July 2015
Volume 56, Issue 8
Free
Eye Movements, Strabismus, Amblyopia and Neuro-ophthalmology  |   July 2015
Crouzon Syndrome: Relationship of Eye Movements to Pattern Strabismus
Author Affiliations & Notes
  • Avery H. Weiss
    Roger Johnson Clinical Vision Laboratory, Division of Ophthalmology, Seattle Children's Hospital, Seattle, Washington, United States
    Department of Ophthalmology, University of Washington, Seattle, Washington, United States
  • John P. Kelly
    Roger Johnson Clinical Vision Laboratory, Division of Ophthalmology, Seattle Children's Hospital, Seattle, Washington, United States
    Department of Ophthalmology, University of Washington, Seattle, Washington, United States
  • Richard A. Hopper
    Division of Plastic and Reconstructive Surgery, University of Washington, Harborview Medical Center, Seattle, Washington, United States
  • James O. Phillips
    Roger Johnson Clinical Vision Laboratory, Division of Ophthalmology, Seattle Children's Hospital, Seattle, Washington, United States
    Department of Otolaryngology, University of Washington, Seattle, Washington, United States
  • Correspondence: Avery H. Weiss, Division of Ophthalmology, OA.9.220, Seattle Children's Hospital, 4800 Sand Point Way NE, Seattle, WA 98105, USA; avery.weiss@seattlechildrens.org
Investigative Ophthalmology & Visual Science July 2015, Vol.56, 4394-4402. doi:10.1167/iovs.14-15645
  • Views
  • PDF
  • Share
  • Tools
    • Alerts
      ×
      This feature is available to Subscribers Only
      Sign In or Create an Account ×
    • Get Citation

      Avery H. Weiss, John P. Kelly, Richard A. Hopper, James O. Phillips; Crouzon Syndrome: Relationship of Eye Movements to Pattern Strabismus. Invest. Ophthalmol. Vis. Sci. 2015;56(8):4394-4402. doi: 10.1167/iovs.14-15645.

      Download citation file:


      © ARVO (1962-2015); The Authors (2016-present)

      ×
  • Supplements
Abstract

Purpose: To characterize conjugate eye movements in Crouzon syndrome (CS) patients with and without strabismus.

Methods: Smooth pursuit, saccades, horizontal optokinetic nystagmus (OKN), and horizontal vestibulo-ocular reflex (VOR) were recorded using binocular video-oculography (VOG) in 10 children with CS (5 orthotropic, 5 strabismic) and 12 age-matched controls. Hess-Lancaster plots were generated from Orbit 1.8 using rectus muscle pulley locations from computed tomography imaging. Two-dimensional eye scan paths from VOG recordings were compared with the Hess-Lancaster plots.

Results: Targeted saccades were normometric on average but variable, and followed the main sequence in both CS groups. Smooth pursuit gains were normal for both CS groups; however, SP gains of the fixating eye in subjects with strabismus were significantly lower. Optokinetic nystagmus gains were reduced in both CS groups (P < 0.02) but were lower in subjects with strabismus. Shifting misalignments of binocular eye position in primary and eccentric gazes were associated with reduction in OKN gain in both CS groups. Vestibulo-ocular reflex gains for both CS groups were largely normal despite the presence of an off-axis vertical component.

Conclusions: Normal gains for saccades and smooth pursuit in CS patients with strabismus are consistent with accurate execution of both movements despite extorsion of the globe. Vestibulo-ocular reflex in CS patients with strabismus had an off-axis vertical component consistent with extorted muscle pulleys. Optokinetic nystagmus is reduced in CS without strabismus owing to binocular position disparities and in CS with strabismus is likely due to cortical suppression associated with cross-axis orientation and exotropia.

Crouzon syndrome (CS) is a genetic disorder characterized by premature closure of the coronal, lambdoidal, and sagittal sutures.1 Postnatal growth of the skull is constrained along the closed suture leading to deformations of skull shape, distortion of facial features, orbital dystopia, and increases in intracranial pressure. Head shape is typically brachycephalic with associated midface retrusion. The orbits are shallow and the globe is protruded, predisposing the cornea to exposure and intermittent protrusion of the globe equator anterior to the eyelid margins in infancy.2 Increased intracranial pressure can result in optic neuropathy with occult visual loss for which these children require serial monitoring.36 Distortion of head shape, abnormal facial appearance, and concerns about increased intracranial pressure restricting brain growth prompt surgical intervention. Expansion and reshaping of the skull, frontal bone, and superior orbits is performed between 9 and 15 months of life when the infant capacity for bone remodeling of the surgical cranial defects is balanced with the stability of the bone.7 Midface advancement is usually performed at 7 to 10 years of age after completion of upper midface growth.8,9 
Strabismus is the most common cause of visual disability in older children with CS.2,10,11 The strabismus is usually characterized by a V-pattern exotropia and “overelevation in adduction.”12 Previously, we have shown that the pattern strabismus and the dissociated vertical strabismus associated with CS can be accounted for by extorsion of the rectus muscle pulleys.13 The resulting extorsion of the globe creates an angular misalignment of the retinal image and the spatial location of the target. To date, the potential impact of the angular misalignment of the retina and extorsion of the muscle pulleys has not been studied. Herein, we compare the accuracy and metrics of eye movements in 10 subjects with CS, 5 with and 5 without pattern strabismus. 
Methods
We retrospectively studied 10 children with CS after institutional review board approval was granted. The research adhered to the tenets of the Declaration of Helsinki. A pediatrician and plastic surgeon specializing in craniofacial disorders established the diagnosis in all subjects. Crouzon syndrome was suspected on the basis of the variable presence of a misshapen skull, hypertelorism with exorbitism, midface hypoplasia, and history of similarly affected relatives with autosomal dominant inheritance. In all cases, the craniofacial diagnosis was confirmed by computed tomography (CT) documentation of premature closure of the coronal, sagittal, and lambdoidal sutures. 
All of the subjects had comprehensive eye examinations with emphasis on assessment of binocular eye alignment in primary gaze and at eccentricities of 15° up, down, right, and left. Binocular deviations were quantified using the prism cover test or the Krimsky test depending on subject cooperation. All but one subject had at least one craniofacial surgery. 
Control data for saccade, smooth pursuit, and vestibulo-ocular reflex (VOR) were obtained from 12 normally developing children (mean age 11.8 years, SD = 3.3) following the same protocols. There was no difference in age between controls and CS subjects (t-test; P = 0.33). 
Stimuli
All visual stimuli were back-projected onto a translucent tangent screen subtending 60 × 80° in a darkened room. Gaze holding was measured during fixation of a point target (0.7° diameter) in primary position and at eccentricities of 15° right, left, up, and down. To elicit horizontal and vertical saccades, the target was stepped pseudo-randomly along the horizontal or vertical meridian. To elicit smooth pursuit. the same target was drifted sinusoidally ±10° at peak velocities of 10, 20, and 30°/s on a blank field to minimize the potential impact of the background on smooth pursuit gain.14,15 To elicit optokinetic nystagmus (OKN), high-contrast (>80%) square-wave gratings oriented vertically with a spatial frequency of 0.1 cyc/deg were drifted at a constant horizontal velocity of 15, 30, and 45°/s. To elicit VOR, we sinusoidally rotated the subject in complete darkness with head erect about an earth-vertical axis of ±10° at frequencies of 0.16, 0.32, and 0.50 Hz (VO-25; Interacoustics USA, Eden Prairie, MN, USA). 
Video-oculography (VOG) Recordings
Eye movements were measured using binocular infrared VOG (Sensorimotoric Instruments, Berlin, Germany) that samples at 60 Hz with a resolution of 0.1° and a calibrated accuracy of 0.5° in children. The VOG recordings and target position data for saccades, smooth pursuits, horizontal OKN, and VOR were exported and analyzed offline using several analysis programs. A custom interactive program (written by co-author JPK) was used to analyze saccades, smooth pursuit, and OKN data. Each VOG recording was manually edited to remove recording artifacts. Individual saccades in the direction of the target step were analyzed using a settable velocity criterion (>30°/s). Each saccade was then analyzed to extract saccade amplitude, peak velocity, and latency to onset from the target step. Saccade peak velocities were derived from filtered position traces (frequency roll-off −3.0 dB at 15 Hz). Saccade gain was calculated as saccade amplitude/target step amplitude. Analysis of sinusoidal smooth pursuit gain was performed by desaccading the recorded eye position traces based on a settable velocity criterion, and then fitting slow-phase eye velocity to a sinusoid of the same frequency as that of the target motion using a least squares algorithm. Smooth pursuit gain, calculated as the ratio of the fit to desaccaded eye velocity divided by the fit to target velocity, was averaged across cycles. Sinusoidal VOR was analyzed using a similar approach. Eye velocity traces were desaccaded and accumulated for multiple cycles of chair rotation and then fit with a least squares approximation to a sine wave at the frequency of the rotation. The gain, phase, and symmetry of the response were calculated. Optokinetic nystagmus velocity was calculated for each slow phase using a settable velocity criterion to define fast phase start and end, thereby defining the intervening slow-phase eye movement. Optokinetic nystagmus gain was defined as the average velocity of all slow phases divided by the corresponding stimulus velocity. 
Prediction of Eye Position Errors
Torsion of the rectus muscle pulleys was obtained from measurements in a previous study.13 In brief, rectus muscle pulley locations were obtained from high-resolution CT images. The relative horizontal position of the superior and inferior (SR/IR) and medial and lateral (MR/LR) rectus muscle pulleys was determined from coronal images normalized in a craniotopic coordinate system. The predicted eye alignment due to rectus muscle pulley displacements were simulated in Orbit 1.8 (Eidactics, San Francisco, CA, USA; http://eidactics.com, in the public domain). Predicted eye position due to torsion of the rectus muscle pulleys of the nonfixating eye was plotted at ±30° eccentricity in 5° steps on a Hess-Lancaster chart in Fick coordinates. The two-dimensional representations of saccades and smooth pursuit eye movements were superimposed on the corresponding Hess-Lancaster chart generated by Orbit 1.8. All coordinates were adjusted for sign, which Orbit 1.8 defines positive directions from the origin as abduction, elevation, and extorsion. The fixating eye was assumed to be the eye showing movement in the appropriate direction. 
Results
The clinical findings and surgical history of the 10 subjects are shown in the Table. Five of the 10 subjects had normal eye alignment in primary gaze. Four subjects had a V-pattern exotropia and one subject had an A-pattern esotropia. Overelevation in adduction either due to extorsion of the rectus muscle pulley or inferior oblique overaction was observed clinically or documented by eye movement recordings in each of the subjects. Eight of the 10 subjects demonstrated stable gaze holding in primary gaze and at eccentricities of 15° up, down, right, and left. Subject 1 had a constant velocity vestibular nystagmus. Two subjects (5 and 10) had a ventricular peritoneal shunt for an Arnold-Chiari malformation, one of which displayed a down-beating nystagmus. The ages at the time of eye movement testing are shown in the Table
Table
 
Clinical Findings and Surgical History
Table
 
Clinical Findings and Surgical History
Saccades
Figure 1 shows the left eye VOG recording of subject 4 with a V-pattern exotropia demonstrating accurate horizontal saccades of the fixating eye to pseudorandom, target steps with intrusion of a small vertical component. Figures 2A and 2E show the relationship of horizontal and vertical saccade amplitude to target amplitude for subjects with and without pattern strabismus. The average gain (and SD) across all horizontal target amplitudes was 0.93 (0.24) for the fixating eye in subjects with strabismus, 0.77 (0.25) for the nonfixating eye in subjects with strabismus, 0.79 (0.12) for subjects without strabismus, and 0.85 (0.07) in age-matched controls. For vertical targets, average gain was 1.0 (0.47) for the fixating eye in subjects with strabismus, 0.79 (0.28) for the nonfixating eye in subjects with strabismus, 0.89 (0.24) for subjects without strabismus, and 0.90 (0.15) in age-matched controls. There were no significant differences in the means of the average gains between controls and the fixating eye in subjects with strabismus, the nonfixating eye in subjects with strabismus, or subjects without strabismus, for either horizontal or vertical targets (all P ≥ 0.06). Of note, the average gains determined from the slopes of the regressions in Figure 2 were within 0.1 of the averaged gains. Our control subjects show horizontal saccade gains (0.85) that are identical to those reported in age-similar controls.1618 The SD of the gains, however, was significantly greater in both CS groups than in controls. 
Figure 1
 
Saccadic eye movements to horizontally stepped targets from subject 4 with V-pattern exotropia. The top trace shows vertical eye movements in which upward deflections are upward eye movements. The lower trace shows horizontal eye movements in which upward deflections are rightward movements and downward deflections are leftward movements. The target (gray line) is stepped 5° to 20° (gray line). A brief segment has been removed due to a blink artifact.
Figure 1
 
Saccadic eye movements to horizontally stepped targets from subject 4 with V-pattern exotropia. The top trace shows vertical eye movements in which upward deflections are upward eye movements. The lower trace shows horizontal eye movements in which upward deflections are rightward movements and downward deflections are leftward movements. The target (gray line) is stepped 5° to 20° (gray line). A brief segment has been removed due to a blink artifact.
Figure 2
 
Saccade gains to horizontal (A) and vertical (E) target steps. For horizontal targets, positive and negative values on the x-axis represent rightward and leftward displacements in degrees, respectively. For vertical targets, positive and negative values on the x-axis represent upward and downward displacements in degrees, respectively. Filled circles and crosses represent the fixating and nonfixating eye in subjects with pattern strabismus, respectively. Open circles represent each eye from subjects without strabismus. Average saccade gain is represented by linear regressions for subjects with and without strabismus (as shown by the figure legend at the top). Insets to the right demonstrate each individual's data connected by lines for the fixating eye in subjects with pattern strabismus (B, F), the nonfixating eye in subjects with pattern strabismus (C, G), and each eye in subjects without strabismus (D, H). The shaded areas are 95% confidence intervals of the means from controls.
Figure 2
 
Saccade gains to horizontal (A) and vertical (E) target steps. For horizontal targets, positive and negative values on the x-axis represent rightward and leftward displacements in degrees, respectively. For vertical targets, positive and negative values on the x-axis represent upward and downward displacements in degrees, respectively. Filled circles and crosses represent the fixating and nonfixating eye in subjects with pattern strabismus, respectively. Open circles represent each eye from subjects without strabismus. Average saccade gain is represented by linear regressions for subjects with and without strabismus (as shown by the figure legend at the top). Insets to the right demonstrate each individual's data connected by lines for the fixating eye in subjects with pattern strabismus (B, F), the nonfixating eye in subjects with pattern strabismus (C, G), and each eye in subjects without strabismus (D, H). The shaded areas are 95% confidence intervals of the means from controls.
Horizontal saccade gains for individual subjects are shown in the insets on the right side of Figure 2 for the fixating eye (Fig. 2B), the nonfixating eye (Fig. 2C) in subjects with pattern strabismus, and all eyes in subjects without strabismus (Fig. 2D). Overall, subjects with pattern strabismus had greater variation in horizontal saccade gain compared with CS subjects without strabismus and controls (F-test; P < 0.0001 and P < 0.001, respectively). Documentation of normal visual acuities in all subjects (excluding subject 4) indicates that monocular positional uncertainty associated with amblyopia did not underlie the variability in saccadic gains.19 The large variability in gain at small target steps is likely due to amplification of measurement errors and small head movements. 
Vertical saccade gains for individual subjects are shown in the insets on the right side of Figure 2 for the fixating eye (Fig. 2F) and the nonfixating eye (Fig. 2G) in subjects with pattern strabismus, and each eye in subjects without strabismus (Fig. 2H). Vertical saccade gains show greater variability in subjects with strabismus compared with subjects without strabismus and controls (F-test; P < 0.0001 and P < 0.0001, respectively). Vertical saccades were hypermetric in subject 1, who had marked overelevation in adduction, constant velocity left-beating oblique nystagmus, and three previous craniotomies. 
Next we addressed whether saccades followed the main sequence, which describes the nonlinear increases in saccade peak velocity with increasing saccade amplitudes.20,21 The left column of Figure 3 plots the main sequence for horizontal saccades of the fixating eye (Fig. 3A) and the nonfixating eye (Fig. 3B) in subjects with pattern strabismus, and both eyes in subjects without strabismus (Fig. 3C). Figures 3D through 3F show the corresponding data for vertical saccades. Both horizontal and vertical saccades of each subject follow the main sequence regardless of eye alignment and overlap with the main sequence of controls. 
Figure 3
 
The relationship between saccade peak velocity (°/s) and saccade amplitude for horizontal and vertical target steps (left and right columns, respectively). The fixating eye in subjects with pattern strabismus is plotted in (A) and (D). The nonfixating eye in subjects with pattern strabismus is plotted in (B) and (E). Each eye in subjects without strabismus is plotted in (C) and (F). Overlaid curves represent a third-order polynomial curve fit to each subject's data. For horizontal targets, positive and negative values on the x-axis represent rightward and leftward saccades in degrees, respectively. For vertical targets, positive and negative values on the x-axis represent upward and downward saccades in degrees, respectively. Gray symbols are data from controls.
Figure 3
 
The relationship between saccade peak velocity (°/s) and saccade amplitude for horizontal and vertical target steps (left and right columns, respectively). The fixating eye in subjects with pattern strabismus is plotted in (A) and (D). The nonfixating eye in subjects with pattern strabismus is plotted in (B) and (E). Each eye in subjects without strabismus is plotted in (C) and (F). Overlaid curves represent a third-order polynomial curve fit to each subject's data. For horizontal targets, positive and negative values on the x-axis represent rightward and leftward saccades in degrees, respectively. For vertical targets, positive and negative values on the x-axis represent upward and downward saccades in degrees, respectively. Gray symbols are data from controls.
To graphically describe the saccadic trajectory of each eye, we superimposed the two-dimensional scan paths of serial saccades from each eye on the estimated Hess-Lancaster plots generated from Orbit 1.8 (Fig. 4). The scan paths of the right eye align on a target stepped horizontally or vertically, despite globe extorsion. The scan path of the left (nonfixating) eye has large position errors related to globe extorsion that are predicted by the Hess-Lancaster plot from Orbit 1.8. 
Figure 4
 
Saccadic eye movements from a subject with a large V-pattern exotropia superimposed on the predicted horizontal and vertical eye positions. Black lines are two-dimensional eye trajectories to horizontal or vertical step targets (continuous recordings from two different test sessions). The movements of the right (fixating) eye are aligned with the target. The blue circles connected with blue lines are predicted gaze positions by Orbit 1.8 software (Hess-Lancaster plot) adjusted for rectus pulley torsion measured from CT scans. The left Hess-Lancaster plot predicts left eye position if the right eye is fixating. The right Hess-Lancaster plot predicts right eye position if the left eye is fixating. Upward and downward eye positions represent upgaze and downgaze, respectively. Horizontal eye positions are noted on each plot by abduction and adduction.
Figure 4
 
Saccadic eye movements from a subject with a large V-pattern exotropia superimposed on the predicted horizontal and vertical eye positions. Black lines are two-dimensional eye trajectories to horizontal or vertical step targets (continuous recordings from two different test sessions). The movements of the right (fixating) eye are aligned with the target. The blue circles connected with blue lines are predicted gaze positions by Orbit 1.8 software (Hess-Lancaster plot) adjusted for rectus pulley torsion measured from CT scans. The left Hess-Lancaster plot predicts left eye position if the right eye is fixating. The right Hess-Lancaster plot predicts right eye position if the left eye is fixating. Upward and downward eye positions represent upgaze and downgaze, respectively. Horizontal eye positions are noted on each plot by abduction and adduction.
Smooth Pursuit
Figure 5 shows horizontal smooth pursuit gains for subjects with and without pattern strabismus. The averages at each pursuit velocity represent 1 to 14 cycles from each subject (mean 8.4 cycles). Gains of the fixating eye in subjects with strabismus were at the lower range of controls, but did not significantly differ from controls (F = 2.0; P = 0.18). Gains in subjects without strabismus were at the upper range of controls, but again did not significantly differ from controls (F = 1.9; P = 0.19). Despite having gains in the normal range, subjects with strabismus had lower gain in the fixating eye compared with subjects without strabismus (repeated measures ANOVA; F = 6.8; P = 0.04). The average phase leads for the fixating eye in subjects with strabismus was 5.2°, 7.9°, and 14.8° at target velocities of 10°, 20°, and 30°, respectively. For subjects without strabismus, the respective phase leads were 4.2°, 10.3°, and 17.7°. For controls, respective phase leads were 4.6°, 9.7°, and 15.7°. 
Figure 5
 
Smooth pursuit gains to a target drifting sinusoidally ±10° at velocities of 10, 20, or 30°/s. Error bars are 95% confidence intervals of the mean. The shaded areas are 95% confidence intervals of the mean from controls.
Figure 5
 
Smooth pursuit gains to a target drifting sinusoidally ±10° at velocities of 10, 20, or 30°/s. Error bars are 95% confidence intervals of the mean. The shaded areas are 95% confidence intervals of the mean from controls.
Figure 6 shows representative horizontal smooth pursuit data from a subject with V-pattern exotropia. The tracing demonstrates consistent tracking, but overall gain was 0.56, consistent with the frequent occurrence of corrective saccades. In general, subjects with low smooth pursuit gains demonstrated a higher frequency of catch-up saccades that increased with increasing target velocity. For all subjects, there was no change in smooth pursuit gain with increasing cycle number (R2 = 0.001). 
Figure 6
 
Smooth pursuit eye movements of each eye from subject 4 with a V-pattern exotropia. The top and middle traces show vertical and horizontal eye movements, respectively. The lower trace shows the target in horizontal sinusoidal motion. Eye movement conventions are the same as in Figure 1. The lower half of the figure shows the velocity traces for the corresponding horizontal and vertical eye movements and target motion.
Figure 6
 
Smooth pursuit eye movements of each eye from subject 4 with a V-pattern exotropia. The top and middle traces show vertical and horizontal eye movements, respectively. The lower trace shows the target in horizontal sinusoidal motion. Eye movement conventions are the same as in Figure 1. The lower half of the figure shows the velocity traces for the corresponding horizontal and vertical eye movements and target motion.
Figure 7 shows two-dimensional eye movement positions of each eye during smooth pursuit from a subject with a large V-pattern exotropia. The two-dimensional scan paths are superimposed on the Hess-Lancaster plots generated from Orbit 1.8. Notice that the left (fixating) eye is correctly following the horizontal motion of the pursuit stimulus. In comparison, the trajectory of the right (nonfixating) eye aligns with the Hess-Lancaster plot, indicating that its position error approximates that predicted from extorsion of the rectus muscle pulleys. 
Figure 7
 
Smooth pursuit eye movement recordings from subject 5 with a large V-pattern exotropia superimposed on predicted horizontal and vertical eye positions. Black lines are two-dimensional eye movements recorded to a target moving in a horizontal sinusoid motion at a peak velocity of 30°/s. The left eye is the fixating eye, as eye movements are aligned to the target. The blue open circles connected with blue lines are gaze positions predicted by Orbit 1.8 software (Hess-Lancaster plot) adjusted for rectus pulley torsion measured from CT scans. Conventions are the same as in Figure 4.
Figure 7
 
Smooth pursuit eye movement recordings from subject 5 with a large V-pattern exotropia superimposed on predicted horizontal and vertical eye positions. Black lines are two-dimensional eye movements recorded to a target moving in a horizontal sinusoid motion at a peak velocity of 30°/s. The left eye is the fixating eye, as eye movements are aligned to the target. The blue open circles connected with blue lines are gaze positions predicted by Orbit 1.8 software (Hess-Lancaster plot) adjusted for rectus pulley torsion measured from CT scans. Conventions are the same as in Figure 4.
Optokinetic Nystagmus
Figure 8 plots horizontal OKN gains for the five subjects with pattern strabismus and five subjects without strabismus. For subjects without strabismus, the average gains of both eyes are plotted; for strabismic subjects, only the gains of the fixating eye are shown. Optokinetic nystagmus gains were significantly reduced in both groups of CS subjects (t-test: pattern strabismus versus controls P < 0.0001 for all velocities; P values for those without strabismus versus controls was 0.020, <0.00001, and 0.001 for 15, 30, and 45°/s, respectively). Subjects without pattern strabismus had an interocular asymmetry in gain that ranged from 0.01 to 0.13. Subjects with pattern strabismus had an interocular asymmetry in gain that ranged from 0.01 to 0.42. Vertical eye movements were often seen during OKN stimulation. Analysis of gaze-holding data revealed the variable presence of a vertical component that was associated with decreased OKN gain in subjects with and without strabismus. The subject in Figure 8B with reduced OKN gain has horizontal or vertical deviations between eyes that were not detected on clinical examination. However, the subject in Figure 8C with high OKN gain has no interocular horizontal or vertical deviation. The remaining three subjects with no clinical evidence of strabismus had similar relationships between eye alignment and OKN gain. 
Figure 8
 
(A) Optokinetic nystagmus gains across three velocities. Filled circles are from five subjects with pattern strabismus. Open circles are from five subjects without pattern strabismus. Error bars are 95% confidence intervals of the mean. The shaded areas are 95% confidence intervals of the mean from controls. (B, C) Two-dimensional eye positions recorded during a gaze holding to targets placed at center and at 15 degrees left, right, up, and down. The right and left eyes are plotted in black and blue, respectively. The R, L, U, and D represent right, left, up, and down, respectively. (B) Subject 6, who has low gain to the OKN stimulus of 45°/s, shows small interocular disparities in eye alignment between gaze locations. (C) Subject 9, who has high gain to the OKN stimulus of 45°/s, shows better interocular eye alignment across gaze locations.
Figure 8
 
(A) Optokinetic nystagmus gains across three velocities. Filled circles are from five subjects with pattern strabismus. Open circles are from five subjects without pattern strabismus. Error bars are 95% confidence intervals of the mean. The shaded areas are 95% confidence intervals of the mean from controls. (B, C) Two-dimensional eye positions recorded during a gaze holding to targets placed at center and at 15 degrees left, right, up, and down. The right and left eyes are plotted in black and blue, respectively. The R, L, U, and D represent right, left, up, and down, respectively. (B) Subject 6, who has low gain to the OKN stimulus of 45°/s, shows small interocular disparities in eye alignment between gaze locations. (C) Subject 9, who has high gain to the OKN stimulus of 45°/s, shows better interocular eye alignment across gaze locations.
Vestibulo-Ocular Reflex
Seven of the 10 subjects had adequate VOR data to chair rotation at frequencies of 0.16, 0.32, and 0.50 Hz. All subjects had VOR gains greater than 0.5 across all rotation frequencies (Fig. 9A). The corresponding phase of the VOR ranged from 165.1 to 195.5° at 0.16 Hz, 175.0 to 207.1° at 0.32 Hz, and 180.0 to 217.9° at 0.50 Hz. Three subjects were excluded due to intolerance of chair rotation testing and constant velocity jerk nystagmus (subject 1), bilateral conductive hearing loss (subject 2), and three suboccipital craniectomies for an Arnold-Chiari malformation type 1 (subject 5). Vertical eye movements were seen in all seven subjects during VOR stimulation. Figure 9B shows a subject in which the left eye demonstrates overelevation in adduction that exceeded the prediction of the Hess-Lancaster plot generated by Orbit that was presumably due to inferior oblique overaction. The right eye follows the prediction of the Hess-Lancaster plot generated by Orbit. 
Figure 9
 
(A) Vestibulo-ocular reflex gains in seven subjects to whole chair rotation about an earth-vertical axis to a peak velocity of 60°/s (0.16, 0.32, and 0.50 Hz). Filled circles are subjects with pattern strabismus. Open circles are subjects without pattern strabismus. The shaded areas are means ± 95% confidence intervals from normative data. (B) Two-dimensional scan paths from subject 7 recorded during the VOR test (black lines). The blue lines are predicted gaze positions by Orbit 1.8 software (Hess-Lancaster plot) adjusted for rectus pulley torsion measured from CT scans. Conventions are the same as in Figure 4.
Figure 9
 
(A) Vestibulo-ocular reflex gains in seven subjects to whole chair rotation about an earth-vertical axis to a peak velocity of 60°/s (0.16, 0.32, and 0.50 Hz). Filled circles are subjects with pattern strabismus. Open circles are subjects without pattern strabismus. The shaded areas are means ± 95% confidence intervals from normative data. (B) Two-dimensional scan paths from subject 7 recorded during the VOR test (black lines). The blue lines are predicted gaze positions by Orbit 1.8 software (Hess-Lancaster plot) adjusted for rectus pulley torsion measured from CT scans. Conventions are the same as in Figure 4.
Discussion
We show that subjects with CS on average generated accurate saccades in response to targets stepped horizontally or vertically. This finding was true for subjects with and without pattern strabismus, indicating that saccades are not impacted by extorsion of the rectus muscle pulleys that result in shifting disparities in horizontal and vertical eye position. Saccades are ballistic eye movements of short duration (40–100 ms) that are generated “open-loop” without visual feedback and of fixed amplitude based on the distance of the target relative to the fovea.20,21 We also examined the main sequence, which refers to the tight relationship between saccade amplitude and velocity. Previous studies have shown that the amplitude of horizontal and vertical saccades is proportional to the number of spike and burst frequencies of the paramedian pontine and mesencephalic reticular formations, respectively.22 Therefore, saccade amplitude is highly correlated with peak saccadic velocity. We found that the saccades of subjects with and without strabismus followed the main sequence for horizontal and vertical saccades.23,24 Confirmation that the fixating and nonfixating eyes of subjects with pattern strabismus on average followed the main sequence is consistent with normal behaviors of the saccadic circuitry. However, analysis of individual trials revealed variability of saccade gains likely related to imprecise targeting due to the conflicting information provided by the extorted eyes. 
Smooth pursuit gains of subjects without strabismus were within the upper limits of the normal range, indicating that the orbital abnormalities of CS did not impact this volitional eye movement. In contrast, SP gains in subjects with strabismus were within the lower limits of the normal range, but were significantly lower than those without strabismus. For subjects with strabismus, the trajectory of smooth eye movements predicted by Orbit aligned with extorted rotation axes. However, the eye movements demonstrated shifting disparities in eye alignment and catch-up saccades, consistent with visual feedback. The attentional shifts that accompany alternating fixation in subjects with a pattern strabismus likely account for the lower smooth pursuit gains in subjects with strabismus. In CS with strabismus, target locations in retinotopic coordinates are rotated clockwise in one eye and counterclockwise in the fellow eye. To overcome this conflicting visual sensory input between the two eyes, the subject selectively tracks the target with one eye. However, alternating fixation between eyes leads to reductions in smooth pursuit gain owing to the delayed visual feedback associated with divided attention to competing retinotopic representations of the target trajectory.2529 
Horizontal OKN gains were reduced in CS subjects with and without strabismus. Horizontal OKN is a conjugate eye movement that helps to stabilize visual images during motion of the visual world relative to the retina. Coupling of motion-selective OKN and sensitivity to binocular disparities at a defined distance has been postulated to stabilize the images within Panum's fusional area and to underlie the rejection of motion signals outside this area.30 Howard and Gonzalez30 showed that horizontal OKN gains remained normal on introduction of a fusible horizontal disparity, but were significantly reduced in response to a vertical disparity of similar magnitude. Of note, the range of stimulus velocities (15, 26, and 34°/s) for eliciting OKN overlaps with those used in this study. Interocular disparities in vertical eye position were recorded during gaze holding in primary and eccentric gaze positions in all CS patients. 
Horizontal OKN gains were reduced more in CS patients with strabismus than CS patients without strabismus. The most obvious differences in the two populations are the presence of strabismus and extorsion of the two eyes viewing the stimulus. Exotropia and globe extorsion are associated with suppression of conflicting visual inputs, which partially accounts for the reduced OKN gains. Exotropic patients demonstrate splitting of the visual field during dichoptic viewing with suppression of part of the temporal retina in each eye, to avoid diplopia and confusion.31 Additionally, humans and cats with congenital strabismus show bidirectional reductions of gains for monocular horizontal OKN, implicating abnormalities in cortical processing of visual motion.32,33 Furthermore, cross-orientation masking may contribute to the reduced horizontal OKN in CS subjects in whom OKN gratings are rotated clockwise in one eye and counterclockwise in the other eye.34,35 Presentation of cross-oriented gratings under binocular viewing has been shown to raise the detection threshold of the fellow eye owing to cortical suppression.35 
The consistent finding of normal angular VOR in patients without pathology of the vestibular organ or vestibulo-cerebellum indicated that the direct VOR pathway is intact in CS.21 The observation that VOR gains were uniformly normal indicated that the VOR was matched to the velocity of the horizontal component during sinusoidal rotation in subjects with and without pattern strabismus. The uniform presence of an off-axis vertical component in subjects with pattern strabismus due to globe extorsion is consistent with encoding of the VOR in craniotopic coordinates. Of note, the vertical deviations observed during horizontal VOR can be attributed to globe extorsion, inferior oblique overaction, or both. When the slope of the off-axis vertical component in eccentric gazes matches the linear increase predicted by Orbit, the vertical deviation can safely be attributed to globe extorsion. In contrast, a vertical deviation showing nonlinear increases in lateral gaze is hard to explain without invoking inferior oblique overaction. 
Although the globe is extorted in subjects with CS having strabismus, the rectus muscle pulleys and retina are rotated by the same amount in the same direction. That is, the mapping between visual inputs in retinal coordinates and rotation axes of the rectus extraocular muscles are in spatial register. A purely horizontal target displacement in the world results in an oblique displacement in retinotopic coordinates, which generates an oblique eye movement with respect to the visual axis and the oculomotor plant. That oblique eye movement is identical to a comparable oblique eye movement in a healthy subject, but it produces a horizontal and vertical displacement of the extorted eye in the world. Therefore, to the extent that both the visual sensory input and the motor machinery maintain a consistent relationship, no adaptation is required to maintain the accuracy and kinematics of the resulting eye movements. 
Subjects with CS and strabismus have an extorted retinotopic view that conflicts with the spatiotopic representation of the world. That is, the visual perception of earth-vertical and the coordination of eye, head, and body movements must adapt for the extorted retinotopic view. The most parsimonious solution to this problem is cortical re-mapping of the spatial representation of the visual field in early visual cortical areas, higher visual sensory areas, and the gain fields of visuomotor areas.3640 
Acknowledgments
Preliminary results from this study were presented at the annual meeting for the Association for Research in Vision and Ophthalmology, Seattle, Washington, United States, 2014. 
Supported by an unrestricted grant from the Peter LeHaye, Barbara Anderson, and William O. Rogers Endowment Funds. 
Disclosure: A.H. Weiss, None; J.P. Kelly, None; R.A. Hopper, None; J.O. Phillips, None 
References
Kreiborg S. Postnatal growth and development of the craniofacial complex in premature craniosynostosis. In: Cohen MM,Jr MacLean RE, eds. Craniosynostosis: Diagnosis, Evaluation, and Management. 2nd ed. New York, NY: Oxford University Press; 2000: 158–174.
Kreiborg S, Cohen MM,Jr. Ocular manifestations of Apert and Crouzon syndromes: qualitative and quantitative findings. J Craniofac Surg. 2010; 21: 1354–1357.
Fries PD, Katowitz JA. Congenital craniofacial anomalies of ophthalmic importance. Surv Ophthalmol. 1990; 35: 87–119.
Tuite GF, Chong WK, Evanson J, et al. The effectiveness of papilledema as an indicator of raised intracranial pressure in children with craniosynostosis. Neurosurgery. 1996; 38: 272–278.
Connolly JP, Gruss J, Seto ML, et al. Progressive postnatal craniosynostosis and increased intracranial pressure. Plast Reconstr Surg. 2004; 113: 1313–1323.
Liasis A, Nischal KK, Walters B, et al. Monitoring visual function in children with syndromic craniosynostosis: a comparison of 3 methods. Arch Ophthalmol. 2006; 124: 1119–1126.
McCarthy JG, Glasberg SB, Cutting CB, et al. Twenty-year experience with early surgery for craniosynostosis: II. The craniofacial synostosis syndromes and pansynostosis—results and unsolved problems. Plast Reconstr Surg. 1995; 96: 284–295.
Shetye PR, Boutros S, Grayson BH, McCarthy JG. Midterm follow-up of midface distraction for syndromic craniosynostosis: a clinical and cephalometric study. Plast Reconstr Surg. 2007; 120: 1621–1632.
Hopper RA, Sandercoe G, Woo A, et al. Computed tomographic analysis of temporal maxillary stability and pterygomaxillary generate formation following pediatric Le Fort III distraction advancement. Plast Reconstr Surg. 2010; 126: 1665–1674.
Diamond GR, Whitaker L. Ocular motility in craniofacial reconstruction. Plast Reconstr Surg. 1984; 73: 31–37.
Coats DK, Paysse EA, Stager DR. Surgical management of V-pattern strabismus and oblique dysfunction in craniofacial dysostosis. J AAPOS. 2000; 4: 338–342.
Tan KP, Sargent MA, Poskitt KJ, Lyons CJ. Ocular overelevation in adduction in craniosynostosis: is it the result of excyclorotation of the extraocular muscles? J AAPOS. 2005; 9: 550–557.
Weiss AH, Phillips J, Kelly JP. Crouzon syndrome: relationship of rectus muscle pulley location to pattern strabismus. Invest Ophthalmol Vis Sci. 2014; 55: 310–317.
Yee RD, Daniels SA, Jones OW, Baloh RW, Honrubia V. Effects of an optokinetic background on pursuit eye movements. Invest Ophthalmol Vis Sci. 1983; 24: 1115–1122.
Collewijn H, Tamminga EP. Human smooth and saccadic eye movements during voluntary pursuit of different target motions on different backgrounds. J Physiol. 1984; 351: 217–250.
Munoz DP, Broughton JR, Goldring JE, Armstrong IT. Age related performance of human subjects on saccadic eye movement tasks. Exp Brain Res. 1998; 121: 391–400.
Yang Q, Kapoula Z. Binocular coordination of saccades at far and at near in children and in adults. J Vis. 2003; 3 (8): 554–561.
Irving EL, Steinbach MJ, Lillakas L, Babu RJ, Hutchings N. Horizontal saccade dynamics across the human life span. Invest Ophthalmol Vis Sci. 2006; 47: 2478–2484.
Raashid RA, Wong AM, Chandrakumar M, Blakeman A, Goltz HC. Short-term saccadic adaptation in patients with anisometropic amblyopia. Invest Ophthalmol Vis Sci. 2013; 54: 6701–6711.
Moschovakis A, Scudder C, Highstein S. The microscopic anatomy and physiology of the mammalian saccadic system. Prog Neurobiol. 1996; 90: 133–254.
Leigh RJ, Zee D. The Neurology of Eye Movements. New York: Oxford University Press; 2006: 20–81.
Scudder CA, Kaneko CS, Fuchs AF. The brainstem burst generator for saccadic eye movements: a modern synthesis. Exp Brain Res. 2002; 142: 439–462.
Becker W, Fuchs AF. Further properties of the human saccadic system: eye movements and correction saccades with and without visual fixation points. Vision Res. 1969; 9: 1247–1258.
Baloh RW, Sills AW, Kumley WE, Honrubia V. Quantitative measurement of saccade amplitude, duration, and velocity. Neurology. 1975; 25: 1065–1070.
Carl JR, Gellman RS. Human smooth pursuit: stimulus-dependent responses. J Neurophysiol. 1987; 57: 1446–1463.
Lisberger SG. Postsaccadic enhancement of initiation of smooth pursuit eye movements in monkeys. J Neurophysiol. 1998; 79: 1918–1930.
Kowler E, Martins AJ, Pavel M. The effect of expectations on slow oculomotor control—IV. Anticipatory smooth eye movements depend on prior target motions. Vision Res. 1984; 24: 197–210.
Kowler E, Aitkin CD, Ross NM, Santos EM, Zhao M. Davida Teller Award Lecture 2013: the importance of prediction and anticipation in the control of smooth pursuit eye movements. J Vis. 2014; 14 (5): 10.
Chappell M, Potter Z, Hine TJ, Mullen KT, Shand J. Reducing magnocellular processing of various motion trajectories tests single process theories of visual position perception. J Vis. 2013; 13 (10): 1–12.
Howard IP, Gonzalez EG. Human optokinetic nystagmus in response to moving binocularly disparate stimuli. Vision Res. 1987; 27: 1807–1816.
Economides JR, Adams DL, Horton JC. Perception via the deviated eye in strabismus. J Neurosci. 2012; 32: 10286–10295.
Valmaggia C, Proudlock F, Gottlob I. Optokinetic nystagmus in strabismus: are asymmetries related to binocularity? Invest Ophthalmol Vis Sci. 2003; 44: 5142–5150.
Hoffmann KP, Distler C, Markner C. Optokinetic nystagmus in cats with congenital strabismus. J Neurophysiol. 1996; 75: 1495–1502.
DeAngelis GC, Robson JG, Ohzawa I, Freeman RD. Organization of suppression in receptive fields of neurons in cat visual cortex. J Neurophysiol. 1992; 68: 144–163.
Li B, Peterson MR, Thompson JK, Duong T, Freeman RD. Cross-orientation suppression: monoptic and dichoptic mechanisms are different. J Neurophysiol. 2005; 94: 1645–1650.
Sugita Y. Global plasticity in adult visual cortex following reversal of visual input. Nature. 1996; 380: 523–526.
Fiser J, Chiu C, Weliky M. Small modulation of ongoing cortical dynamics by sensory input during natural vision. Nature. 2004; 431: 573–578.
Fernandez-Ruiz J, Diaz R, Moreno-Briseño P, Campos-Romo A, Ojeda R. Rapid topographical plasticity of the visuomotor spatial transformation. J Neurosci. 2006; 26: 1986–1990.
Karkhanis AN, Heider B, Silva FM, Siegel RM. Spatial effects of shifting prisms on properties of posterior parietal cortex neurons. J Physiol. 2014; 592: 3625–3646.
Luauté J, Schwartz S, Rossetti Y, et al. Dynamic changes in brain activity during prism adaptation. J Neurosci. 2009; 29: 169–178.
Figure 1
 
Saccadic eye movements to horizontally stepped targets from subject 4 with V-pattern exotropia. The top trace shows vertical eye movements in which upward deflections are upward eye movements. The lower trace shows horizontal eye movements in which upward deflections are rightward movements and downward deflections are leftward movements. The target (gray line) is stepped 5° to 20° (gray line). A brief segment has been removed due to a blink artifact.
Figure 1
 
Saccadic eye movements to horizontally stepped targets from subject 4 with V-pattern exotropia. The top trace shows vertical eye movements in which upward deflections are upward eye movements. The lower trace shows horizontal eye movements in which upward deflections are rightward movements and downward deflections are leftward movements. The target (gray line) is stepped 5° to 20° (gray line). A brief segment has been removed due to a blink artifact.
Figure 2
 
Saccade gains to horizontal (A) and vertical (E) target steps. For horizontal targets, positive and negative values on the x-axis represent rightward and leftward displacements in degrees, respectively. For vertical targets, positive and negative values on the x-axis represent upward and downward displacements in degrees, respectively. Filled circles and crosses represent the fixating and nonfixating eye in subjects with pattern strabismus, respectively. Open circles represent each eye from subjects without strabismus. Average saccade gain is represented by linear regressions for subjects with and without strabismus (as shown by the figure legend at the top). Insets to the right demonstrate each individual's data connected by lines for the fixating eye in subjects with pattern strabismus (B, F), the nonfixating eye in subjects with pattern strabismus (C, G), and each eye in subjects without strabismus (D, H). The shaded areas are 95% confidence intervals of the means from controls.
Figure 2
 
Saccade gains to horizontal (A) and vertical (E) target steps. For horizontal targets, positive and negative values on the x-axis represent rightward and leftward displacements in degrees, respectively. For vertical targets, positive and negative values on the x-axis represent upward and downward displacements in degrees, respectively. Filled circles and crosses represent the fixating and nonfixating eye in subjects with pattern strabismus, respectively. Open circles represent each eye from subjects without strabismus. Average saccade gain is represented by linear regressions for subjects with and without strabismus (as shown by the figure legend at the top). Insets to the right demonstrate each individual's data connected by lines for the fixating eye in subjects with pattern strabismus (B, F), the nonfixating eye in subjects with pattern strabismus (C, G), and each eye in subjects without strabismus (D, H). The shaded areas are 95% confidence intervals of the means from controls.
Figure 3
 
The relationship between saccade peak velocity (°/s) and saccade amplitude for horizontal and vertical target steps (left and right columns, respectively). The fixating eye in subjects with pattern strabismus is plotted in (A) and (D). The nonfixating eye in subjects with pattern strabismus is plotted in (B) and (E). Each eye in subjects without strabismus is plotted in (C) and (F). Overlaid curves represent a third-order polynomial curve fit to each subject's data. For horizontal targets, positive and negative values on the x-axis represent rightward and leftward saccades in degrees, respectively. For vertical targets, positive and negative values on the x-axis represent upward and downward saccades in degrees, respectively. Gray symbols are data from controls.
Figure 3
 
The relationship between saccade peak velocity (°/s) and saccade amplitude for horizontal and vertical target steps (left and right columns, respectively). The fixating eye in subjects with pattern strabismus is plotted in (A) and (D). The nonfixating eye in subjects with pattern strabismus is plotted in (B) and (E). Each eye in subjects without strabismus is plotted in (C) and (F). Overlaid curves represent a third-order polynomial curve fit to each subject's data. For horizontal targets, positive and negative values on the x-axis represent rightward and leftward saccades in degrees, respectively. For vertical targets, positive and negative values on the x-axis represent upward and downward saccades in degrees, respectively. Gray symbols are data from controls.
Figure 4
 
Saccadic eye movements from a subject with a large V-pattern exotropia superimposed on the predicted horizontal and vertical eye positions. Black lines are two-dimensional eye trajectories to horizontal or vertical step targets (continuous recordings from two different test sessions). The movements of the right (fixating) eye are aligned with the target. The blue circles connected with blue lines are predicted gaze positions by Orbit 1.8 software (Hess-Lancaster plot) adjusted for rectus pulley torsion measured from CT scans. The left Hess-Lancaster plot predicts left eye position if the right eye is fixating. The right Hess-Lancaster plot predicts right eye position if the left eye is fixating. Upward and downward eye positions represent upgaze and downgaze, respectively. Horizontal eye positions are noted on each plot by abduction and adduction.
Figure 4
 
Saccadic eye movements from a subject with a large V-pattern exotropia superimposed on the predicted horizontal and vertical eye positions. Black lines are two-dimensional eye trajectories to horizontal or vertical step targets (continuous recordings from two different test sessions). The movements of the right (fixating) eye are aligned with the target. The blue circles connected with blue lines are predicted gaze positions by Orbit 1.8 software (Hess-Lancaster plot) adjusted for rectus pulley torsion measured from CT scans. The left Hess-Lancaster plot predicts left eye position if the right eye is fixating. The right Hess-Lancaster plot predicts right eye position if the left eye is fixating. Upward and downward eye positions represent upgaze and downgaze, respectively. Horizontal eye positions are noted on each plot by abduction and adduction.
Figure 5
 
Smooth pursuit gains to a target drifting sinusoidally ±10° at velocities of 10, 20, or 30°/s. Error bars are 95% confidence intervals of the mean. The shaded areas are 95% confidence intervals of the mean from controls.
Figure 5
 
Smooth pursuit gains to a target drifting sinusoidally ±10° at velocities of 10, 20, or 30°/s. Error bars are 95% confidence intervals of the mean. The shaded areas are 95% confidence intervals of the mean from controls.
Figure 6
 
Smooth pursuit eye movements of each eye from subject 4 with a V-pattern exotropia. The top and middle traces show vertical and horizontal eye movements, respectively. The lower trace shows the target in horizontal sinusoidal motion. Eye movement conventions are the same as in Figure 1. The lower half of the figure shows the velocity traces for the corresponding horizontal and vertical eye movements and target motion.
Figure 6
 
Smooth pursuit eye movements of each eye from subject 4 with a V-pattern exotropia. The top and middle traces show vertical and horizontal eye movements, respectively. The lower trace shows the target in horizontal sinusoidal motion. Eye movement conventions are the same as in Figure 1. The lower half of the figure shows the velocity traces for the corresponding horizontal and vertical eye movements and target motion.
Figure 7
 
Smooth pursuit eye movement recordings from subject 5 with a large V-pattern exotropia superimposed on predicted horizontal and vertical eye positions. Black lines are two-dimensional eye movements recorded to a target moving in a horizontal sinusoid motion at a peak velocity of 30°/s. The left eye is the fixating eye, as eye movements are aligned to the target. The blue open circles connected with blue lines are gaze positions predicted by Orbit 1.8 software (Hess-Lancaster plot) adjusted for rectus pulley torsion measured from CT scans. Conventions are the same as in Figure 4.
Figure 7
 
Smooth pursuit eye movement recordings from subject 5 with a large V-pattern exotropia superimposed on predicted horizontal and vertical eye positions. Black lines are two-dimensional eye movements recorded to a target moving in a horizontal sinusoid motion at a peak velocity of 30°/s. The left eye is the fixating eye, as eye movements are aligned to the target. The blue open circles connected with blue lines are gaze positions predicted by Orbit 1.8 software (Hess-Lancaster plot) adjusted for rectus pulley torsion measured from CT scans. Conventions are the same as in Figure 4.
Figure 8
 
(A) Optokinetic nystagmus gains across three velocities. Filled circles are from five subjects with pattern strabismus. Open circles are from five subjects without pattern strabismus. Error bars are 95% confidence intervals of the mean. The shaded areas are 95% confidence intervals of the mean from controls. (B, C) Two-dimensional eye positions recorded during a gaze holding to targets placed at center and at 15 degrees left, right, up, and down. The right and left eyes are plotted in black and blue, respectively. The R, L, U, and D represent right, left, up, and down, respectively. (B) Subject 6, who has low gain to the OKN stimulus of 45°/s, shows small interocular disparities in eye alignment between gaze locations. (C) Subject 9, who has high gain to the OKN stimulus of 45°/s, shows better interocular eye alignment across gaze locations.
Figure 8
 
(A) Optokinetic nystagmus gains across three velocities. Filled circles are from five subjects with pattern strabismus. Open circles are from five subjects without pattern strabismus. Error bars are 95% confidence intervals of the mean. The shaded areas are 95% confidence intervals of the mean from controls. (B, C) Two-dimensional eye positions recorded during a gaze holding to targets placed at center and at 15 degrees left, right, up, and down. The right and left eyes are plotted in black and blue, respectively. The R, L, U, and D represent right, left, up, and down, respectively. (B) Subject 6, who has low gain to the OKN stimulus of 45°/s, shows small interocular disparities in eye alignment between gaze locations. (C) Subject 9, who has high gain to the OKN stimulus of 45°/s, shows better interocular eye alignment across gaze locations.
Figure 9
 
(A) Vestibulo-ocular reflex gains in seven subjects to whole chair rotation about an earth-vertical axis to a peak velocity of 60°/s (0.16, 0.32, and 0.50 Hz). Filled circles are subjects with pattern strabismus. Open circles are subjects without pattern strabismus. The shaded areas are means ± 95% confidence intervals from normative data. (B) Two-dimensional scan paths from subject 7 recorded during the VOR test (black lines). The blue lines are predicted gaze positions by Orbit 1.8 software (Hess-Lancaster plot) adjusted for rectus pulley torsion measured from CT scans. Conventions are the same as in Figure 4.
Figure 9
 
(A) Vestibulo-ocular reflex gains in seven subjects to whole chair rotation about an earth-vertical axis to a peak velocity of 60°/s (0.16, 0.32, and 0.50 Hz). Filled circles are subjects with pattern strabismus. Open circles are subjects without pattern strabismus. The shaded areas are means ± 95% confidence intervals from normative data. (B) Two-dimensional scan paths from subject 7 recorded during the VOR test (black lines). The blue lines are predicted gaze positions by Orbit 1.8 software (Hess-Lancaster plot) adjusted for rectus pulley torsion measured from CT scans. Conventions are the same as in Figure 4.
Table
 
Clinical Findings and Surgical History
Table
 
Clinical Findings and Surgical History
×
×

This PDF is available to Subscribers Only

Sign in or purchase a subscription to access this content. ×

You must be signed into an individual account to use this feature.

×