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.

Three dimensional kinematics of rapid compensatory eye movements in humans with unilateral vestibular deafferentation.

Saccades executed with the head stationary have kinematics conforming to Listing's law (LL), confining the ocular rotational axis to Listing's plane (LP). In unilateral vestibular deafferentation (UVD), the vestibulo-ocular reflex (VOR), which does not obey LL, has at high head acceleration a slow phase that has severely reduced velocity during ipsilesional rotation, and mildly reduced velocity during contralesional rotation. Studying four subjects with chronic UVD using 3D magnetic search coils, we investigated kinematics of stereotypic rapid eye movements that supplement the impaired VOR. We defined LP with the head immobile, and expressed eye and head movements as quaternions in LP coordinates. Subjects underwent transient whole body yaw at peak acceleration 2,800 degrees /s(2) while fixating targets centered, or 20 degrees up or down prior to rotation. The VOR shifted ocular torsion out of LP. Vestibular catch-up saccades (VCUS) occurred with mean latency 90 +/- 44 ms (SD) from ipsilesional rotation onset, maintained initial non-LL torsion so that their quaternion trajectories paralleled LP, and had velocity axes changing by half of eye position. During contralesional rotation, rapid eye movements occurred at mean latency 135 +/- 36 ms that were associated with abrupt decelerations (ADs) of the horizontal slow phase correcting 3D deviations in its velocity axis, with quaternion trajectories not paralleling LP. Rapid eye movements compensating for UVD have two distinct kinematics. VCUS have velocity axis dependence on eye position consistent with LL, so are probably programmed in 2D by neural circuits subserving visual saccades. ADs have kinematics that neither conform to LL nor match the VOR axis, but appear instead programmed in 3D to correct VOR axis errors.

Shifts in listing's plane produced by vertical axis rotation: sustained ocular torsion due to semicircular canal stimulation.

PURPOSE: With the head upright and stationary, ocular torsion is confined by Listing's Law (LL), so that three-dimensional eye rotational axes form Listing's plane (LP). During head rotation, the vestibulo-ocular reflex violates LL by driving ocular torsion opposite to head torsion, sometimes out of LP. Saccades originating from non-Listing's initial torsional positions remain in a plane offset from, but parallel to, the original LP. The present study was conducted to determine whether whole-body yaw alters the position and orientation of LP. METHODS: Eight normal subjects and six with unilateral vestibular deafferentation (UVD) underwent binocular eye and head movement recordings with 3-D magnetic search coils. Visual fixations were used to define LP, after which subjects underwent whole-body yaw rotation of 30 degrees or 70 degrees , at peak accelerations from 125 deg/s(2) to 2800 deg/s(2). Gaze during rotation was either central or 20 degrees up. After rotation, a dynamic LP (DLP) was defined during fixations. RESULTS: Orientation and thickness of the DLP did not vary significantly from the previously defined LP; however, DLP was offset an average of 4 degrees +/- 4 degrees (mean +/- SD), 87% of head torsion relative to LP. Stimulus intensity, UVD, and starting vertical gaze direction had no effect on DLP offset or orientation. The DLP torsional offset declined toward the original LP with a time constant of approximately 1 minute, suggesting mediation by neural integration. CONCLUSIONS: Yaw rotation can cause stable torsional offsets in the location of Listing's Plane.

Effect of unilateral vestibular deafferentation on the initial human vestibulo-ocular reflex to surge translation.

Transient whole-body surge (fore-aft) translation at 0.5 G peak acceleration was administered to six subjects with unilateral vestibular deafferentation (UVD), and eight age-matched controls. Subjects viewed eccentric targets to determine if linear vestibulo-ocular reflex (LVOR) asymmetry might lateralize otolith deficits. Eye rotation was measured using magnetic search coils. Immediately before surge, subjects viewed a luminous target 50 cm away, centered or displaced 10 degrees horizontally or vertically. The target was extinguished during randomly directed surges. LVOR gain relative to ideal velocity in subjects with UVD for the contralesional horizontally eccentric target (0.59 +/- 0.08, mean +/- SEM) did not differ significantly from normal (0.50 +/- 0.04), but gain for the ipsilesional eccentric target (0.35 +/- 0.02) was significantly less than normal (0.48 +/- 0.03, P < 0.05). Normal subjects had mean gain asymmetry for horizontally eccentric targets of 0.17 +/- 0.03, but asymmetry in UVD was significantly increased to 0.35 +/- 0.05 (P < 0.05). Four of six subjects with UVD had maximum gain asymmetry outside normal 95% confidence limits. Asymmetry did not correlate with UVD duration. Gain for 10 degrees vertically eccentric targets averaged 0.38 +/- 0.14 for subjects with UVD, insignificantly lower than the normal value of 0.75 +/- 0.15 (P > 0.05). Surge LVOR latency was symmetrical in UVD, and did not differ significantly from normal. There was no significant difference in response between dark and visible target conditions until 200 ms after surge onset. Chronic human UVD, on average, significantly impairs the surge LVOR for horizontally eccentric targets placed ipsilesionally, but this asymmetry is small relative to interindividual variation.

Temporal dynamics of semicircular canal and otolith function following acute unilateral vestibular deafferentation in humans.

Dynamic changes of deficits in canal and otolith vestibulo-ocular reflexes (VORs) to high acceleration, eccentric yaw rotations were investigated in five subjects aged 25-65 years before and at frequent intervals 3-451 days following unilateral vestibular deafferentation (UVD) due to labyrinthectomy or vestibular neurectomy. Eye and head movements were recorded using magnetic search coils during transients of directionally random, whole-body rotation in darkness at peak acceleration 2,800 degrees/s2. Canal VORs were characterized during rotation about a mid-otolith axis, viewing a target 500 cm distant until rotation onset in darkness. Otolith VOR responses were characterized by the increase in VOR gain during identical rotation about an axis 13 cm posterior to the otoliths, initially viewing a target 15 cm distant. Pre-UVD canal gain was directionally symmetrical, averaging 0.87 +/- 0.02 (+/-SEM). Contralesional canal gain declined from pre-UVD by an average of 22% in the first 3-5 days post-UVD, before recovering to an asymptote of close 90% of pre-UVD level at 1-3 months. This recovery corresponded to resolution of spontaneous nystagmus. Ipsilesional gain declined to 59%, and showed no consistent recovery afterwards. Pre-UVD otolith gain was directionally symmetrical, averaging 0.56 +/- 0.02. Immediately after UVD, the contralesional otolith gain declined to 0.30 +/- 0.02, and did not recover. Ipsilesional otolith gain declined profoundly to 0.08 +/- 0.03 (P < 0.01), and never recovered. In contrast to the modest and directionally symmetrical effect of UVD on the human otolith VOR during pure translational acceleration, otolith gain during eccentric yaw rotation exhibited a profound and lasting deficit that might be diagnostically useful in lateralizing otolith pathology. Most recovery of the human canal gain to high acceleration transients following UVD is for contralesional head rotation, occurring within 3 months as spontaneous nystagmus resolves.

Vestibulo-ocular reflex to transient surge translation: complex geometric response ablated by normal aging.

The linear vestibulo-ocular reflex (LVOR) to surge (fore-aft) translation has complex kinematics varying with target eccentricity and distance. To determine normal responses and aging changes, 9 younger [age, 28 +/- 2 (SE) yr] and 11 older subjects (age, 69 +/- 2 yr) underwent 0.5 g whole body surge transients while wearing binocular scleral search coils. Linear chair position and head acceleration were measured with a potentiometer and accelerometer. Subjects viewed centered and 10 degrees horizontally and vertically eccentric targets 50, 25, or 15 cm distant before unpredictable onset of randomly directed surge in darkness (LVOR) and light (V-LVOR). Response directions were kinematically appropriate to eccentricity in all subjects, but there were significantly more measurable LVOR and V-LVOR responses (63-79%) in younger than older subjects (38-44%, P < 0.01). Minimal LVOR latency averaged 48 +/- 4 ms for younger and significantly longer at 70 +/- 6 ms for older subjects. In the interval 200-300 ms after surge onset, horizontal LVOR gain (relative to ideal velocity) of younger subjects averaged over all target distances was 0.55 +/- 0.04 and was significantly reduced in older subjects to 0.33 +/- 0.04. Horizontal V-LVOR gain was 0.58 +/- 0.04 in younger and significantly lower at 0.35 +/- 0.06 in older subjects. Vertical gains did not differ significantly between groups. Target visibility had no effect in either group during the initial 200 ms. The LVOR and V-LVOR were augmented by saccades in younger more than older subjects. Aging thus decreases LVOR velocity gain, response rate, and saccade augmentation, but prolongs latency.

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

Magnetic resonance imaging (MRI) demonstrates that the lateral rectus pulley shifts 0.5 mm inferiorly relative to the medial rectus in 20 degrees upgaze, but 0.5 mm superiorly in 20 degrees 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 degrees /s2 peak) in darkness while fixating straight ahead, as well as +/- 18 degrees 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 degrees forward relative to the head axis, while that of the abducting eye (AB) tilted 0.6 +/- 0.8 degrees backward. In downgaze, the AD rotational axis tilted 8.6 +/- 1.0 degrees forward, and AB 5.7 +/- 1.2 degrees forward. In upgaze, the AD rotational axis tilted backward by 0.1 +/- 0.7 degrees, and AB backward 3.4 +/- 0.9 degrees. 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.

Human angular vestibulo-ocular reflex initiation: relationship to Listing's law.

An ideal vestibulo-ocular reflex (VOR) generates ocular rotations compensatory for head motion. During visually guided movements, Listing's law (LL) constrains eye rotation to axes in Listing's 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 degrees up, or 20 degrees 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.

Human surge linear vestibulo-ocular reflex during tertiary gaze viewing.

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.

Initiation and cancellation of the human heave linear vestibulo-ocular reflex after unilateral vestibular deafferentation.

The effect of unilateral vestibular deafferentation (UVD) on the linear vestibulo-ocular reflex (LVOR) was studied in 11 humans an average of 52 months following surgical UVD. Controls consisted of seven healthy age-matched subjects. The LVOR was evoked by directionally random, transient whole body interaural (heave) translation with a peak acceleration of 0.5 g while subjects viewed earth-fixed (LVOR) and head-fixed (cancellation) targets 15, 25, and 200 cm distant. The magnitude of the LVOR slow phase was inversely proportional to target distance for both subject groups. Neither latency nor the magnitude of the LVOR significantly differed in the ipsi- vs contralesional directions (P>0.1) in UVD. When the target disappeared at heave onset, subjects with UVD had LVOR slow phase displacement 100 ms later that was 5% of ideal at 15 cm, 6% at 25 cm, and 16% at 200 cm. This was significantly less than corresponding control values of 41, 43, and 50%. During cancellation the LVOR magnitude 100 ms from heave onset was reduced at all target distances by an average of 40+/-4%, and the relative reduction did not significantly differ between controls and subjects with UVD (P>0.1). Cancellation latency did not vary significantly among target distances or subject groups. It is concluded that after UVD, the LVOR is bilaterally and symmetrically reduced but remains modulated by viewing distance and cancellation effort.

Vestibular catch-up saccades augmenting the human transient heave linear vestibulo-ocular reflex.

Vestibular catch-up saccades (VCUS) cued by the semicircular canals can supplement the deficient angular vestibulo-ocular reflex during transient rotations to stabilize gaze in people with unilateral vestibular deafferentation (Tian et al. 2000). However, a possible analogous role for VCUS to augment a deficient linear vestibulo-ocular reflex (LVOR) has not been carefully studied. We investigated VCUS in 9 younger, 8 older normal, and 12 vestibulopathic subjects undergoing directionally random heave (interaural) translations at 0.5 g peak acceleration. Eye and head movements were sampled at 1200 Hz using magnetic search coils and a cranial accelerometer. Subjects fixated visible targets 200, 50, or 15 cm distant immediately before unpredictable onset of translation in either darkness or light. Evoked slow phase eye rotations opposite to the direction of head translation accounted for only 19-70% of ideal eye position, being less for nearer targets, and VCUS commonly occurred to augment the deficiency. Eye position error relative to geometric ideal was highly correlated to VCUS amplitude ( P<0.001). This error was systematically corrected by VCUS whose latency decreased, and speed and frequency increased, with decreasing target distance. When targets remained visible, nearly all subjects made VCUS for nearer targets. In darkness, VCUS for the nearest target were significantly less common for older normal and vestibulopathic subjects than in younger normal subjects ( P<0.001). In older and vestibulopathic subjects, VCUS latency was significantly prolonged. We conclude that otolith-mediated VCUS calibrated to target distance assist LVOR slow phases, but the ability to generate VCUS in darkness is impaired in older normal and vestibulopathic subjects. In the presence of visual information, VCUS can be generated in older and vestibulopathic subjects, albeit at prolonged latency perhaps indicating visual augmentation of deficient vestibular input.

Effect of aging on the human initial interaural linear vestibulo-ocular reflex.

To determine age-related changes, the initial linear vestibulo-ocular reflex (LVOR) of eight older subjects of mean age 65+/-7 years (mean +/- SD, range 56-75 years) was compared with that of nine younger subjects of mean age 24+/-5 years (range 18-31 years) in response to random transients of whole-body heave (interaural) translation at peak acceleration of 0.5 g delivered by a pneumatic actuator. Binocular eye rotations were measured with magnetic search coils, while linear head position and acceleration were measured with a potentiometer and piezoelectric accelerometer. Subjects viewed targets 200 cm, 50 cm, or 15 cm distant immediately before the unpredictable onset of randomly directed translation in darkness (LVOR) and in light (LVVOR). All subjects maintained ideal vergence of 1.5-2 degrees for the 200-cm target, 6-8 degrees for the 50-cm target, and 21-26 degrees for the 15-cm target, with actual vergences depending on individual interpupillary distances. Search coil recording of angular position of the upper teeth showed head rotation to be negligible (less than 0.5 degrees ) for the first 250 ms after onset of head translation, excluding a role for the angular VOR in the responses studied. The LVOR response to heave translation was an oppositely directed eye rotation occurring after a mean latency of 62+/-3 ms for older and 42+/-3 ms (mean +/- SD) for younger subjects ( P<0.0001). The peak of the latency distribution was 60-100 ms for older and 20-60 ms for younger subjects. During the early interval, 70-80 ms from head motion onset prior to a pursuit contribution or saccades, all subjects had significantly enhanced LVOR with decreasing target distance. In this interval, the LVOR position amplitude of younger subjects was 0.17+/-0.01 degrees, 0.40+/-0.01 degrees, 0.57+/-0.01 degrees (mean +/- SE), respectively, in descending order of target distance. Early sensitivities were significantly reduced for older subjects to 0.07+/-0.01 degrees, 0.23+/-0.01 degrees, 0.40+/-0.01 degrees ( P<0.0001). There was no significant effect of target visibility in either group during the first 110 ms ( P>0.05). Visual-otolith interaction was mainly reflected not by the vestibular slow phase, but by vestibular catch-up saccades (VCUS) in the compensatory direction. The effect of aging on the initial human LVOR is thus to: prolong latency, reduce early sensitivity, and reduce occurrence of vestibular catch-up saccades.

Dynamic visual acuity during passive and self-generated transient head rotation in normal and unilaterally vestibulopathic humans.

To determine whether dynamic visual acuity (DVA) during head rotations on the stationary body can lateralize unilateral vestibular deafferentation and detect non-labyrinthine compensation mechanisms, 15 normal and 11 subjects with unilateral vestibular deafferentation underwent manually imposed and self-generated transient yaw head rotations during measurement of binocular DVA. DVA was measured by a four-alternative, forced choice, staircase procedure with optotype presentation only when head velocity exceeded thresholds of 50 degree or 75 degree/s. Eye and head movements were recorded using search coils to characterize ocular motor strategies. During directionally unpredictable, manually imposed contralesional rotation, unilaterally deafferented subjects had decreases in DVA from the static condition of 0.36 +/- 0.22 and 0.47 +/- 0.53 log of the minimum angle resolvable (logMAR, mean +/- SD), respectively, for 50 degree and 75 degree/s thresholds, not significantly greater than those of normal subjects (0.26 +/- 0.13 and 0.36 +/- 0.14, P>0.05). However, during manually imposed ipsilesional rotation, vestibulopathic subjects had decreases in DVA of 0.66 +/- 0.36 and 1.08 +/- 0.47 logMAR, significantly greater than during contralesional rotation ( P<0.01). The DVA reduction difference for the ipsi- and contralesional directions was less during self-generated than during manually imposed head rotations. The directional difference for manually administered head rotations yielded a robust diagnostic measure with essentially no overlap in performance with normal subjects. Diagnostic performance for DVA during self-generated head rotation was poorer. Recordings of eye and head movements made using search coils during DVA testing confirmed a deficient vestibulo-ocular reflex (VOR) during ipsilesional rotation, with most unilaterally vestibulopathic subjects employing predictive smooth eye movements and vestibular catch-up saccades. Measurement of DVA during transient head rotation on the body thus reliably can detect and lateralize vestibular pathology and compensatory mechanisms. Extravestibular mechanisms for compensation appear more effective during self-generated than manually imposed head rotations.