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Asymmetric adaptive gain changes of the vertical vestibulo-ocular reflex in cats.

The present study was conducted to examine adaptive gain changes of vertical vestibulo-ocular reflex (VOR) after exposure to a vertical visual-vestibular mismatch in cats. The visual-vestibular mismatch was induced by oscillating the animals for an hour about an inter-aural axis at frequencies of 0.16 and 0.32 Hz with the peak velocity of 20 degrees/s, coupled with either in-phase ("gain decrease" conditioning) or out-of-phase ("gain increase" conditioning) sinusoidal rotation of a random-dot pattern. Eye movements were measured with a magnetic search coil system. Before conditioning, vertical VOR showed up-down asymmetric responses. That is, upward slow phase eye velocity (SPV) in response to downward head rotation was significantly larger than downward SPV in response to upward head rotation. After adaptation to "gain increase" conditioning, VOR gain increased in both stimulus directions. The increase in VOR gain was significantly larger for upward SPV than for downward SPV. After adaptation to "gain decrease" conditioning, VOR gain decreased in both stimulus directions. The decrease in VOR gain was, however, significantly larger for downward SPV than for upward SPV. Our results indicate that VOR in the vertical plane adaptively changes but that the gain change shows a directional asymmetry. This asymmetry was dependent on the direction of the slip of visual image rather than the direction of head rotation, and the gain change was smaller when the retinal slip was generated downward. Possible explanations for the asymmetry are discussed on a physiological and anatomical basis.

Adaptation, Physiological↗

Psychophysical measurement of eye drifts and tremor by dichoptic or monocular vernier acuity.

If the two segments of a vernier target are presented to different eyes, i.e. dichoptically, thresholds are three to four times higher than with presentation to the same eye. This increase in thresholds is mainly due to uncorrelated movements of both eyes, such as tremor and drifts, that occur even under steady fixation. The psychophysically measured thresholds allow one to calculate an upper estimate for the amplitudes of uncorrelated eye movements during fixation. This estimate matches the best results from direct eye position recording, with the calculated mean amplitude of eye tremor corresponding to roughly one photoreceptor diameter. The combined amplitude of both correlated and uncorrelated eye movements was also measured by delaying one segment of the vernier relative to its partner under monocular or dichoptic conditions. Fixation proved to be relatively stable, and trained observers could sustain eye position within a few min arc.

Cues↗

Spontaneous nystagmus and gaze-holding ability in monkeys after intravitreal picrotoxin injections.

1. Eye movements were measured in three rhesus monkeys after monocular intravitreal injections of picrotoxin, a gamma-aminobutyric acid (GABA) antagonist. The effects of this drug were tested when the animals were in a completely dark room, when they performed a smooth pursuit task, and when they viewed either a stationary pattern or a full-field optokinetic pattern rotating horizontally. 2. Between 15 and 20 min after the injection, a sustained conjugate spontaneous nystagmus developed in the dark, with the slow-phase movement in the temporal-to-nasal direction with respect to the injected eye. Peak slow-phase velocity ranged from 15 to 45 degrees/s. The nystagmus persisted for at least 1 h but stopped by the next day. 3. In a well-lit room, the nystagmus was completely suppressed, even during monocular viewing with the injected eye. When the lights were turned off, the slow-phase velocity of the spontaneous nystagmus slowly increased to a steady-state level within 70-120 s. 4. Horizontal smooth pursuit eye movements to a 1 degree target light moving in front of the animal +/- 20 degrees to either side of center of gaze at constant speeds were normal. Target speeds ranging from 15 to 60 degrees/s for both monocular and binocular viewing conditions were used. Binocular and monocular optokinetic nystagmus (OKN) to a full-field drum rotating at a constant velocity (5-90 degrees/s) were also normal. The initial pursuit and steady-state components of OKN were measured, as well as the velocity-storage component (optokinetic after nystagmus, OKAN).(ABSTRACT TRUNCATED AT 250 WORDS)

Animals↗

Conjugate ocular oscillations during shifts of the direction and depth of visual fixation.

PURPOSE: To characterize dynamic properties of combined saccade-vergence eye movements that occur as the point of visual fixation is shifted between objects lying in different directions and at different depths. METHODS: Using the scleral search-coil technique, eye movements were measured in 10 normal subjects as they made voluntary, disjunctive gaze shifts comprising a range of saccades and vergence movements. RESULTS: By analyzing eye acceleration records, the authors identified small-amplitude (0.2-0.7 degrees), high-frequency (23-33 Hz), conjugate horizontal oscillations of the eyes during the vergence movement that followed the initial saccade. When the shift of the fixation point required a large vergence component (17 degrees , every subject showed these oscillations; they were present in approximately a third of responses. Approximately 5% of responses showed oscillations that had horizontal and vertical components. Oscillations were less prominent with shifts that had smaller vergence components and were absent after saccades made between targets located at optical infinity. CONCLUSIONS: These findings suggest that a common mechanism gates both the saccadic and vergence components of disjunctive gaze shifts, a likely candidate being the pontine omnipause neurons. When a saccade is immediately followed by a prolonged vergence movement, the omnipause neurons remain silent, leading to small-amplitude saccadic oscillations. Shifts in the point of visual fixation that require a large vergence movement may be a useful experimental strategy to induce saccadic oscillations.

Adult↗

Influence of background luminance on visual sensitivity during saccadic eye movements.

Detection thresholds were measured for a brief test flash projected on a uniform background before, during, and after saccadic eye movement. The amount and duration of threshold elevation during saccades was directly dependent on back-ground illumination; no significant elevations occurred at backgrounds of 2.0 log fl or less. Similar results were obtained during fixation when the backgrounds were "saccadically" displaced. An occipital evoked potential was recorded in association with both eye movements and background displacements at higher background luminances (no test flash). These results may indicate an activation of a selected population of neural elements - probably the "Y" channels - which occurs during saccades in illuminated environments and which renders the channels less responsive to additional, simultaneous, and appropriately structured stimuli.

Adult↗

Eye movement responses to linear head motion in the squirrel monkey. I. Basic characteristics.

1. The purpose of this study was to quantify the response characteristics of eye movements produced by linear head oscillations in the dark (the linear vestibuloocular reflex, or LVOR). Horizontal, vertical, and torsional eye movements were measured in adult squirrel monkeys by the use of a dual scleral search-coil technique during linear oscillations (0.5, 1.5, and 5.0 Hz, 0.36 g peak acceleration) along the animals' interaural (IA), dorsoventral (DV), and nasooccipital (NO) axes. 2. Two LVOR responses, horizontal eye movements during IA-axis translation and vertical eye movements during DV-axis motion, were in a compensatory direction for head translation. Response amplitudes increased as frequency increased, whereas phase typically showed a lead. 3. Two other LVORs, torsional responses during IA-axis translation (all frequencies) and vertical responses during NO-axis oscillations (0.5 Hz), behaved differently. These two LVORs cannot be functionally compensatory for head translation because they degrade fixation on targets, and therefore image stability, by rotating the eyes off target (NO-vertical) or torting the eyes relative to the visual world (IA-torsional). Responses to NO-axis motion at frequencies greater than 0.5 Hz depended on initial eye position and fixation distance and are described in the companion paper. 4. The effect of head orientation on the LVOR was assessed by testing four head positions in 90 degrees steps around the axis of head motion for each of the three axes of translation. This was done, first, to determine whether the LVORs are responses to the "swinging vector" of gravitoinertial force during linear head motion or to head translation; and second, to quantify potential effects of static head (otolith) orientation on the LVORs. Results showed no systematic effects of head orientation on LVOR responses in the frequency bandwidth studied. This indicates that the LVORs are dependent on the direction of linear motion relative to the head (and otolith organs) but not on the swinging vector of gravitoinertial force, and that the LVORs are uninfluenced by static orientation of the head and reloading of the otoliths.

Animals↗

Capture of the visual direction of monocular objects by adjacent binocular objects.

Investigations of binocular visual direction have concentrated mainly on stationary objects. Eye positions were generally not measured and binocular fixation was assumed to be perfect. During the viewing of stationary objects, vergence errors are not negligible but small. During the viewing of moving objects, however, errors in binocular fixation are much larger. Existing rules for binocular visual direction were examined under the latter, more demanding viewing conditions. Eye movements were measured objectively by the scleral coil technique. Subjects viewed a large stereogram in which the half-images oscillated in counterphase. The stereogram contained two square random-dot patterns placed side by side with a gap in between. A vertical line, visible only to one eye, oscillated in the gap. Subjects were asked to adjust the amplitude of line motion until the line was perceived to be stationary. In so doing, they set amplitudes equal to the amplitudes of half-image motion if the gap between the patterns was narrow. They set amplitudes significantly smaller in wider gaps. Subjects made considerable fixational errors in following the oscillations of the line and the random-dot patterns. The results of the settings and of the retinal errors together refute existing rules for binocular visual direction of monocular objects. Perceived directions of monocular objects cannot be specified by geometrical rules that include only the positions of the objects and of the two eyes. The results suggest that perceived directions of monocular objects are captured by the binocular visual directions of adjacent binocular objects. Capture of binocular visual direction was found to be effective for gaps as wide as 8 deg between the binocular objects. The phenomenon of binocular capture has negative consequences for the general use of nonius lines as indicators of eye position.

Depth Perception↗

Hypometric saccades and low-gain pursuit resulting from a thalamic hemorrhage.

Saccadic and pursuit eye movements were measured in a patient with a right thalamic hemorrhage using an infrared reflection technique. Saccades were hypometric when directed away from the side of the lesion, and pursuit was low in gain, with many interposed saccades, when directed toward the side of the lesion. This eye movement pattern is similar to that observed in hemidecorticate patients. We postulate that the ocular abnormalities observed in our patients were secondary to an interruption of the efferent pathways from the right cerebral areas mediating saccadic and smooth-pursuit eye movements.

Eye Movements↗

Two- rather than three-dimensional representation of saccades in monkey superior colliculus.

Saccades are controlled by neurons in the brainstem reticular formation that receive input from the superior colliculus and cortex. Recently two quantitative models have been proposed for the role of the colliculus in the generation of three-dimensional eye movements. In order to test these models, three-dimensional eye movements were measured in the alert monkey to investigate whether the saccadic motor map of the superior colliculus is two-dimensional, representing retinal target vectors, or three-dimensional, representing three-dimensional motor error for the rotation of the eye. Electrical stimulation of the superior colliculus produced two-dimensional, not three-dimensional, eye movements. It is therefore concluded that the collicular motor map is two-dimensional.

Animals↗

Role of monkey nucleus reticularis tegmenti pontis in the stabilization of Listing's plane.

An important problem in motor control is how the nervous system deals with redundant degrees of freedom. It has been well documented that voluntary eye movements are constrained to a plane by Listing's law. Recent evidence has indicated that Listing's law is implemented downstream from the motor superior colliculus (SC), but controversy exists whether this synergy results from a neural control mechanism or from passive mechanical properties of the oculomotor plant. To address this problem, we have investigated the role of the caudal nucleus reticularis tegmenti pontis (cNRTP), which is functionally positioned inbetween the SC and cerebellar vermis, in the three-dimensional (3-D) control of saccades. In three rhesus monkeys, 3-D eye movements were measured while recording from single units in the cNRTP. In contrast to the SC, movement fields of cNRTP cells were best described by 3-D eye displacement vectors. We also performed electrical microstimulation with the eyes starting from a large range of initial eye positions. Evoked movements were always ipsilaterally directed but were often endowed with a fixed torsional component in either the positive or the negative direction. In two monkeys, small amounts of muscimol were unilaterally injected into the cNRTP. The results of these experiments strongly suggest that the cNRTP contributes to the stabilization of Listing's plane against torsional errors of the saccadic system. It is concluded, therefore, that the saccadic burst generator is 3-D, and that Listing's law is at least partially implemented by a neural control strategy.

Animals↗

ON-pathway dysfunction in a patient with acquired unilateral night blindness.

PURPOSE: To investigate possible functional correlates of an apparent ON-pathway defect observed in the cone electroretinogram of a patient with acquired unilateral night blindness. METHOD: Visual evoked potentials were recorded to the onset of a grid pattern consisting of either incremental or decremental squares. Saccadic eye movements were measured to luminance increments and decrements presented 5 degrees from fixation. The patient's results were compared with normative data. RESULTS: Visual evoked potential latencies were prolonged to incremental stimulation of the patient's affected left eye but were within normal limits for the other three conditions (increments and decrements, right eye; decrements, left eye). A similar pattern of asymmetry between latencies to incremental and decremental stimulation of the affected eye was observed for saccadic eye movements. CONCLUSIONS: The observed predominant delay in response to luminance increments supports the hypothesis of an ON-pathway dysfunction in this patient with acquired unilateral night blindness.

Adult↗

Relationship between saccadic eye movements and cortical activity as measured by fMRI: quantitative and qualitative aspects.

We investigated the quantitative relationship between saccadic activity (as reflected in frequency of occurrence and amplitude of saccades) and blood oxygenation level dependent (BOLD) changes in the cerebral cortex using functional magnetic resonance imaging (fMRI). Furthermore, we investigated quantitative changes in cortical activity associated with qualitative changes in the saccade task for comparable levels of saccadic activity. All experiments required the simultaneous acquisition of eye movement and fMRI data. For this purpose we used a new high-resolution limbus-tracking technique for recording eye movements in the magnetic resonance tomograph. In the first two experimental series we varied both frequency and amplitude of saccade stimuli (target jumps). In the third series we varied task difficulty; subjects performed either pro-saccades or anti-saccades. The brain volume investigated comprised the frontal and supplementary eye fields, parietal as well as striate cortex, and the motion sensitive area of the parieto-occipital cortex. All these regions showed saccade-related BOLD responses. The responses in these regions were highly correlated with saccade frequency, indicating that repeated processing of saccades is integrated over time in the BOLD response. In contrast, there was no comparable BOLD change with variation of saccade amplitude. This finding speaks for a topological rather than activity-dependent coding of saccade amplitudes in most cortical regions. In the experiments comparing pro- vs anti-saccades we found higher BOLD activation in the "anti" task than in the "pro" task. A comparison of saccade parameters revealed that saccade frequency and cumulative amplitude were comparable between the two tasks, whereas reaction times were longer in the "anti" task than the pro task. The latter finding is taken to indicate a more demanding cortical processing in the "anti" task than the "pro" task, which could explain the observed difference in BOLD activation. We hold that a quantitative analysis of saccade parameters (especially saccade frequency and latency) is important for the interpretation of the BOLD changes observed with visual stimuli in fMRI.

Adult↗

Cultural variation in eye movements during scene perception.

In the past decade, cultural differences in perceptual judgment and memory have been observed: Westerners attend more to focal objects, whereas East Asians attend more to contextual information. However, the underlying mechanisms for the apparent differences in cognitive processing styles have not been known. In the present study, we examined the possibility that the cultural differences arise from culturally different viewing patterns when confronted with a naturalistic scene. We measured the eye movements of American and Chinese participants while they viewed photographs with a focal object on a complex background. In fact, the Americans fixated more on focal objects than did the Chinese, and the Americans tended to look at the focal object more quickly. In addition, the Chinese made more saccades to the background than did the Americans. Thus, it appears that differences in judgment and memory may have their origins in differences in what is actually attended as people view a scene.

Adult↗

Mechanisms underlying spatial representation revealed through studies of hemispatial neglect.

The representations that mediate the coding of spatial position were examined by comparing the behavior of patients with left hemispatial neglect with that of nonneurological control subjects. To determine the spatial coordinate system(s) used to define "left" and "right," eye movements were measured for targets that appeared at 5 degrees, 10 degrees, and 15 degrees to the relative left or right defined with respect to the midline of the eyes, head, or midsaggital plane of the trunk. In the baseline condition, in which the various egocentric midlines were all aligned with the environmental midline, patients were disproportionately slower at initiating saccades to left than right targets, relative to the controls. When either the trunk or the head was rotated and the midline aligned with the most peripheral position while the eyes remained aligned with the midline of the environment, the results did not differ from the baseline condition. However, when the eyes were rotated and the midline aligned with the peripheral position, saccadic reaction time (SRT) differed significantly from the baseline, especially when the eyes were rotated to the right. These findings suggest that target position is coded relative to the current position of gaze (oculocentrically) and that this eye-centered coding is modulated by orbital position (eye-in-head signal). The findings dovetail well with results from existing neurophysiological studies and shed further light on the spatial representations mediated by the human parietal cortex.

Aged↗

Beating the beat: reading can be faster than the frequency of eye movements in persons with congenital nystagmus.

PURPOSE: Rapid serial visual presentation (RSVP) of text has been reported to foster higher reading rates than presentation in a continuous text (CT) format, possibly because scanning eye movements are minimized. We investigated how this might be relevant for persons with congenital nystagmus (CN). METHODS: We evaluated whether reading rates differ in persons with CN for RSVP versus CT presentation of single sentences under otherwise similar conditions. In a second experiment, we presented unrelated words to observers with CN in RSVP format while measuring their eye movements to determine whether reading can occur during the high-velocity, nonfoveating periods of the CN wave form. Both sentences and random words were selected from the MNRead corpus and displayed at 2x, 4x, or 8x the threshold word size on a 21-inch computer monitor. RESULTS: Subjects with CN have virtually equivalent maximum reading speeds of 449 and 448 words per minute, respectively, for RSVP and CT presentation of sentences. Typically, reading rates were faster than the frequency of CN, which suggests that subjects could read during the nonfoveating periods of the nystagmus waveform. This finding was confirmed using random words that, unlike those in sentences, cannot be inferred from contextual cues. Examination of eye movements recorded during reading indicated that random words are read correctly with 47% to 65% accuracy (depending on word size) during the nonfoveating periods of the CN waveform. CONCLUSION: A clinical implication of these results is that reading performance in persons with CN should be facilitated by large text sizes that remain legible during a greater fraction of the CN waveform.

Adolescent↗

Task-dependent modulation of the sensorimotor transformation for smooth pursuit eye movements.

To investigate the transformation of retinal image velocity into smooth pursuit eye velocity, eye movements were measured in the presence of two moving targets. In the first experiment, the targets were identical in all respects except for direction of motion, and the monkey was not cued to attend to either target. In this experiment, smooth pursuit eye velocity elicited by two targets was the vector average of the response evoked by each target alone. In subsequent experiments, we examined the effects of stimulus and task parameters on the selectivity of pursuit. When the targets were made different colors and monkeys were cued for the color of the rewarded target, their pursuit eye movements were biased in the direction of the rewarded target, but still showed a substantial influence of the nonrewarded target (distractor). It did not matter whether the same target color was used for an entire session or whether the color was randomized from trial to trial. Reducing uncertainty about the axis of motion of the rewarded target also had little effect. However, the pattern of image motion appeared to have a substantial effect; radial image motion favored averaging, and winner-take-all pursuit was found only with nonradial image motion. We conclude that the sensorimotor interface for pursuit uses a flexible decision rule that can vary continuously from vector averaging to winner-take-all. We present a simple recurrent network model that reflects this range of behavior. The model has allowed us to identify three computational elements (selection bias, competitive inhibition, and response normalization) that should be taken into consideration in future models of smooth pursuit.

Analysis of Variance↗

Hypothesized eye movements of neurolinguistic programming: a statistical artifact.

Neurolinguistic programming's hypothesized eye-movements were measured independently from videotapes of 30 subjects, aged 15 to 76 yr., who were asked to recall visual pictures, recorded audio sounds, and textural objects. chi 2 indicated that subjects' responses were significantly different from those predicted. When chi 2 comparisons were weighted by number of eye positions assigned to each modality (3 visual, 3 auditory, 1 kinesthetic), subjects' responses did not differ significantly from the expected pattern. These data indicate that the eye-movement hypothesis may represent randomly occurring rather than sensory-modality-related positions.

Adolescent↗

The role of vergence in the perception of distance: a fair test of Bishop Berkeley's claim.

Binocular eye movements were measured while subjects perceived the wallpaper illusion in order to test the claim made by Bishop Berkeley in 1709 that we perceive the distance of nearby objects by evaluating the vergence angles of our eyes. Four subjects looked through a nearby fronto-parallel array of vertical rods (28-35 cm away) as they binocularly fixated a point about 1 meter away. The wallpaper illusion was perceived under these conditions, i.e. the rods appeared farther away than their physical location. We found that although binocular fixation at an appropriate distance was needed to begin perceiving the wallpaper illusion (at least for naive observers), once established, the illusion was quite robust in the sense that it was not affected by changing vergence. No connection between the apparent localization of the rods and vergence was observed. We conclude that it is unlikely that vergence, itself, is responsible for the perceived distance shift in the wallpaper illusion, making it unlikely that vergence contributes to the perception of distance as Bishop Berkeley suggested. We found this to be true even when vergence angles were relatively large (more than 2 deg), the region in which the control of vergence eye movements has been shown to be both fast and effective.

Adult↗