Repetitive Saccades Research Articles

Oculomotor fatigability with decrements of saccade and smooth pursuit for diagnosis of myasthenia gravis

Background and objectivesAs the efficacy of current diagnostic methods for myasthenia gravis (MG) remains suboptimal, there is ongoing interest in developing more effective diagnostic models. As oculomotor fatigability is one of the most common and diagnostic symptoms in MG, we aimed to investigate whether quantitative saccadic and smooth-pursuit fatigability analyses with video-oculography (VOG) are useful for diagnosis of MG.MethodsA convenience cohort of 46 MG patients was recruited prospectively, including 35 with ocular and 11 with generalized MG (mean age, 50.9 ± 14.5 years; 17 females); 24 healthy controls (HCs) (mean age, 50.6 ± 16.3 years; 13 females) also were enrolled. Seventy-five repetitive saccades and smooth pursuits were recorded in ranges of 20° (horizontal plane) and 15° (vertical plane) using a three-dimensional VOG system. Based on the oculomotor range of the second saccade and smooth pursuit and the mean ranges of the last five of each, the estimated decrements (%) reflecting oculomotor fatigability were calculated.ResultsThe baseline oculomotor ranges did not show significant difference between the MG and HCs groups. However, following repetitive saccades and pursuits, the oculomotor ranges were decreased substantially during the last five cycles compared to baseline in the MG group. No such decrements were observed in the HC group (p < 0.01, Mann–Whitney U test). Receiver operating characteristic (ROC) analysis revealed that repetitive vertical saccades yielded the best differentiation between the MG and HC groups, with a sensitivity of 78.3% and specificity of 95.8% when using a decrement with an amplitude of 6.4% as the cutoff.ConclusionThis study presents an objective and reproducible method for measuring decrements of oculomotor ranges after repetitive saccadic and pursuit movements. Quantification of oculomotor fatigability using VOG could be a sensitive and specific diagnostic tool for MG and allows easy, cost-effective, accurate, and non-invasive measurements.Classification of evidenceThis study provides class III evidence that VOG-based quantification of saccadic and pursuit fatigability accurately identifies patients with MG.

The King-Devick test in an outpatient concussion clinic: Assessing the diagnostic and prognostic value of a vision test in conjunction with exercise testing among acutely concussed adolescents

ObjectiveThis study investigated the diagnostic and prognostic value of the King-Devick (K-D) test in conjunction with treadmill testing in adolescents after sport-related concussion (SRC) in an outpatient concussion management clinic without baseline measures. DesignProspective cohort. MethodsThe K-D test was administered pre- and post-exercise on a graded treadmill test to acutely concussed (AC, <10 days from injury, n = 46, 15.4 ± 2.1 years) participants for 2 clinic visits (1 week apart) and to matched controls (MC, n = 30, 15.8 ± 1.4 years) for 2 visits (1 week apart). Initial K-D test times were compared between MC and AC. Changes in times from pre- to post- exercise during a treadmill test were compared for MC and AC and from Visit 1 to Visit 2. Smooth pursuits and repetitive saccades were compared with initial visit K-D test performance. ResultsComparison of pre-exercise K-D test times at Visit 1 distinguished MC from AC (46.1 ± 9.2 s vs. 53.7 ± 13.0 s, p = .007). Comparison of pre- and post-exercise K-D test times revealed significant improvements for MC (46.1 ± 9.2 s vs. 43.1 ± 8.5 s, p < .001) and AC who recovered by Visit 2 (Fast Recovery Group [FRG], n = 23, 50.4 ± 10.0 s vs. 47.3 ± 9.8 s, p = .002). No significant difference was seen in pre- and post-exercise K-D test times on Visit 1 for AC who took longer than 2 weeks to recover (Slow Recovery Group [SRG], n = 23, 57.0 ± 15.0 s vs. 56.0 ± 16.3 s, p = .478). At Visit 1, AC had more abnormal smooth pursuits than MC (17% vs. 3%, non-significant, p = .064). AC, however, had significantly more abnormal repetitive saccades than MC (37% vs. 3%, p = .001) and AC with abnormal repetitive saccades took significantly longer to complete the Visit 1 pre-exercise K-D test than AC with normal repetitive saccades (58.6 ± 16.0 s vs 50.8 ± 10.2 s, p = .049). ConclusionThe study supports utility of the K-D test as part of outpatient concussion assessment. Lack of improvement in K-D test performance after an exercise test may be an indicator of delayed recovery from SRC.

Saccades and handedness interact to affect scene memory.

Repetitive saccades benefit memory when executed before retrieval, with greatest effects for episodic memory in consistent-handers. Questions remain including how saccades affect scene memory, an important visual component of episodic memory. The present study tested how repetitive saccades affect working and recognition memory for novel scenes. Handedness direction (left–right) and degree (strong/consistent vs. mixed/inconsistent) was measured by raw and absolute laterality quotients respectively from an 8-question handedness inventory completed by 111 adults. Each then performed either 30 s of repetitive horizontal saccades or fixation before or after tasks of scene working memory and scene recognition. Regression with criterion variables of overall percent correct accuracy and d-prime sensitivity showed that when saccades were made before working memory, there was better overall accuracy as a function of increased direction but not degree of handedness. Subjects who made saccades before working memory also performed worse during subsequent recognition memory, while subjects who fixated or made saccades after the working memory task performed better. Saccades made before recognition resulted in recognition accuracy that was better (Cohen’s d = 0.3729), but not significantly different from fixation before recognition. The results demonstrate saccades and handedness interact to affect scene memory with larger effects on encoding than recognition. Saccades before scene encoding in working memory are detrimental to short- and long-term memory, especially for those who are not consistently right-handed, while saccade execution before scene recognition does not appear to benefit recognition accuracy. The findings are discussed with respect to theories of interhemispheric interaction and control of visuospatial attention.

Gaze-dependent phoria and vergence adaptation

Incomitance is a condition with gaze-dependent deviations of ocular alignment and is common in strabismus patients. The physiological mechanisms that maintain equal horizontal ocular alignment in all gaze directions (concomitance) in healthy individuals are poorly explored. We investigate adaptive processes in the vergence system that are induced by horizontal incomitant vergence stimuli (stimuli that require a gaze-dependent vergence response in order to re-establish binocular single vision). We measured horizontal vergence responses elicited after healthy subjects shifted their gaze from a position that required no vergence to a position that required convergence. Repetitive saccades into a position with a convergence stimulus rapidly decreased phoria (defined as the deviation of ocular alignment in the absence of a binocular stimulus). This change of phoria was present in all viewing directions (from 0° to 0.86° ± 0.40°, p < 0.001) but was more pronounced in the gaze direction with a convergence stimulus (from 0.26° ± 0.13° to 1.39° ± 0.33°, p < 0.001). We also found that vergence velocity rapidly increased (p = 0.015) and vergence latency promptly decreased (p < 0.001). We found gaze-dependent modulation of phoria in combined saccade-vergence eye movements and also in pursuit-vergence eye movements. Thus, acute horizontal, gaze-dependent changes of vergence, such as may be encountered in new onset strabismus due to paralysis, can rapidly increase vergence velocity and decrease latency. Gaze-specific (concomitant) and gaze-independent (incomitant) phoria levels will adapt. These early adaptive processes increase the efficacy of binocular vision and maintain good ocular alignment in all directions of gaze.

Gaze Dependent Vergence Adaptation

PURPOSE The innervational pattern of extraocular muscles that maintain ocular alignment vary with gaze direction, age, and orbital anatomy. A muscle paresis, for example, may cause a misalignment, which is characterized by a gaze dependent deviation of the ocular alignment. Clinically this is termed incomitant strabismus. In this study we aimed at investigating the physiological mechanisms that enable orthophoria, i.e. good ocular alignment, in all directions of gaze. For this purpose we explored the physiological response to vergence stimuli and assessed their directional specificity. METHODS Vergence stimuli of gaze dependent magnitude were used to model image disparity of an incomitant, 'paretic', strabismus. We measured consecutive horizontal vergence responses that were elicited after subjects shifted their gaze from a gaze position without image disparity into a field of view with increased image disparity. RESULTS We found that repetitive saccades into a field of view with increased image disparity led to a rapid decrease of the phoria level, i.e. the magnitude of ocular misalignment in optically dissociated eyes decreased over time. The decrease was more pronounced in the gaze direction with increased disparity and to a lesser extent in the other gaze directions. Moreover, we confirmed a rapid increase of the vergence velocity over time. The gaze dependent modulation of phoria was found in both, smooth pursuit and saccadic eye movements. CONCLUSION Thus an acute gaze dependent change of image disparity, such as may be encountered in new onset paretic strabismus, leads to an increased velocity of the vergence response and an increase of the phoria level with a gaze specific and a gaze independent component. This early adaptive response enables an increased efficacy of binocular vision and an orthophorisation in all directions of gaze in a case of a new onset incomitance. Meeting abstract presented at VSS 2015.

Rotating Snakes Illusion - Quantitative analysis reveals islands in luminance space with opposite illusory rotation

The "Rotating Snakes" illusion is based on patterns with repeated asymmetric luminance steps, arranged in concentric bands forming a "snake wheel". In the underlying luminance sequence "black – darker grey (g1) – white – lighter grey (g2)" we varied the luminances of g1 and g2, and measured illusion strength via a nulling task: On a gamma-corrected VDU, repetitive saccades were performed passing a "snake wheel" that physically rotated, and the participants adjusted rotation direction and speed until a stationary percept obtained. We found that our participants performed perceptual nulling (in the range of ± 1°/s) of the seeming rotation quite reliably and convincingly; when the gaze was directed to the center of the wheel after null-adjustment, the actual rotation could be quite surprising (depending on the levels [g1, g2]). Typical settings for [g1, g2] as measured from images by A. Kitaoka, are around [20%, 60%]. Indeed, we found a marked illusion in an "island" region [g1≈{0–25%}, g2≈{20–75%}]. Unexpectedly, we detected a second island around [60%, 90%] with opposite rotation direction, although the relative order of g1 and g2 stayed the same. Furthermore, there was also some rotation illusion when altogether only 3 luminance levels were visible, e.g.: 0–0–50–100%. These quantitative measurements of illusion strength have revealed new phenomena in this illusion, which challenge the two explanatory models put forth so far. Meeting abstract presented at VSS 2014

Cross-frequency interaction of the eye-movement related LFP signals in V1 of freely viewing monkeys

Recent studies have emphasized the functional role of neuronal activity underlying oscillatory local field potential (LFP) signals during visual processing in natural conditions. While functionally relevant components in multiple frequency bands have been reported, little is known about whether and how these components interact with each other across the dominant frequency bands. We examined this phenomenon in LFP signals obtained from the primary visual cortex of monkeys performing voluntary saccadic eye movements (EMs) on still images of natural-scenes. We identified saccade-related changes in respect to power and phase in four dominant frequency bands: delta-theta (2–4 Hz), alpha-beta (10–13 Hz), low-gamma (20–40 Hz), and high-gamma (>100 Hz). The phase of the delta-theta band component is found to be entrained to the rhythm of the repetitive saccades, while an increment in the power of the alpha-beta and low-gamma bands were locked to the onset of saccades. The degree of the power modulation in these frequency bands is positively correlated with the degree of the phase-locking of the delta-theta oscillations to EMs. These results suggest the presence of cross-frequency interactions in the form of phase-amplitude coupling (PAC) between slow (delta-theta) and faster (alpha-beta and low gamma) oscillations. As shown previously, spikes evoked by visual fixations during free viewing are phase-locked to the fast oscillations. Thus, signals of different types and at different temporal scales are nested to each other during natural viewing. Such cross-frequency interaction may provide a general mechanism to coordinate sensory processing on a fast time scale and motor behavior on a slower time scale during active sensing.

Visual feature binding in early infancy.

How does the developing brain of the human infant solve the feature-binding problem when visual stimuli consisting of multiple colored objects are presented? A habituation--dishabituation procedure revealed that 1-month-old infants have the ability to discriminate changes in the conjunction of a familiar shape and color in two objects. However, this good earlier performance was followed by poorer performance at 2 months of age. The performance improved again at 3 months of age. Detailed analysis of the oculomotor behaviors revealed that the age of 2 months was a period of drastic transition when the tendency to stay with the fixated objects disappeared and repetitive saccades between the two objects emerged. Our findings suggest that the ability to perceive conjunctions of features is available to infants very early, that the perceptual/neural basis at 1 and at 3 months of age may be fundamentally different, and that feature integration by vigorous eye movements or selective attention may be the key functional difference between the age groups.

The influence of repetitive eye movements on vergence performance

We measured the peak velocity of convergence eye movement responses in four normal subjects before and after a large number of either repetitive vergence or repetitive saccadic eye movements. A 20% decrease in the mean value of peak velocity was observed in vergence responses after 100 repetitive step vergence eye movements. However, 100 cycles of slow sinusoidal vergence tracking did not induce any notable change in vergence dynamics. Five hundred repetitive saccadic eye movements also caused an approximately 20% decrease in peak velocity. The reduction in peak velocity was related to the number of repetitions for both vergence and saccadic fatiguing stimuli. The frequency of occurrence of double-vergences was also used as an index to monitor the influence of repetitive eye movements on convergence performance. Results showed that repetitive step convergence movements could double, or even triple, the frequency of the occurrence of double-vergence responses, while slow sinusoidal vergence tracking or repetitive saccades had no influence on the frequency of response doubles.

Saccadic Dysmetria and Adaptation after Lesions of the Cerebellar Cortex

We studied the effects of small lesions of the oculomotor vermis of the cerebellar cortex on the ability of monkeys to execute and adapt saccadic eye movements. For saccades in one horizontal direction, the lesions led to an initial gross hypometria and a permanent abolition of the capacity for rapid adaptation. Mean saccade amplitude recovered from the initial hypometria, although variability remained high. A series of hundreds of repetitive saccades in the same direction resulted in gradual decrement of amplitude. Saccades in other directions were less strongly affected by the lesions. We suggest the following. (1) The cerebellar cortex is constantly recalibrating the saccadic system, thus compensating for rapid biomechanical changes such as might be caused by muscle fatigue. (2) A mechanism capable of slow recovery from dysmetria is revealed despite the permanent absence of rapid adaptation.

Disconjugate adaptation of saccades: contribution of binocular and monocular mechanisms

We studied the effects of prism–induced disparity on static and intrasaccadic alignment in six normal human subjects. A ten diopter base–out prism, calling for convergence, was placed in front of the central field of the right eye, so that at the center the eye viewed through the prism; at left and right, outside the prism. During 15 min of training, subjects made repetitive saccades solely in the right field of vision (C-R-C sequence). This paradigm required relative divergence for centrifugal (C-R) saccades and relative convergence for centripetal (R-C) saccades, as well as increase of the amplitude for all saccades made by the right eye. We found that during training, all subjects incorporated the necessary change in alignment into the saccades. After training the resultant intrasaccadic disconjugacy persisted when tested during monocular viewing, indicating that motor learning had occurred. Subjects demonstrated increased divergence for C-R and increased convergence for R-C saccades, in accordance with the change acquired during adaptation to the prism. In addition, five subjects developed increased divergence for C-L saccades, for which they did not train. Smaller and less consistent divergence was also observed for L-C saccades. Changes in intrasaccadic alignment were accompanied by changes in the relative velocities of the two eyes’ saccades and slowing of the peak velocities in both eyes during training. Static alignment showed a general tendency toward convergence that did not parallel the changes in the intrasaccadic alignment, suggesting that saccade adaptation is system–specific. The pattern of transfer of the intrasaccadic disconjugacy to saccades in the untrained field and the changes in the relative speeds of the two eyes cannot be explained by monocular adjustment of the saccades. Our results indicate that both a binocular mechanism—saccade–vergence interaction—and monocular adaptation contribute to disconjugate adaptation of saccades.

Infants' acquisition of spatiotemporal expectations.

The microdevelopment of infants' visual expectations was examined by analysis of the eye movements that 80 three-month-old human infants made during interstimulus intervals (ISIs) of an alternating picture sequence. For comparison, identical eye movement data were gathered from 10 infants who watched an irregular sequence. Shifts during ISIs were exhibited by all infants and occurred on 48% of all trials. Initially, infants' ISI shifts repeated saccades that had successfully located the preceding picture; during the course of the alternating session, repetitive saccades declined while alternating and anticipatory saccades increased. For infants who saw the irregular sequence, the frequency of ISI shifts did not vary systematically over trials. Analysis of saccade latencies suggested that infants quickly learned to inhibit a prepotent tendency in order to execute task-appropriate saccades.