Ewa Niechwiej-Szwedo

Eye Position Stability in Amblyopia and in Normal Binocular Vision

PURPOSE We investigated whether the sensory impairments of amblyopia are associated with a decrease in eye position stability (PS). METHODS The positions of both eyes were recorded simultaneously in three viewing conditions: binocular, monocular fellow eye viewing (right eye for controls), and monocular amblyopic eye viewing (left eye for controls). For monocular conditions, movements of the covered eye were also recorded (open-loop testing). Bivariate contour ellipses (BCEAs), representing the region over which eye positions were found 68.2% of the time, were calculated and normalized by log transformation. RESULTS For controls, there were no differences between eyes. Binocular PS (log(10)BCEA = -0.88) was better than monocular PS (log(10)BCEA = -0.59) indicating binocular summation, and the PS of the viewing eye was better than that of the covered eye (log(10)BCEA = -0.33). For patients, the amblyopic eye exhibited a significant decrease in PS during amblyopic eye (log(10)BCEA = -0.20), fellow eye (log(10)BCEA = 0.0004), and binocular (log(10)BCEA = -0.44) viewing. The PS of the fellow eye depended on viewing condition: it was comparable to controls during binocular (log(10)BCEA = -0.77) and fellow eye viewing (log(10)BCEA = -0.52), but it decreased during amblyopic eye viewing (log(10)BCEA = 0.08). Patients exhibited binocular summation during fellow eye viewing, but not during amblyopic eye viewing. Decrease in PS in patients was mainly due to slow eye drifts. CONCLUSIONS Deficits in spatiotemporal vision in amblyopia are associated with poor PS. PS of amblyopic and fellow eyes is differentially affected depending on viewing condition.

Effects of anisometropic amblyopia on visuomotor behavior, I: saccadic eye movements.

PURPOSE Impairment of spatiotemporal visual processing is the hallmark of amblyopia, but its effects on eye movements during visuomotor tasks have rarely been studied. Here the authors investigate how visual deficits in anisometropic amblyopia affect saccadic eye movements. METHODS Thirteen patients with anisometropic amblyopia and 13 control subjects participated. Participants executed saccades and manual reaching movements to a target presented randomly 5° or 10° to the left or right of fixation in three viewing conditions: binocular, amblyopic, and fellow eye viewing. Latency, amplitude, and peak velocity of primary and corrective saccades were measured. RESULTS Initiation of primary saccades was delayed and more variable when patients viewed monocularly with their amblyopic eye. During binocular viewing, saccadic latency exhibited increased variability and no binocular advantage in patients (i.e., mean latency was similar to that during fellow eye viewing). Mean amplitude and peak velocity of primary saccades were comparable between patients and control subjects; however, patients exhibited greater variability in saccade amplitude. The frequency of corrective saccades was greater when patients viewed with their fellow eye than it was with binocular or amblyopic eye viewing. Latency, amplitude, and peak velocity of corrective saccades in patients were normal in all viewing conditions. CONCLUSIONS Saccades had longer latency and decreased precision in amblyopia. Once saccades were initiated, however, the dynamics of saccades were not altered. These findings suggest that amblyopia is associated with slower visual processing in the afferent (sensory) pathway rather than a deficit in the efferent (motor) pathway of the saccadic system.

Effects of Anisometropic Amblyopia on Visuomotor Behavior, III: Temporal Eye-Hand Coordination during Reaching

PURPOSE To examine the effects of anisometropic amblyopia on the temporal pattern of eye-hand coordination during visually-guided reaching. METHODS Eighteen patients with anisometropic amblyopia and 18 control subjects were recruited. Participants executed reach-to-touch movements toward visual targets under three viewing conditions: binocular, monocular amblyopic eye, and monocular fellow eye viewing. Temporal coordination between eye and hand movements was examined during reach planning (interval between the initiation of saccade and reaching) and reach execution (interval between the initiation of saccade and reach peak velocity). The frequency and dynamics of secondary saccades were also examined. RESULTS Patients with severe amblyopia spent a longer time planning the reaching response after fixating the target in comparison with control subjects and patients with mild amblyopia (P = 0.029). In comparison with control subjects, all patients extended the acceleration phase of the reach after target fixation (P = 0.018). Secondary (reach-related) saccades were initiated during the acceleration phase of the reach and patients executed these saccades with greater frequency than control subjects (P < 0.0001). The amplitude and peak velocity of reach-related saccades were higher when patients viewed with the amblyopic eye in comparison with the other viewing conditions (P < 0.001). CONCLUSIONS This is the first study to show that patients with anisometropic amblyopia modified the temporal dynamics of eye-hand coordination during visually-guided reaching. They extended the planning and execution intervals after target fixation and increased the frequency of secondary, reach-related saccades. These may represent visuomotor strategies to compensate for the spatiotemporal visual deficits to achieve good reaching accuracy and precision.

Effects of Strabismic Amblyopia and Strabismus without Amblyopia on Visuomotor Behavior, I: Saccadic Eye Movements

PURPOSE It has previously been shown that anisometropic amblyopia affects the programming and execution of saccades. The aim of the current study was to investigate the impact of strabismic amblyopia on saccade performance. METHODS Fourteen adults with strabismic amblyopia, 13 adults with strabismus without amblyopia, and 14 visually normal adults performed saccades and reach-to-touch movements to targets presented at ± 5° and ± 10° eccentricity during binocular and monocular viewing. Latency, amplitude, and peak velocity of primary and secondary saccades were measured. RESULTS In contrast to visually normal participants who had shorter primary saccade latency during binocular viewing, no binocular advantage was found in patients with strabismus with or without amblyopia. Patients with amblyopia had longer saccade latency during amblyopic eye viewing (P < 0.0001); however, there were no significant differences in saccade amplitude precision among the three groups across viewing conditions. Further analysis showed that only patients with severe amblyopia and no stereopsis (n = 4) exhibited longer latency (which was more pronounced for more central targets; P < 0.0001), and they also had reduced amplitude precision during amblyopic eye viewing. In contrast, patients with mild amblyopia (n = 5) and no stereopsis had normal latency and reduced precision during amblyopic eye viewing (P < 0.001), whereas those with gross stereopsis (n = 5) had normal latency and precision. There were no differences in peak velocity among the groups. CONCLUSIONS Distinct patterns of saccade performance according to different levels of visual acuity and stereoscopic losses in strabismic amblyopia were found. These findings were in contrast to those in anisometropic amblyopia in which the altered saccade performance was independent of the extent of visual acuity or stereoscopic deficits. These results were most likely due to different long-term sensory suppression mechanisms in strabismic versus anisometropic amblyopia.

The Effect of Sensory Uncertainty Due to Amblyopia (Lazy Eye) on the Planning and Execution of Visually-Guided 3D Reaching Movements

Background Impairment of spatiotemporal visual processing in amblyopia has been studied extensively, but its effects on visuomotor tasks have rarely been examined. Here, we investigate how visual deficits in amblyopia affect motor planning and online control of visually-guided, unconstrained reaching movements. Methods Thirteen patients with mild amblyopia, 13 with severe amblyopia and 13 visually-normal participants were recruited. Participants reached and touched a visual target during binocular and monocular viewing. Motor planning was assessed by examining spatial variability of the trajectory at 50–100 ms after movement onset. Online control was assessed by examining the endpoint variability and by calculating the coefficient of determination (R2) which correlates the spatial position of the limb during the movement to endpoint position. Results Patients with amblyopia had reduced precision of the motor plan in all viewing conditions as evidenced by increased variability of the reach early in the trajectory. Endpoint precision was comparable between patients with mild amblyopia and control participants. Patients with severe amblyopia had reduced endpoint precision along azimuth and elevation during amblyopic eye viewing only, and along the depth axis in all viewing conditions. In addition, they had significantly higher R2 values at 70% of movement time along the elevation and depth axes during amblyopic eye viewing. Conclusion Sensory uncertainty due to amblyopia leads to reduced precision of the motor plan. The ability to implement online corrections depends on the severity of the visual deficit, viewing condition, and the axis of the reaching movement. Patients with mild amblyopia used online control effectively to compensate for the reduced precision of the motor plan. In contrast, patients with severe amblyopia were not able to use online control as effectively to amend the limb trajectory especially along the depth axis, which could be due to their abnormal stereopsis.

Effects of induced monocular blur versus anisometropic amblyopia on saccades, reaching, and eye-hand coordination.

PURPOSE We previously showed that anisometropic amblyopia affects the programming and execution of saccades and reaching movements. In our current study, we investigated whether these amblyopia-related changes simply are due to a reduction in visual acuity alone by inducing artificial blur in one eye in visually-normal participants. METHODS Twelve visually-normal participants performed saccades and reach-to-touch movements to targets presented on a computer screen during binocular and monocular viewing. A contact lens was used to blur the vision of one eye to a mean acuity level of 20/50. Saccades and reaching kinematics were compared before blur, immediately after blur, and 5 hours after blur was induced. The 5 hours after blur kinematic data from visually-normal participants also were compared to those from 12 patients with anisometropic amblyopia who had comparable acuity in the amblyopic eye. RESULTS Primary saccades (latency, amplitude, peak velocity), reaching movements (reaction time, movement time, peak acceleration, duration of the acceleration phase), and eye-hand coordination (saccade-to-reach planning interval, saccade-to-reach peak velocity interval) were not affected by induced monocular blur in visually-normal participants, either immediately or 5 hours after blur. Compared to visually-normal participants after 5 hours of blur, patients with anisometropic amblyopia had significantly longer and more variable saccade latency during amblyopic eye viewing, lower peak acceleration, and a longer acceleration phase during reaching, and a different temporal pattern of eye-hand coordination. CONCLUSIONS Artificially-induced monocular blur in visually-normal participants did not affect saccades, reaching movements, and eye-hand coordination during a simple reach-to-touch task even after a period of blur exposure. In contrast, patients with anisometropic amblyopia demonstrated significantly different kinematics while performing the same task. These results indicate that loss of visual acuity alone cannot explain the kinematic changes seen in patients with mild anisometropic amblyopia.

Effects of Strabismic Amblyopia on Visuomotor Behavior: Part II. Visually Guided Reaching

PURPOSE To examine the effects of impaired spatiotemporal vision on reaching movements in participants with strabismic amblyopia and to compare their performance to those with strabismus only without amblyopia and to visually normal participants. METHODS Sixteen adults with strabismic amblyopia, 14 adults with strabismus only, and 16 visually normal adults were recruited. Participants executed reach-to-touch movements toward targets presented randomly 5° or 10° to the left or right of central fixation in three viewing conditions: both eyes, monocular amblyopic eye (nondominant eye for participants without amblyopia), and monocular fellow eye (dominant eye for participants without amblyopia). Visual feedback of the target was removed on 50% of the trials at the initiation of reaching. RESULTS Both groups with abnormal binocular vision (strabismic amblyopia and strabismus only) had reach latency, accuracy, and precision comparable to visually normal participants when viewing with both eyes and fellow (dominant) eye. Latencies were significantly delayed by more than 30 ms in all participants with reduced binocularity during amblyopic eye or nondominant eye viewing compared with controls (P < 0.0001). Participants with strabismic amblyopia and negative stereopsis also had reduced reach precision (i.e., increased variability) during amblyopic eye viewing. In contrast, participants with strabismus only and negative stereopsis had comparable precision across all viewing conditions. Participants with strabismus only and those with strabismic amblyopia used a similar motor strategy; regardless of viewing condition, reach peak acceleration was significantly reduced (P < 0.05) and the duration of acceleration phase was extended in comparison with visually normal participants. There were no significant differences for the deceleration phase. CONCLUSIONS Participants with strabismic amblyopia and those with strabismus only attain relatively normal reach accuracy and precision. However, they use a different reach strategy that involves changing the motor plan. A similar compensatory strategy was reported previously in participants with anisometropic amblyopia. Our results provide further support that normal binocular vision during development provides important input for the development of visually guided reaching movements.

Proprioceptive role for palisade endings in extraocular muscles: Evidence from the Jendrassik Maneuver

A proprioceptive hypothesis for the control of eye movements has been recently proposed based on neuroanatomical tracing studies. It has been suggested that the non-twitch motoneurons could be involved in modulating the gain of sensory feedback from the eye muscles analogous to the gamma (gamma) motoneurons which control the gain of proprioceptive feedback in skeletal muscles. We conducted behavioral and psychophysical experiments to test the above hypothesis using the Jendrassik Maneuver (JM) to alter the activity of gamma motoneurons. It was hypothesized that the JM would alter the proprioceptive feedback from the eye muscles which would result in misregistration of eye position and mislocalization of targets. In the first experiment, vergence eye movements and pointing responses were examined. Data showed that the JM affected the localization responses but not the actual eye position. Perceptual judgments were tested in the second experiment, and the results showed that targets were perceived as farther when the afferent feedback was altered by the JM. Overall, the results from the two experiments showed that eye position was perceived as more divergent with the JM, but the actual eye movements were not affected. We tested this further in Experiment 3 by examining the effect of JM on the amplitude and velocity of saccadic eye movements. As expected, there were no significant differences in saccadic parameters between the control and experimental conditions. Overall, the present study provides novel insight into the mechanism which may be involved in the use of sensory feedback from the eye muscles. Data from the first two experiments support the hypothesis that the JM alters the registered eye position, as evidenced by the localization errors. We propose that the altered eye position signal is due to the effect of the JM which changes the gain of the sensory feedback from the eye muscles, possibly via the activity of non-twitch motoneurons.

Abnormal visual experience during development alters the early stages of visual-tactile integration.

Visual experience during the critical periods in early postnatal life is necessary for the normal development of the visual system. Disruption of visual input during this period results in amblyopia, which is associated with reduced activation of the striate and extrastriate cortices. It is well known that visual input converges with other sensory signals and exerts a significant influence on cortical processing in multiple association areas. Recent work in healthy adults has also shown that task-relevant visual input can modulate neural excitability at very early stages of information processing in the primary somatosensory cortex. Here we used electroencephalography to investigate visual-tactile interactions in adults with abnormal binocular vision due to amblyopia and strabismus. Results showed three main findings. First, in comparison to a visually normal control group, participants with abnormal vision had a significantly lower amplitude of the P50 somatosensory event related potential (ERP) when visual and tactile stimuli were presented concurrently. Second, the amplitude of the P100 somatosensory ERP was significantly greater in participants with abnormal vision. These results indicate that task relevant visual input does not significantly influence the excitability of the primary somatosensory cortex, instead, the excitability of the secondary somatosensory cortex is increased. Third, participants with abnormal vision had a higher amplitude of the P1 visual ERP when a tactile stimulus was presented concurrently. Importantly, these results were not modulated by viewing condition, which indicates that the impact of amblyopia on crossmodal interactions is not simply related to the reduced visual acuity as it was evident when viewing with the unaffected eye and binocularly. These results indicate that the consequences of abnormal visual experience on neurophysiological processing extend beyond the primary and secondary visual areas to other modality-specific areas.

The effect of progressively increased physical efforts on visual evoked potentials in volleyball players and non-athletes

Abstract We assessed the effect of physical effort with increasing intensity on neural activity in the visual pathway in volleyball players (n = 10) and non-athletes (n = 10). Participants performed three 10-min tests of increasing intensity on a cycle ergometer. Each participant was assigned individual workloads below the lactate threshold (40% [Vdot]O2max), at the lactate threshold (65–75% [Vdot]O2max), and above the lactate threshold (80% [Vdot]O2max). Four recordings of visual evoked potentials were made: pre-exercise and immediately after each of the three subsequent tests. We assessed neural activity of the visual pathway by examining the amplitude and latency of the N75, P100, and N135 components of the visual evoked potentials waveform. Pre-exercise P100 wave latency was shorter (P < 0.05) in volleyball players than in non-athletes. In non-athletes, the latency of P100 following the first and second effort (40% and 65–75% [Vdot]O2max) was reduced compared with pre-exercise (P < 0.01). However, P100 latency increased and P100 amplitude decreased after the third test (80% [Vdot]O2max) in non-athletes. In contrast, no significant changes in the latency or amplitude of visual evoked potentials were observed in the athletes in the three tests. Neural conductivity in the visual pathway after exercise might be at least partially dependent on the individuals personal training adaptation status.