Jun-Ru Tian

Testing quasi-visual neurons in the monkey's frontal eye field with the triple-step paradigm.

Abstract. To look successively at sites where several spots of light have appeared in the dark, we cannot simply rely on the image left by these targets on our retina. Our brain has to update target coordinates by taking into account each gaze movement that has taken place. A particular type of brain cell – the quasi-visual (QV) neuron – is assumed to play an important role in this updating by combining target coordinates and eye displacement signals. However, what is exactly this role? Is a QV neuron an element of a working memory that encodes the location of a potential target, or is it pointing to the location of the single goal selected for the next saccade? The two roles theoretically correspond to successive stages of processing: the locations of the optional targets would be stored at one stage, whereas the location of the next selected target would be stored at the subsequent stage. With a task that imposes a choice of goals – the triple-step paradigm – we found evidence that several groups of QV neurons can become simultaneously activated in the monkeys frontal eye field (FEF), suggesting that each group represents a different target location. This supports the hypothesis that the FEF itself contains the spatial information about not yet selected targets.

New Tests of Vestibular Function

Abstract: The vestibulo‐ocular reflex (VOR) is the only drive for short‐latency eye movements stabilizing the retina during externally imposed, sudden, high‐head accelerations. New strategies can exploit this unique VOR feature to study it under conditions relevant to the daily lives of patients, and to exclude the contributions from confounding nonvestibular mechanisms. Testing of the yaw vestibulo‐ocular reflex (VOR) during random, whole‐body rotational transients at ≤2800°/s2 delivered about centered and eccentric axes enables measurement of gains and millisecond latencies of the canal and otolith VORs in humans. Repeated measurements in acute unilateral deafferentation show sequential recovery of canal and otolith VORs to contralesional rotation, but severe and permanent deficits to ipsilesional rotation. Patients with bilateral loss of caloric responses show severe bilateral loss of VORs to transient rotation, suggesting that the apparent preservation of their VORs during sinusoidal rotations at moderate frequencies may be due instead to somatosensory inputs.

Vestibular function in severe bilateral vestibulopathy

OBJECTIVES To assess residual vestibular function in patients with severe bilateral vestibulopathy comparing low frequency sinusoidal rotation with the novel technique of random, high acceleration rotation of the whole body. METHODS Eye movements were recorded by electro-oculography in darkness during passive, whole body sinusoidal yaw rotations at frequencies between 0.05 and 1.6 Hz in four patients who had absent caloric vestibular responses. These were compared with recordings using magnetic search coils during the first 100 ms after onset of whole body yaw rotation at peak accelerations of 2800°/s2. Off centre rotations added novel information about otolithic function. RESULTS Sinusoidal yaw rotations at 0.05 Hz, peak veocity 240°/s yielded minimal responses, with gain (eye velocity/head velocity)<0.02, but gain increased and phase decreased at frequencies between 0.2 and 1.6 Hz in a manner resembling the vestibulo-ocular reflex. By contrast, the patients had profoundly attenuated responses to both centred and eccentric high acceleration transients, representing virtually absent responses to this powerful vestibular stimulus. CONCLUSION The analysis of the early ocular response to random, high acceleration rotation of the whole body disclosed a profound deficit of semicircular canal and otolith function in patients for whom higher frequency sinusoidal testing was only modestly abnormal. This suggests that the high frequency responses during sinusoidal rotation were of extravestibular origin. Contributions from the somatosensory or central predictor mechanisms, might account for the generation of these responses. Random, transient rotation is better suited than steady state rotation for quantifying vestibular function in vestibulopathic patients.

Dynamic visual acuity during yaw rotation in normal and unilaterally vestibulopathic humans.

Optimal visual acuity is achieved only when images are moving on the fovea at ≤ 2– 4°/s.1,2 During head motion, the vestibulo-ocular reflex (VOR) and other ocular motor subsystems normally stabilize images through compensatory eye movements. Dynamic visual acuity (DVA) during imposed head movement should reflect the performance of compensatory eye movements, leading to the supposition that VOR performance might be inferred from DVA. The present study investigates the effectiveness of DVA during various types of rotation to detect and lateralize unilateral peripheral vestibular deafferentation. In a four-alternative forced choice, subjects indicated the random orientations of an obliquely oriented letter “E” displayed 600 cm away. Optotype sizes varied by 0.1 log of the minimum angle resolvable (logMAR), and were visible only during head rotation. Binocular DVA was determined from 30–40 trials for each speed and direction using a computer-controlled staircase algorithm (QUEST).4 We studied normal subjects aged 18–72 yrs (15 for head thrust and 17 for whole-body transients), and 14 unilaterally vestibulopathic subjects aged 25–75 yrs who had undergone neurectomy or labyrinthectomy 7 days to 9 years prior to testing (11 underwent each type of motion). Subjects had best corrected static visual acuity 20/20 or better. Eye and head (bitebar) movements were sampled at 1200 Hz using magnetic search coils. Directionally predictable and unpredictable transients of whole-body yaw rotation were delivered by a 500-N-m servodriven chair with peak accelerations of 1000, 1600, and 2800°/s2, with optotypes presented for either 75 or 300 ms beginning 50 ms from rotation onset (FIG. 1A). For predictable motions, DVA in vestibulopathic subjects was not significantly different from normal. Search-coil recording indicated that deficient ipsilesional VOR was augmented by stereotypic anticipatory slow eye movements and vestibular catch-up saccades (VCUS).5 Only when both the timing and direction of high-acceleration rotations were unpredictable was the sensitivity of DVA of vestibulopathic subjects significantly subnormal during ipsilesional rotation. During ipsilesional rotations with 75-ms optotype presentation, unilaterally vestibulopathic subjects experienced a decrease in DVA from the static condition of 0.24 ± 0.10, 0.35 ± 0.12, 0.58 ± 0.11 logMAR (mean ± SD), respectively, for the three peak head accelerations of 1000, 1600, and 2800°/s2. This was significantly more in each case than the respective values of 0.15 ± 0.08, 0.20 ± 0.13, 0.23 ± 0.14

Functional anatomy of the extraocular muscles during vergence.

Magnetic resonance imaging (MRI) now enables precise visualisation of the mechanical state of the living human orbit, enabling inferences about the effects of mechanical factors on ocular kinematics. We used 3-dimensional (3D) magnetic search coil recordings and MRI to investigate the mechanical state of the orbit during vergence in humans. Horizontal convergence of 23 degrees from a remote to a near target aligned on one eye was geometrically ideal, and was associated with lens thickening and extorsion of the rectus pulley array of the aligned eye with superior oblique muscle relaxation and inferior oblique muscle contraction. There was no rectus muscle co-contraction. Subjective fusion through a 1 degree vertical prism caused a clockwise (CW) torsion in both eyes, as well as variable vertical and horizontal vergences that seldom corresponded to prism amount or direction. MRI under these conditions did not show consistent torsion of the rectus pulley array, but a complex pattern of changes in rectus extraocular muscle (EOM) crossections, consistent with co-contraction. Binocular fusion during vergence is accomplished by complex, 3D eye rotations seldom achieving binocular retinal correspondence. Vergence eye movements are sometimes associated with changes in rectus EOM pulling directions, and may sometimes be associated with co-contraction. Thus, extraretinal information about eye position would appear necessary to interpret binocular correspondence, and to avoid diplopia.

Human Angular Vestibulo-Ocular Reflex Initiation: Relationship to Listing's Law

Abstract: An ideal vestibulo‐ocular reflex (VOR) generates ocular rotations compensatory for head motion. During visually guided movements, Listings law (LL) constrains eye rotation to axes in Listings plane (LP). Recently, it has been reported that the VOR axis is not collinear with the rotation axis of the head, but is influenced by eye position in the orbit. Elaborate models have been proposed suggesting dynamic neural control of the VOR axis. By examining the variability and time course of changes in VOR axis orientation, we sought to test plausibility of these models. Binocular LPs were defined in eight humans. The VOR was evoked by a highly repeatable, transient, whole‐body yaw rotation in darkness at peak acceleration 2800 deg/s2. Immediately prior to rotation, subjects regarded targets at eye level, 20° up, or 20° down. Eye and head positions were expressed in LP coordinates for comparison with LL. Eye position generally followed head position and departed LP when the head axis tilted out of LP. In the velocity domain the VOR axis tilted 28 ± 9% of the change in vertical eye position, but there was significant intrasubject variation (14% to 41%). This roughly “quarter‐angle” behavior began with the earliest detectable VOR. Given the brief latency and marked interindividual variability of the eye position dependence of the VOR rotational axis, and the small deviation of the VOR from LL in the position domain, it is speculated that this behavior is largely due to orbital mechanics interacting with the basic neural commands that initiate the VOR.

Impaired Linear Vestibulo-Ocular Reflex Initiation and Vestibular Catch-Up Saccades in Older Persons

The vestibulo-ocular reflex, which stabilizes gaze to reduce retinal slip during head perturbations, has two components: the angular (AVOR), mediated by the semicircular canals, and the linear (LVOR), mediated by the otoliths. Progressive losses in vestibular sensory cells and primary neurons begins at about age 40 yrs,1 and are associated with age-related impairments in the steady-state1–3 and transient AVOR.4 However, little is known about possible age-related impairments of the LVOR. Vestibular catch-up saccades (VCUS) cued by the semicircular canals during transient rotations can supplement the hypometric AVOR to assist people with vestibular deafferentation to stabilize gaze.5 However, VCUS cued by otolith organs have not been previously studied, especially in terms of a possible association with aging. This study sought to characterize LVOR initiation and VCUS in older humans. We investigated nine younger subjects 24 ± 5 years of age (mean ± SD, range 18– 31) and eight older subjects 65 ± 7 years of age (range 56–75) who gave written informed consent to a protocol approved by the UCLA Human Subject Protection Committee. Random lateral (“heave”) translations were delivered by a pneumatic position servo at peak acceleration of 0.5 G over a distance of ± 25 cm. Subjects were firmly secured to a chair-mounted head-holder. Eye and head movements were sampled at 1200 Hz using binocular magnetic search coils and a cranial accelerometer. Ten responses were averaged for each condition. Subjects fixed targets at 200, 50, or 15 cm distant immediately before unpredictable onset of randomly directed translation in dark (LVOR) or light (visually enhanced LVOR, LVVOR). All older subjects maintained ideal vergence of 1.5–2 deg for the 200-cm target, 6–8 deg for the 50-cm target, and 21–26 deg for the 15-cm target, with actual vergences depending on individual interpupillary distances. Search coil recording of head rotation showed it to be negligible (< 0.5°)for the first 250 ms after onset of head translation, excluding a role for the AVOR in the responses studied. The typical

Human Surge Linear Vestibulo‐Ocular Reflex during Tertiary Gaze Viewing

Abstract: The otolith‐mediated linear vestibulo‐ocular reflex (IVOR) was studied in 9 normal humans undergoing transient whole‐body surges at 0.5 g peak acceleration while viewing targets eccentrically placed in tertiary positions that combined horizontal and vertical eccentricities at distance of 15, 25, or 50 cm both in darkness and light. Mean velocity gain (±SEM) for the horizontal component was 0.61 ± 0.04 in darkness and increased to 0.72 ± 0.03 for visible targets (P < 0.05), and for the vertical component was 0.54 ± 0.02 in darkness, not significantly different from horizontal component gain. For visible targets, vertical component gain significantly increased to 0.63 ± 0.04 (P < 0.05) with visible targets, but remained significantly less than horizontal component gain.

Human angular vestibulo-ocular reflex axis disconjugacy : Relationship to magnetic resonance imaging evidence of globe translation

Abstract: Magnetic resonance imaging (MRI) demonstrates that the lateral rectus pulley shifts 0.5 mm inferiorly relative to the medial rectus in 20° upgaze, but 0.5 mm superiorly in 20° downgaze, whereas the globe translates 0.7 mm nasally in adduction and 0.2 mm nasally in abduction. If pulleys influence ocular kinematics, these effects would predict disconjugate alterations of the yaw vestibulo‐ocular reflex (VOR) rotational axes. Binocular eye and head movements were recorded using three‐dimensional search coils in 8 humans (age 24 ± 2 years, mean ± SE) undergoing directionally randomized, transient, whole‐body yaw (2800°/s2 peak) in darkness while fixating straight ahead, as well as ± 18° vertically. Eye and head rotational velocity axes were expressed as quaternions in Listing coordinates. In the initial 70 ms, the ocular axis varied with vertical gaze by one‐quarter the angle of target elevation, but this effect summed significantly with a disconjugate effect of horizontal duction. In central gaze, the mean adducting eye (AD) rotational axis tilted 3.4 ± 0.8° forward relative to the head axis, while that of the abducting eye (AB) tilted 0.6 ± 0.8° backward. In downgaze, the AD rotational axis tilted 8.6 ± 1.0° forward, and AB 5.7 ± 1.2° forward. In upgaze, the AD rotational axis tilted backward by 0.1 ± 0.7°, and AB backward 3.4 ± 0.9°. We suggest that nasal globe translation relative to the fixed trochlea produces binocular extorsion accounting for yaw VOR axis disconjugacy, and thus a horizontal duction dependence in VOR rotational axis summating with classic dependence of VOR axis on vertical gaze. Confirmation of predicted duction‐dependent VOR disconjugacy supports the idea that rectus pulleys influence kinematics for all eye movements.