment of any sensory structure involved in ocular motility results in an imbalance between the sensorimotor integration, and consequent abnormal eye movements, sometimes accompanied by erroneous perceptions. Adequate coordination between sensory and motor systems is important for development of reading and writing skills.     

Temporal dynamics of ocular position dependence of the initial human vestibulo-ocular reflex

PURPOSE: While an ideal vestibulo-ocular reflex (VOR) generates ocular rotations compensatory for head motion, during visually guided movements, Listing's Law (LL) constrains the eye to rotational axes lying in Listing's Plane (LP). The present study was conducted to explore the recent proposal that the VOR's rotational axis is not collinear with the head's, but rather follows a time-dependent strategy intermediate between LL and an ideal VOR. METHODS: Binocular LPs were defined during visual fixation in eight normal humans. The VOR was evoked by a highly repeatable transient whole-body yaw rotation in darkness at a peak acceleration of 2800 deg/s2. Immediately before rotation, subjects regarded targets 15 or 500 cm distant located at eye level, 20 degrees up, or 20 degrees down. Eye and head responses were compared with LL predictions in the position and velocity domains. RESULTS: LP orientation varied both among subjects and between individual subject's eyes, and rotated temporally with convergence by 5 +/- 5 degrees (+/-SEM). In the position domain, the eye compensated for head displacement even when the head rotated out of LP. Even within the first 20 ms from onset of head rotation, the ocular velocity axis tilted relative to the head axis by 30% +/- 8% of vertical gaze position. Saccades increased this tilt. Regardless of vertical gaze position, the ocular rotation axis tilted backward 4 degrees farther in abduction than in adduction. There was also a binocular vertical eye velocity transient and lateral tilt of the ocular axis. CONCLUSIONS: These disconjugate, short-latency axis perturbations appear intrinsic to the VOR and may have neural or mechanical origins.     

Interactions between saccades and vestibulo-ocular reflex during double gaze shifts

After fixating the center, human subjects were required to track two visual targets (T1, T2) presented in the horizontal plane in a dark room. When T2 was lit 200-600 msec after T1, T2 was given and also second saccadic eye movement unsolicited at various positions of eye and head during the course of gaze (eye position in the orbit plus head position) shift toward T1. Under all circumstances, the final gaze reached T2 without significant difference from the trials made by eye movement alone, suggesting head and eye positions are perfectly monitored to adjust the amplitude of gaze. As head velocity increased, gaze velocity increased and duration decreased with little change in eye velocity, contrary to the previous assumption that vestibulo-ocular reflex adjusts the time course of gaze shift to be constant.     

Amplitude changes in response to target displacements during human eye-head movements

Sensorimotor adaptation, the ability to adjust motor output in response to persistent changes in sensory input, is a key function of the central nervous system. Although a great deal is known about vestibulo-ocular reflex and saccadic adaptation, relatively little is known about the behavior and neural mechanisms underlying gaze adaptation when the head is free to move. In an attempt to understand the mechanisms of gaze adaptation, and constrain hypotheses concerning the locus at which changes in gaze control may be implemented, we altered the size of large, head-unrestrained gaze shifts made to visual targets by surrepetitiously moving the visual target forward (30 degrees -->60 degrees ) or backwards (60 degrees -->30 degrees ) during gaze shifts. In our 10 human subjects, after a few hundred back-step trials, gaze amplitudes were reduced by between 6 degrees and 27 degrees. Similarly, after a few hundred forward adaptation trials, our subjects increased gaze amplitude by between 0 degrees and 26 degrees. Changes in the amplitude of primary gaze shifts occurred regardless of the particular combinations of eye and head movements that made up the amplitude-altered gaze shifts. When gaze shifts were initiated with the eyes in systematically different positions relative to the head, the resulting changes in gaze, eye and head movement amplitudes were consistent with the hypothesis that gaze adaptation occurs at the level of a gaze shift command and not by altering separately the signals that produce eye and head movements.     

Coordination of head and eye movements to fixate continuous and intermittent targets

To compare head-eye co-ordination with and without a target which was visible during the movement, subjects fixated in the direction of target lamps which: (i) flashed for 40 msec followed by 1 sec darkness; (ii) were continuously illuminated for 3 sec. Ballistic head movements were produced which made up 85 and 75 per cent respectively of the gaze displacement in conditions (i) and (ii). Eye movements were a combination of voluntary step, vestibulo-ocular reflex, position correcting steps and slow movements. Saccades produced by passive head rotation were modified during similar fixation movements. Accuracy of responses to flash was high although response components showed wide variability.     

Slow target-directed eye movements in ataxia-telangiectasia

PURPOSE: To analyze the slow eye movements that shift the direction of gaze in patients with ataxia-telangiectasia (A-T). METHODS: Eye and head movements were recorded with search coils in three patients with A-T during attempted gaze shifts, both with the head immobilized and free to move. RESULTS: Gaze shifts frequently included both saccadic and slow components. The slow movements were recorded after 42% of saccades and had an average peak velocity of 6.1 deg/sec and a mean amplitude of 2.0. They occurred with the head stationary and moving, could be directed centripetally or centrifugally, had velocity waveforms that were relatively linear or exponential, and always moved the eyes toward the visual target. CONCLUSIONS: The slow movements appear to differ from pursuit and vestibular eye movements and are not fully explained by the various types of abnormal eye movements that can follow saccades, such as gaze-evoked nystagmus or postsaccadic drift. Their origin is uncertain, but they could represent very slow saccades, due to aberrant inhibition of burst cell activity during the saccade.     

Photorefractive keratectomy in ophthalmic residents

PURPOSE: To find out how ophthalmologists themselves experience the correction of myopia after photorefractive keratectomy. Visuomotor functions were of special interest. METHODS: Four ophthalmology residents and one medical engineer underwent photorefractive keratectomy for myopia. Objective measurements including refraction, corneal topography, perimetry, contrast sensitivity, pattern visual evoked potentials, in vivo confocal microscopy, and a car driving simulator test were performed preoperatively, postoperatively, and at 6 months. Subjective evaluation was reported. RESULTS: Performing ophthalmological examinations and microsurgery without spectacles was easier postoperatively and was appreciated by the four ophthalmology residents. Minimal haze formation, good accuracy, and normal performance in the car driving simulator were also observed. Visual fields, contrast sensitivity, and pattern visual evoked potentials did not show changes. Negative observations included postoperative pain for 2 to 4 days, dry eye symptoms, a period of anisometropia between operations, and hypersensitivity of the lids. CONCLUSIONS: The four ophthalmic residents were satisfied with the outcome of their refractive surgery. Low to moderate myopic correction did not affect the objective measurements of high and low contrast sensitivity, pattern visual evoked potentials, or simulated car driving in dark illumination.     

Head-free reading of horizontally and vertically arranged texts

Parameters of eye and head movements and their coordination in reading horizontally and vertically arranged texts were compared. Reading was faster for horizontally arranged than for vertically arranged texts by 24%, primarily due to larger gaze amplitude for horizontal reading, and thus smaller numbers of saccades and fixations. The higher velocity of gaze saccades for given amplitudes in horizontal than vertical reading also contributed to the difference in reading speed. The horizontal bias in reading is at least partly due to the oculomotor system, because the higher velocity for given amplitude of horizontal saccade was also observed in a control experiment devoid of lexical load, in which a sequentially stepping laser target was tracked. The analysis of instantaneous phase of eye and head movements with a new metric derived by the Hilbert transform suggests that eye and head coupling is stronger for vertical than for horizontal direction in both reading and laser-tracking tasks. These results, combined with previous evidence that text familiarity modulates the timing and strength of head movement commands with respect to eye movements (Vis. Res. 39 (1999) 3761), indicate that the coupling strength between eye and head movements is variable depending on the direction of gaze shift and cognitive context.     

Fixation disparity,accommodation, dark vergence and dark focus during inclined gaze*

We investigated several oculomotor functions at different angles of vertical inclination of the gaze direction from 15 deg upwards to 45 deg downwards. The mean accommodative resting state (measured in a dark visual field) increased when the eyes or the head were declined from 0 to 45 deg. Fixation disparity (the vergence error in minutes of arc relative to the principle visual directions) became more eso when a fusion target at a viewing distance of 40 cm was lowered: declining the gaze by 45 deg changed mean fixation disparity by 1.8 min arc with eye inclination (keeping the head upright), and by 0.9 min arc with head inclination (with eye position unchanged relative to the head). When the eyes were lowered, the individual rate of eso change in fixation disparity was correlated with the amount of the subjects’ near shifts in the resting position of vergence, measured in darkness. Significant test-retest correlations between repeated measurements showed that the effects of eye inclination on vergence varied in a reproducible way among individuals with good binocular vision.     

Coordination of eye and head movements during reading

PURPOSE: There is little information regarding the characteristics of head movements during reading. This study was undertaken to investigate horizontal and vertical head movements during two different reading tasks. METHODS: Head and eye movements were monitored with an infrared pupil and head tracker in 15 subjects during repeated reading of text from an A4-sized card and a card 90 degrees wide. In addition, head and eye movements were recorded in 45 subjects to compare head movement propensity during an A4 text-reading task and a saccadic task of an equivalent gaze shift. RESULTS: During the A4 standard reading task, horizontal and vertical head movements accounted for 4.7% and 28.7% of the gaze shift, respectively. During the 90 degrees text reading, horizontal head movements accounted for 40.3% of the gaze amplitude, and vertical head movements accounted for 28.4%. Horizontal gaze velocities increased significantly on repeated A4 and 90 degrees text readings, as did horizontal head velocities and amplitudes. Reading head movement propensities were significantly smaller than saccadic head movement propensities (P < 0.001). CONCLUSIONS: Head movement strategies are rapidly switched between the A4 and 90 degrees text-reading paradigms. They are minimized during A4 text reading but actively assist the gaze strategy during 90 degrees text reading. Horizontal head movement is reduced during A4 reading compared to the equivalent saccadic task and may be suppressed to improve fixation stability. The results support the view that the head and eye movement system is a highly coupled but extremely flexible system.     

Physiology and pathology of eye-head coordination

Human head movement control can be considered as part of the oculomotor system since the control of gaze involves coordination of the eyes and head. Humans show a remarkable degree of flexibility in eye-head coordination strategies, nonetheless an individual will often demonstrate stereotypical patterns of eye-head behaviour for a given visual task. This review examines eye-head coordination in laboratory-based visual tasks, such as saccadic gaze shifts and combined eye-head pursuit, and in common tasks in daily life, such as reading. The effect of the aging process on eye-head coordination is then reviewed from infancy through to senescence. Consideration is also given to how pathology can affect eye-head coordination from the lowest through to the highest levels of oculomotor control, comparing conditions as diverse as eye movement restrictions and schizophrenia. Given the adaptability of the eye-head system we postulate that this flexible system is under the control of the frontal cortical regions, which assist in planning, coordinating and executing behaviour. We provide evidence for this based on changes in eye-head coordination dependant on the context and expectation of presented visual stimuli, as well as from changes in eye-head coordination caused by frontal lobe dysfunction.     

Use of infrared TV cameras built into head-mounted display to measure torsional eye movements

PURPOSE: The head-mounted display (HMD) has produced conflict between visual and vestibular stimuli because the HMD image does not move with the head motion of the wearer. The HMD can show binocular parallax three-dimensional (3D) images, in which vergence and accommodation conflict. Thus, the HMD may affect the normal visual/vestibular functions. We attempted to develop a system that makes possible the measurement of torsional eye movements, vergence eye movements, and pupillary responses of the HMD wearer. METHODS: Our apparatus is composed of two infrared CCD cameras installed in the HMD. Iris images produced by these cameras are analyzed by a personal computer using free software. Further, a third camera fixed on the HMD projects an image of the view as the subject sees it, via video tape recorder or frame memory to the HMD. Images can be stored, replayed, or frozen. RESULTS: Our system can measure torsional eye movement with 0.20 degrees resolution every 1/30 (or 1/60) seconds even though the pupil size alternates during measurement. Binocular eye movement and pupillary response are also measured. CONCLUSION: A system was developed which can be used for assessment of the effect of 3D HMD on the visual system. A third camera coupled with HMD can control visual stimulus independently of head motion (vestibular stimulus).     

Visual signs and symptoms of multiple system atrophy

Multiple system atrophy (MSA) is a rare movement disorder and a member of the ‘parkinsonian syndromes’, which also include Parkinson's disease (PD), progressive supranuclear palsy (PSP), dementia with Lewy bodies (DLB) and corticobasal degeneration (CBD). Multiple system atrophy is a complex syndrome, in which patients exhibit a variety of signs and symptoms, including parkinsonism, ataxia and autonomic dysfunction. It can be difficult to separate MSA from the other parkinsonian syndromes but if ocular signs and symptoms are present, they may aid differential diagnosis. Typical ocular features of MSA include blepharospasm, excessive square‐wave jerks, mild to moderate hypometria of saccades, impaired vestibular‐ocular reflex (VOR), nystagmus and impaired event‐related evoked potentials. Less typical features include slowing of saccadic eye movements, the presence of vertical gaze palsy, visual hallucinations and an impaired electroretinogram (ERG). Aspects of primary vision such as visual acuity, colour vision or visual fields are usually unaffected. Management of the disease to deal with problems of walking, movement, daily tasks and speech problems is important in MSA. Optometrists can work in collaboration with the patient and health‐care providers to identify and manage the patient's visual deficits. A more specific role for the optometrist is to correct vision to prevent falls and to monitor the anterior eye to prevent dry eye and control blepharospasm.     

Study of dynamic counterrolling of the eye--quantitative analysis of effects by visual and vestibular systems

Dynamic counterrolling of the eye is induced when the head is tilted to one side: it includes cyclorotatory nystagmus, which is affected by visual and vestibular systems. Both of these two ocular movements were measured quantitatively through a video recording system, and the role of visual and vestibular systems in visual stabilization was analyzed. The relationship between the optokinetic and vestibulo-ocular systems was variable in relation to the velocity of head tilting. The optokinetic system contributed more in slow head tilting. As the velocity of head tilting increased, the suppression by the optokinetic system was decreased and eventually the vestibulo-ocular system became more dominant. This suggests that the role of visual and vestibular systems in head tilting is similar to that in head rotation. Visual and vestibular systems seem to work together mutually with some individual variation in stabilizing vision with sensory control in the higher level of the visual cortex.     

Driving habits of patients with glaucoma

BACKGROUND: Central visual field defects due to glaucoma are common, increasing with old age. Impaired visual processing, for instance caused by glaucoma, may play a role in the aetiology of car accidents involving older drivers which can result in personal injury. Mandatory eye exams with assessment of the visual field in elderly people holding a driving licence will become more and more important, especially in a continuously ageing and increasingly mobile population. MATERIALS AND METHODS: In this prospective study, 80 patients with overt glaucoma and 52 patients without glaucoma, all holders of a valid driving licence, were enrolled. For each patient, the best corrected visual acuity was recorded and an examination of the central visual field was performed with automatic perimetry. In addition, a detailed questionnaire about the current driving habits of the patient was requested. RESULTS: In summary, 29 patients (36 %; 95 % CI: 26 - 48 %) of 80 glaucoma patients were driving a motor vehicle with binocular congruent scotomata within the central 30 degrees visual field, which is not sufficient to meet current legal requirements in Austria. In addition, 3 out of 29 impaired patients had a visual acuity that was below the mandatory legal requirements. A total of 39 patients (49 %; 95 % CI: 37 - 60 %) of the glaucoma patients fulfilled legal requirements. Examination of these patients showed only monocular or binocular central visual field defects that were not congruent. However, 12 (15 %; 95 % CI: 8 - 25 %) patients were holders of a valid driving licence, but had stopped driving some time ago. Based on the prevalence of glaucoma and the number of driving licence holders, the projected number of actively driving glaucoma patients who do not meet the legal requirements regarding the visual field is probably around 15,400 (7,400 - 29,500) in Austria and around 163,500 (79,000 - 313,500) in Germany. CONCLUSIONS: Time limits for the validity of the driving licence within the European Community have been set. In addition, the legal requirements for driving a motor vehicle should also be clearly defined, especially the requirements regarding the visual field and the acceptable dimensions of central scotomata. In addition, a mandatory eye exam for older drivers to be performed by ophthalmologists should be considered in order to detect persons posing a safety risk in traffic.     

Head and eye movements and the role of memory limitations in a visual search paradigm

The image information guiding visual behavior is acquired and maintained in an interplay of gaze shifts and visual short-term memory (VSTM). If storage capacity of VSTM is exhausted, gaze shifts can be used to regain information not currently represented in memory. By varying the separation between relevant image regions, S. Inamdar and M. Pomplun (2003) demonstrated a trade-off between VSTM storage and gaze shifts, which were performed as pure eye movements, that is, without a head movement component. Here we extend this paradigm to larger gaze shifts involving both eye and head movements. We use a comparative visual search paradigm with two relevant image regions and region separation as independent variable. Image regions were defined by two cupboards displaying colored geometrical objects in roughly equal arrangements. Subjects were asked to find differences in the arrangement of the objects in the two cupboards. Cupboard separation was varied between 30 degrees and 120 degrees . Images were presented with two projectors on a 150 degrees x 70 degrees curved screen. Head and eye movements were simultaneously recorded with an ART head tracker and an ASL mobile eye tracker, respectively. In the large separation conditions, the number of gaze shifts between the two cupboards was reduced, while fixation duration increased. Furthermore, the head movement proportions negatively correlated with the number of gaze shifts and positively correlated with fixation duration. We conclude that the visual system uses increased VSTM involvement to avoid gaze movements and in particular movements of the head. Scan path analysis revealed two subject-specific strategies (encode left, compare right, and vice versa), which were consistently used in all separation conditions.     

Surgical treatment of torticollis in cases of congenital nystagmus with strabismus

To correct compensatory head turn in twelve cases with congenital nystagmus, they were classified into two types according to the relative visual lines of both eyes to each other with respect to the sagittal axis of the head or the median plane of the body. One was termed the symmetrical pattern and the other was termed the asymmetrical pattern. In cases of the symmetrical pattern, a neutral zone exists in which the dominant eye in in the adducted position of gaze with esotropia and in the abducted position of gaze with exotropia. However, in the case of the asymmetrical pattern the neutral zone of the dominant eye is located in the abducted position of gaze with esotropia and in the abducted position of gaze with exotropia. Surgery was performed by shifting the dominant eye to the direction of the sagittal axis of the head in accordance with the degree of ocular deviation in the primary position. In asymmetrical pattern cares, both eyes were surgically shifted in parallel to the direction of the sagittal axis of the head without regard to the types of strabismus. The operation was based on the degree of compensatory head turn. We compared the surgical results the two types. In symmetrical cases, decreasing strabismus was disappointing compared to the head turn, while in asymmetrical cases decreasing head turn was disappointing as compared to strabismus. From these results surgery should be confined to the dominant eye in symmetrical cases, taking as the basis for operation the degree of head turn and not the ocular deviation.(ABSTRACT TRUNCATED AT 250 WORDS)     

反向偏斜与上斜肌麻痹

反向偏斜（dkew deviation）为一种后天获得性的共同性垂直斜视,临床表现为头部倾斜、眼球旋转及主观视觉的垂直方向倾斜,该类患者大脑感知的主观视觉世界在垂直方向是倾斜的,因而眼睛和头部向偏斜的视觉方向旋转,以恢复垂直方向的定位。反向偏斜的病因为内耳椭圆囊至眼运动神经核的前庭-眼反射通路受损。通过文献回顾,简要概述反向偏斜的病因、临床表现、临床分型,并与常见的上斜肌麻痹相鉴别,借以提高眼科临床医师对反向偏斜的重视,避免将其误诊为单纯的上斜肌麻痹,而忽略对椭圆囊耳石器或中枢神经病灶的诊断。     

The effects of sustained vertical gaze deviation on the resting state of the vergence system

Vergence of the eyes in the dark depends on the vertical direction of gaze. In three experiments this phenomenon was studied using eye inclinations and head tilts of 5 min duration during which monocular or binocular near and distant stimuli were inspected. The effects of eye inclination and head tilt on dark vergence were temporally stable; they exhibited even a tendency to increase with the passage of time. On return to horizontal gaze, positive aftereffects were found, that is dark vergence was biased towards its value with a vertically deviated gaze. The effect of vertical gaze direction turned out to be additive to the effect of binocular near fixation. These findings represent evidence against the hypothesis that the effect of vertical gaze direction on dark vergence is mediated by a feedforward signal that is related to voluntary effort in raising or depressing the eyes.     

Differential impact of partial cortical blindness on gaze strategies when sitting and walking - an immersive virtual reality study

The present experiments aimed to characterize the visual performance of subjects with long-standing, unilateral cortical blindness when walking in a naturalistic, virtual environment. Under static, seated testing conditions, cortically blind subjects are known to exhibit compensatory eye movement strategies. However, they still complain of significant impairment in visual detection during navigation. To assess whether this is due to a change in compensatory eye movement strategy between sitting and walking, we measured eye and head movements in subjects asked to detect peripherally-presented, moving basketballs. When seated, cortically blind subjects detected ∼80% of balls, while controls detected almost all balls. Seated blind subjects did not make larger head movements than controls, but they consistently biased their fixation distribution towards their blind hemifield. When walking, head movements were similar in the two groups, but the fixation bias decreased to the point that fixation distribution in cortically blind subjects became similar to that in controls - with one major exception: at the time of basketball appearance, walking controls looked primarily at the far ground, in upper quadrants of the virtual field of view; cortically blind subjects looked significantly more at the near ground, in lower quadrants of the virtual field. Cortically blind subjects detected only 58% of the balls when walking while controls detected ∼90%. Thus, the adaptive gaze strategies adopted by cortically blind individuals as a compensation for their visual loss are strongest and most effective when seated and stationary. Walking significantly alters these gaze strategies in a way that seems to favor walking performance, but impairs peripheral target detection. It is possible that this impairment underlies the experienced difficulty of those with cortical blindness when navigating in real life.