Simultaneous recordings of human microsaccades and drifts with a contemporary video eye tracker and the search coil technique.

Human eyes move continuously, even during visual fixation. These "fixational eye movements" (FEMs) include microsaccades, intersaccadic drift and oculomotor tremor. Research in human FEMs has grown considerably in the last decade, facilitated by the manufacture of noninvasive, high-resolution/speed video-oculography eye trackers. Due to the small magnitude of FEMs, obtaining reliable data can be challenging, however, and depends critically on the sensitivity and precision of the eye tracking system. Yet, no study has conducted an in-depth comparison of human FEM recordings obtained with the search coil (considered the gold standard for measuring microsaccades and drift) and with contemporary, state-of-the art video trackers. Here we measured human microsaccades and drift simultaneously with the search coil and a popular state-of-the-art video tracker. We found that 95% of microsaccades detected with the search coil were also detected with the video tracker, and 95% of microsaccades detected with video tracking were also detected with the search coil, indicating substantial agreement between the two systems. Peak/mean velocities and main sequence slopes of microsaccades detected with video tracking were significantly higher than those of the same microsaccades detected with the search coil, however. Ocular drift was significantly correlated between the two systems, but drift speeds were higher with video tracking than with the search coil. Overall, our combined results suggest that contemporary video tracking now approaches the search coil for measuring FEMs.

Behavior of the human translational vestibulo-ocular reflex during simultaneous head translation and rotation.

BACKGROUND: During head translations, vestibular eye movements are ∼ 60% of those required to hold the line of sight on target but, during translation of the orbits due to head rotation about an eccentric axis, the eyes are held %eye on target. OBJECTIVE: To resolve this paradoxical behavior of vestibulo-ocular reflexes. METHODS: Subjects sat on a moving platform viewing a near target and were: (1) rotated en bloc in yaw about a vertical axis centered on the head at 1 Hz; (2) rotated with their head displaced ∼ 10 cm anterior (eccentric rotation) at 1 Hz; (3) translated along the inter-aural axis at 1.9 Hz; (4) rotated with the head centered at 1 Hz while they were translated along the inter-aural axis at 1.9 Hz. We calculated compensation ratio (CR): Eye velocity/eye velocity geometrically required to hold the eye on target. RESULTS: During yaw, mean CR was 0.88 and during eccentric rotation CR was 0.93. During translation at 1.9 Hz, CR was 0.65. During combined rotation at 1.0 Hz and translation at 1.9 Hz, CR was 0.81 for head rotations and 0.74 for head translations. CONCLUSIONS: Translations of the orbits due to head rotation are better compensated for than translations of the orbits due to head translation. These different behaviors may be determined by context, the important difference being whether the subject is moving through the environment.

Amplitude and frequency prediction in the translational vestibulo-ocular reflex.

The goal of this study was to assess the effect of amplitude and frequency predictability on the performance of the translational vestibulo-ocular reflex (tVOR). Eye movements were recorded in 5 subjects during continuous vertical translation that consisted of a series of segments with: 1) 3 amplitudes at constant frequency (2 Hz) or 2) 3 different frequencies (1.6, 2, 2.5 Hz). Stimulus changes were presented in a pseudo-random order. We found that there was little change in the tVOR immediately after an unexpected stimulus change, as if eye velocity were being driven more by an expectation based on previous steady-state motion than by current head translation. For amplitude transitions, only about 30% of the eventual response change was seen in the first half cycle. Similarly, a sudden change in translation frequency did not appear in eye velocity for 70 ms, compared to a 8 ms lag during similar yaw rotation. Finally, after a sudden large decrease in frequency, the eyes continued to track at the original higher frequency, resulting initially in an anti-compensatory tVOR acceleration. Our results elucidate further the complexity of the tVOR and show that motion prediction based on prior experience plays an important role in its response.

Saccades during attempted fixation in parkinsonian disorders and recessive ataxia: from microsaccades to square-wave jerks.

During attempted visual fixation, saccades of a range of sizes occur. These "fixational saccades" include microsaccades, which are not apparent in regular clinical tests, and "saccadic intrusions", predominantly horizontal saccades that interrupt accurate fixation. Square-wave jerks (SWJs), the most common type of saccadic intrusion, consist of an initial saccade away from the target followed, after a short delay, by a "return saccade" that brings the eye back onto target. SWJs are present in most human subjects, but are prominent by their increased frequency and size in certain parkinsonian disorders and in recessive, hereditary spinocerebellar ataxias. Here we asked whether fixational saccades showed distinctive features in various parkinsonian disorders and in recessive ataxia. Although some saccadic properties differed between patient groups, in all conditions larger saccades were more likely to form SWJs, and the intervals between the first and second saccade of SWJs were similar. These findings support the proposal of a common oculomotor mechanism that generates all fixational saccades, including microsaccades and SWJs. The same mechanism also explains how the return saccade in SWJs is triggered by the position error that occurs when the first saccadic component is large, both in the healthy brain and in neurological disease.

Neurological basis for eye movements of the blind.

When normal subjects fix their eyes upon a stationary target, their gaze is not perfectly still, due to small movements that prevent visual fading. Visual loss is known to cause greater instability of gaze, but reported comparisons with normal subjects using reliable measurement techniques are few. We measured binocular gaze using the magnetic search coil technique during attempted fixation (monocular or binocular viewing) of 4 individuals with childhood-onset of monocular visual loss, 2 individuals with late-onset monocular visual loss due to age-related macular degeneration, 2 individuals with bilateral visual loss, and 20 healthy control subjects. We also measured saccades to visual or somatosensory cues. We tested the hypothesis that gaze instability following visual impairment is caused by loss of inputs that normally optimize the performance of the neural network (integrator), which ensures both monocular and conjugate gaze stability. During binocular viewing, patients with early-onset monocular loss of vision showed greater instability of vertical gaze in the eye with visual loss and, to a lesser extent, in the normal eye, compared with control subjects. These vertical eye drifts were much more disjunctive than upward saccades. In individuals with late monocular visual loss, gaze stability was more similar to control subjects. Bilateral visual loss caused eye drifts that were larger than following monocular visual loss or in control subjects. Accurate saccades could be made to somatosensory cues by an individual with acquired blindness, but voluntary saccades were absent in an individual with congenital blindness. We conclude that the neural gaze-stabilizing network, which contains neurons with both binocular and monocular discharge preferences, is under adaptive visual control. Whereas monocular visual loss causes disjunctive gaze instability, binocular blindness causes both disjunctive and conjugate gaze instability (drifts and nystagmus). Inputs that bypass this neural network, such as projections to motoneurons for upward saccades, remain conjugate.

Influence of orbital eye position on vertical saccades in progressive supranuclear palsy.

Disturbance of vertical saccades is a cardinal feature of progressive supranuclear palsy (PSP). We investigated whether the amplitude and peak velocity (PV) of saccades are affected by the orbital position from which movements start in PSP patients and age-matched control subjects. Subjects made vertical saccades in response to ±5° vertical target jumps with their heads in one of three positions: head "center," head pitched forward ∼15°, and head pitched back ∼15°. All patients showed some effect of starting eye position, whether beginning in the upward or downward field of gaze, on saccade amplitude, PV, and net range of movement. Generally, reduction of amplitude and PV were commensurate and bidirectional in the affected hemifield of gaze. Such findings are unlikely to be because of orbital factors and could be explained by varying degrees of involvement of rostral midbrain nuclei in the pathological process.

Critical role of cerebellar fastigial nucleus in programming sequences of saccades.

The cerebellum plays an important role in programming accurate saccades. Cerebellar lesions affecting the ocular motor region of the fastigial nucleus (FOR) cause saccadic hypermetria; however, if a second target is presented before a saccade can be initiated (double-step paradigm), saccade hypermetria may be decreased. We tested the hypothesis that the cerebellum, especially FOR, plays a pivotal role in programming sequences of saccades. We studied patients with saccadic hypermetria because of either genetic cerebellar ataxia or surgical lesions affecting FOR and confirmed that the gain of initial saccades made to double-step stimuli was reduced compared with the gain of saccades to single target jumps. Based on measurements of the intersaccadic interval, we found that the ability to perform parallel processing of saccades was reduced or absent in all of our patients with cerebellar disease. Our results support the crucial role of the cerebellum, especially FOR, in programming sequences of saccades.

Visual and vestibular determinants of the translational vestibulo-ocular reflex.

Prior studies indicate that the human translational vestibulo-ocular reflex (tVOR) generates eye rotations approximately half the magnitude required to keep the line of sight pointed at a stationary object--a compensation ratio (CR) of ∼0.5. We asked whether changes of visual or vestibular stimuli could increase the CR of tVOR. First, subjects viewed their environment through an optical device that required eye movements to increase by ∼50% to maintain fixation of a stationary visual target. During vertical translation, eye movements did increase, but tVOR CR remained at ∼0.5. Second, subjects viewed through LCD goggles providing 4 Hz strobe vision that minimized retinal image motion; this reduced tVOR CR. Finally, subjects were rotated in roll while they translated vertically; no increase in tVOR occurred. Taken with prior studies, we conclude that tVOR is optimally set to generate eye rotations that are about 50% of those required to stabilize the line of sight.