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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↗

Association of abnormal smooth pursuit eye movements with the deficit syndrome in schizophrenic patients.

OBJECTIVE: The authors' goal was to test the hypothesis that abnormal smooth pursuit eye movements in schizophrenic patients are associated with the deficit syndrome. METHOD: The eye movements of 24 normal comparison subjects, 32 patients with nondeficit schizophrenia, and 11 patients with deficit schizophrenia were tested with infrared oculography using foveapetal step-ramp targets. RESULTS: The group of schizophrenic patients had normal latency to pursuit onset, abnormally decreased open-loop acceleration and abnormally decreased velocity during the periods of closed-loop acceleration and steady-state pursuit. The subgroup of schizophrenic patients with the deficit syndrome had particularly poor performance during the periods of open- and closed-loop acceleration. CONCLUSIONS: Patients with schizophrenia have abnormal smooth pursuit eye movements in response to a step-ramp stimulus, and the defects are particularly pronounced in patients with the deficit syndrome. Abnormal smooth pursuit eye movements in schizophrenia and related disorders have been consistently linked with primary and enduring negative symptoms.

Adult↗

Involuntary eye movements in response to first- and second-order motion.

We trained monkeys to maintain fixation while first- and second-order motion stimuli were displayed centrally in the visual field. Stimulus velocity, spatial frequency and contrast were varied to determine differences in patterns of involuntary eye movements elicited by random onset of stimulus motion. We observed different patterns of eye movement latency and velocity suggesting very early (< or = 100 ms) components of oculomotor activity are used to initiate smooth pursuit of object trajectory. Eye movement latency was insensitive to the complexity of stimulus motion, whereas second-order motion elicited faster eye movements than first-order motion. Instantaneous eye movement velocity might be related to the earliest stages of visual processing of component motion.

Animals↗

An information maximization model of eye movements.

We propose a sequential information maximization model as a general strategy for programming eye movements. The model reconstructs high-resolution visual information from a sequence of fixations, taking into account the fall-off in resolution from the fovea to the periphery. From this framework we get a simple rule for predicting fixation sequences: after each fixation, fixate next at the location that minimizes uncertainty (maximizes information) about the stimulus. By comparing our model performance to human eye movement data and to predictions from a saliency and random model, we demonstrate that our model is best at predicting fixation locations. Modeling additional biological constraints will improve the prediction of fixation sequences. Our results suggest that information maximization is a useful principle for programming eye movements.

Algorithms↗

A comparison of pursuit eye movement and perceptual performance in speed discrimination.

Currently there is considerable debate as to the nature of the pathways that are responsible for the perception and motor performance. We have studied the relationship between perceived speed, which is the experiential representation of a moving stimulus, and the speed of smooth pursuit eye movements, the motor action. We determined psychophysical thresholds for detecting small perturbations in the speed of moving patterns, and then by an ideal observer analysis computed analogous "oculometric" thresholds from the eye movement traces elicited by the same stimuli on the same trials. Our results confirm those of previous studies that show a remarkable agreement between perceptual judgments for speed discrimination and the fine gradations in eye movement speed. We analyzed the initial pursuit period of long duration (1000 ms) and short (200 ms) duration perturbations. When we compared the errors for perception and pursuit on a trial-by-trial basis there was no correlation between perceptual errors and eye movement errors. The observation that both oculometric and psychometric performance were similar, with Weber fractions in the normal range, but that there is no correlation in the errors suggests that the motor system and perception share the same constraints in their analysis of motion signals, but act independently and have different noise sources. We simulated noise in two models of perceptual and eye movement performance. In the first model we postulate an initial common source for the perceptual and eye movement signals. In that case about ten times the observed noise is required to produce no correlation in trial-by-trial performance. In the second model we postulate that the perceptual signal is a combination of a reafferent eye velocity signal plus the perturbation signal while the pursuit signal is derived from the oculomotor plant plus the perturbation signal. In this model about three times the noise level in the independent signals will mask any correlation due to the common perturbation signal.

Humans↗

Parametric sensitivity analysis of a homeomorphic model for saccadic and vergence eye movements.

A non-linear sixth order homeomorphic model, fitted with parameters based on eye movements and physiological data, was tuned so that it provided good simulations for the shapes of the magnitude, velocity and acceleration trajectories. Excellent quantitative agreement was obtained in terms of the Main Sequence diagrams for human eye movements. Parametric sensitivity analysis was done for a saccade of ten degree amplitude, a physiologically normal magnitude at which experimental data is both abundant and relatively noise free. Among the many useful results of this sensitivity analysis are that pulse width (PW) and pulse height (PH) were confirmed as the two controlling parameters for the human eye movement model. Output behavior was relatively insensitive to variations of the passive elements of the plant. This analysis also pointed out that more physiological data are needed to understand the role of the non-linear force-velocity relationship of the extraocular muscles.

Computers↗

Eye movements and schizophrenia in Papua New Guinea: qualitative analyses with case histories.

Smooth pursuit eye movement dysfunction is a psychophysiological and genetic marker for schizophrenia seen in 50-80% of patients and in about 40% of their first-degree relatives. In this study, we qualitatively assessed the smooth pursuit eye movements of 33 psychiatric patients (including 32 diagnosed with schizophrenia) and 30 control subjects in the Port Moresby area of Papua New Guinea. Brief case histories of each patient were also reviewed. Using a conservative estimate of smooth pursuit dysfunction, we found that 42% of the psychiatric patients had the marker, compared to 10% of the controls. Specific eye movement abnormalities were also much more common among the patients. A patient who had previously 'run amok' and another who was a cargo cultist had smooth pursuit dysfunction; a patient whose psychotic symptoms may have been due to cerebral malaria did not have the marker. Highland and coastal patients were similar in their expression of the marker. This study, the first of its kind done outside of large-scale, urbanized societies, provides further evidence for a common biological basis for schizophrenia in biologically and culturally diverse populations worldwide.

Acute Disease↗

Saccadic eye movements in tracking, fixation, and rest in schizophrenic and normal subjects.

Horizontal eye movements were recorded electrooculographically during two different eye fixation tasks, during an eyes-closed waking state, and during eye tracking on a sinusoidally moving target in 16 chronic schizophrenics and in 12 normal subjects. The relationship between saccadic eye movements during tracking and in the other experimental situations was investigated. The intensities of eye fixation were successively decreased from Experiment I (eye fixation on a stationary target) through Experiment II (eye fixation on an imagined spot in the dark) to Experiment III (eyes closed in the dark, no cue for eye fixation), in that order. The frequency of saccades increased as the intensities of fixation decreased from Experiment I to Experiment III in both schizophrenic and normal groups. It was demonstrated that the frequency of saccades was higher in schizophrenics than in normal subjects in all of the experimental conditions. Some correlations were found between the increased frequency of saccades seen during eye tracking and the similar increases seen in eyes-fixated or eyes-closed states in schizophrenic subjects. It is suggested that the increased saccades seen during eye tracking and in other experimental conditions in schizophrenics are related to a deficit of nonvoluntary attention, due to a failure of an inhibitory mechanism.

Adult↗

Fast eye movement initiation of ocular torsion in mesodiencephalic lesions.

Three patients with episodic ocular torsion and skew deviation due to mesodiencephalic lesions were studied by using binocular three-dimensional scleral search coils. The conjugate ocular torsion (upper pole of each eye rotating toward the side of the brainstem lesion) was initiated by a torsional fast eye movement. During prolonged episodes, torsional nystagmus was also present. Cessation of the ocular torsion and skew deviation occurred by slow eye movements with exponentially decreasing velocities in 2 patients, and by multiple fast torsional movements in 1 patient. In 1 patient, the abnormal eye movements were temporally linked to dystonic movements in the limbs on the side opposite the brainstem lesion. The occurrence of skew deviation with conjugate ocular torsion in brainstem lesions has been attributed to functional asymmetry in vestibular pathways responsible for the slow-phase compensatory eye movement response to roll. In comparison, the findings in our patients show that in mesodiencephalic lesions conjugate ocular torsion with skew deviation may be generated by torsional fast eye movements, indicating activation of the burst cells of the rostral interstitial nucleus of the medial longitudinal fasciculus.

Adult↗

Smooth pursuit eye movements in dementia of the Alzheimer type.

Smooth pursuit eye movements (SPEM) to a sinusoidally modulated target moving horizontally across a cathode ray tube screen were examined for 17 patients with dementia of the Alzheimer type (DAT) and for 14 age-matched control subjects. There were 3 target-motion conditions at frequencies representing varying ranges of target velocity. DAT patients differed from controls on all measures of smooth pursuit quality: their gain was reduced at high target velocities and lower target accelerations, they made more frequent directionally appropriate saccades and had more saccadic intrusions, they led the target with their eyes (phase lead) in all 3 conditions, and lag-adjusted cross-correlation coefficients, computed between digitized eye-movement and target signals, were lower among patients. The cross-correlation measure was most sensitive to between-group variability. These results suggest that the impaired SPEM observed in DAT patients reflect degeneration of cortical oculomotor centers, either through inappropriate saccadic intrusions in smooth pursuit as a result of physiologic disinhibition or through effects on attentional processes or both.

Acceleration↗

Commentary: eye movement research with clinical populations.

The preceding set of chapters span the disciplines of neurology and psychiatry, and provide a diverse introduction to clinical eye movement research. They illustrate how oculomotor paradigms can be used to learn about acute and chronic perturbations in brain function, disturbances in brain development, disturbances in sensorimotor as well as cognitive systems, and the effects of therapeutic and illicit drugs on brain function. This commentary discusses these contributions, provides an overview of broad methodological issues involved in applying eye movement studies to psychiatric populations using the antisaccade task as an exemplar, and considers the potential of collaborations between eye movement and brain imaging researchers to advance understanding of clinical eye movement abnormalities and of what they reveal about the organization of the oculomotor system.

Brain↗

Lateral asymmetry of eye movements in temporal lobe epileptic patients with unilateral foci.

Eye movements in response to visual stimuli (Benton Visual Retention Test) were examined in 22 temporal lobe epileptics (TLEs), 10 primary generalized epileptics (PGEs), and 20 normal controls. In the normal controls, the percent fixation time on the left peripheral figure was higher than that on the right peripheral figure, a tendency also found in the PGEs. In TLEs with right-sided foci, the percent fixation time on the left peripheral figure was higher than that on the right peripheral figure, the direction of asymmetry found in the normal controls and PGEs. However, when calculated as laterality indices (the degree of asymmetry) TLEs with right-sided foci were significantly more negative than those of both the normal controls and PGEs. In TLEs with left sided foci, the percent fixation time on the right peripheral figure tended to be higher than that on the left peripheral figure, an asymmetry which differed significantly from the normal controls, PGEs and the TLEs with right-sided foci. The results here showed that TLEs with unilateral foci had distinct eye movements which varied with the laterality of the lesion in the direction of functional overactivation of the epileptogenic hemisphere.

Epilepsy, Generalized↗

Smooth pursuit eye movement deficits after pontine nuclei lesions in humans.

Eye movements were recorded electroculographically in four patients with basal pontine lesions, demonstrated by MRI. The most prominent eye movement abnormality observed was mild to severe impairment of smooth pursuit and optokinetic nystagmus, mainly ipsilateral to the lesion. This abnormality is thought to result from damage to the pontine nuclei, which form a crucial relay between the cerebral cortex and the cerebellum controlling smooth pursuit. Abnormalities of saccades and the vestibulo-ocular reflex in one patient are also discussed.

Adult↗

Eye movements and reading with large print and optical magnifiers in macular disease.

PURPOSE: Reading rate has been the main performance measure in studies that have compared reading with large print and optical magnifiers; eye movement characteristics have not been considered. We compared both eye movement characteristics and reading rates for subjects with macular disease reading without and with a range of low-vision devices. METHODS: Silent reading rate and eye movement characteristics for text passages at critical print size of 21 subjects aged 14 to 88 years with macular disease were measured with and without their preferred low-vision device. Saccadic frequency was determined from a sequencing task comprising five letters each separated by 5 degrees. Eye movements were recorded using an infrared limbal reflection system. RESULTS: There were no significant differences in reading rate, fixation durations, saccade numbers per word, or percent retrace time when using a low-vision device compared with reading without a low-vision device. The percentage of regressions was, however, lower with the low-vision device. Saccadic frequency in the sequencing task was predictive of reading performance with and without a low-vision device. CONCLUSIONS: When reading at critical print size, in terms of reading rate or saccades per word, there was no advantage to using large print over an optical low-vision device.

Adolescent↗

Rapid eye movements in REM sleep--more evidence for a periodic organization.

Density scores of horizontal eye movements during 70 REM sleep periods of normal young adults and combat neurotic patients were subjected to spectral analysis. The results showed that in 58% of all REM periods, spectral peaks occurred at either 0.1 c/min or 0.05 c/min. The percentages of spectral peaks at these frequencies were equal in both groups. Since the estimated variance at these frequencies was significantly higher than the estimated variance at the adjacent frequencies and the mean variance at the rest of the spectra, it was concluded that eye movements in REM sleep tend to cluster every 10-20 min. These results and findings on the neural control of REM ocular activity suggest that REMs in sleep are generated by at least 3 generators: a burst generator, an isolated eye movement generator, and a 10-20 min periodic generator.

Adult↗

Asynchronism of saccadic eye movement in young diabetics as related to HbAIc.

The saccadic eye movements of young diabetic subjects (type I) were analyzed with respect to their synchronism (30 degrees gaze jumps). Regarding the duration (end) of saccadic eye movements, it was found that in diabetics (n = 41) the asymmetry between both eyes (less than or equal to 35 ms) is appreciably more than in normal individuals of equivalent age (n = 25; less than or equal to 10 ms). The asynchronism described is closely correlated with the hemoglobin AIc concentration in the blood.

Brain Diseases↗

Neural control of vergence eye movements: neurons encoding vergence velocity.

Single-unit recordings were made from midbrain areas in monkeys trained to make both conjugate and disjunctive (vergence) eye movements. Previous work had identified cells with a firing rate proportional to the vergence angle, without regard to the direction of conjugate gaze. The present study describes the activity of neurons that burst for disjunctive eye movements. Convergence burst cells display a discrete burst of activity just before and during convergence eye movements. For most of these cells, the profile of the burst is correlated with instantaneous vergence velocity and the number of spikes in the burst is correlated with the size of the vergence movement. Some of these cells also have a tonic firing rate that is positively correlated with vergence angle (convergence burst-tonic cells). Divergence burst cells have similar properties, except that they fire for divergent and not convergent movements. Divergence burst cells are encountered far less often than convergence burst cells. Both convergence and divergence burst cells were found in an area of the mesencephalic reticular formation just dorsal and lateral to the oculomotor nucleus. Convergence burst cells were also recorded in another more dorsal mesencephalic region, rostral to the superior colliculus. Both of the areas also contain cells that encode vergence angle. Models of the vergence system derived from psychophysical data imply the existence of a vergence integrator, the output of which is vergence angle. Some models also suggest the presence of a parallel element that improves the frequency response of the vergence system, but has no effect on the steady-state behavior of the system. Vergence burst cells would be suitable inputs to a vergence integrator. By providing a vergence velocity signal to motoneurons, they may improve the dynamic response of the vergence system. The behavior of vergence burst cells during vergence movements is similar to that of the medium-lead burst cells during saccades. The proposed roles for vergence velocity cells are analogous to those of the saccadic burst cells. In this respect, the neural organization of the vergence system resembles that of the saccadic system, despite the distinct difference in the kinematics of these two types of eye movements.

Action Potentials↗

Influence of eye movements on Rett stereotypies: evidence suggesting a stage-specific regression.

The influence of eye movements on hand use and pervasive stereotypies in Rett syndrome was studied, to better understand the developmental abnormality in this disorder. Nine patients in the post-regression phase were offered objects. As expected, the girls looked at the objects but usually did not reach for them. Nor were their characteristic hand stereotypies altered by such looking. But the occurrence of stereotypies was promoted by overall shifts in gaze, ie, eye movements in any direction. This finding may be relevant to the late-infancy loss of voluntary hand use in Rett syndrome associated with onset of pervasive stereotypies. It suggests a stage-specific regression to a level characteristic of normal 3-month-old infants who do not reach and grasp, but whose hand clasping and mouthing may be triggered by the perceptual consequences of exploratory eye movements and shifts in gaze.

Adolescent↗