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From the University of Leicester, Ophthalmology Group, Faculty of Medicine and Biological Sciences, Leicester, United Kingdom.
| Abstract |
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METHODS. Horizontal and vertical look and stare OKN gains were recorded in 15 healthy volunteers (40°/s) using new methods to delineate look and stare OKN. Responses with right and left eye viewing were compared to investigate consistency of individual OKN asymmetry. In a second experiment, the symmetry of stare OKN was measured in nine volunteers varying velocity (20°/s and 40°/s), contrast (50% and 100%), grating contrast profile (square or sine wave), and stimulus shape (full screen or circular vignetted).
RESULTS. There was no horizontal or vertical asymmetry in look or stare OKN gain for all volunteers grouped together. However, individual vertical asymmetries were strongly correlated for left and right eye viewing (look: r = 0.77, P = 0.0008; stare: r = 0.75, P = 0.001) and for look and stare OKN (r = 0.66, P = 7.3 x 10–5) because of a strong correlation for downward moving stimuli (r = 0.73, P = 0.002). Horizontal and vertical asymmetries were not significantly affected by variations in stimulus parameter.
CONCLUSIONS. Although no horizontal or vertical OKN asymmetries existed for volunteers grouped together, vertical OKN was characterized by idiosyncratic asymmetries that remained consistent for an individual. Look and stare OKN gain is strongly associated for downward moving stimuli.
Horizontal stare OKN has been widely investigated, and it is generally accepted that there is no asymmetry in healthy adults with good binocularity (Proudlock FA, et al. IOVS 2001;42:ARVO Abstract 300).2 4 5 6 7 8 There is, however, controversy regarding the symmetry of vertical stare OKN. Various authors (Proudlock FA, et al. IOVS 2001;42:ARVO Abstract 300)5 7 9 10 11 12 13 14 15 16 have found vertical asymmetry with increased gain for upward-moving stimuli. Ogino et al.,9 Wei et al.,13 14 Clément,15 LeLeiver et al.,10 and Garbutt et al.11 all found an upward asymmetry with targets of low stimulus speeds, whereas Takahashi et al.7 could only demonstrate asymmetry at higher target velocities. Hainline et al.2 compared the vertical OKN asymmetries of infants and adults, finding an upward preference in infants. No asymmetry was seen in adults. These findings were supported by Baloh et al.17 and Collins et al.,18 who also found no asymmetry in adults. A downward preference was reported by Schor and Levi.19
Fewer studies have been performed of the asymmetries of look OKN than of stare OKN. For horizontal look OKN, Valmaggia et al.8 have recently described nasalward preference for volunteers with no measurable binocularity, for look as well as for stare OKN. This asymmetry was not present in controls. Clément et al.,12 using an EOG recording technique, investigated look OKN at velocities of 27°/s, 39°/s, and 51°/s and found upward preferences at 39°/s and 51°/s. In addition, the association between look and stare OKN has not been investigated, either in terms of individual gains in nasalward, temporalward, upward, and downward directions or in terms of horizontal and vertical asymmetries.
The aims of this study were to investigate horizontal and vertical asymmetries in look and stare OKN and the consistency of OKN asymmetries within patients by comparing responses during monocular viewing with right eye open and left eye open. The association between look and stare OKN in different directions of stimulus motion was also compared. In a second experiment, we investigated the effect of different stimulus parameters (velocity, contrast, type of grating, stimulus shape) on the horizontal and vertical asymmetries of stare OKN.
Our results indicated that look OKN is typically mixed with stare OKN, which occurs after the quick phase, before the observer is able to acquire a new detail to track in the moving visual field. We have implemented a new method of delineating between look and stare OKN based on the distribution of the duration of slow phases during look OKN.
| Methods |
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Experiment 1
Fifteen healthy volunteers (3 men, 12 women; age range, 24–45 years; mean [± SD] age, 32.4 ± 5.8 years) were recruited. Both eyes were examined. There was no known history of ophthalmologic, neurologic, or otologic abnormality. An orthoptic examination was performed on all volunteers to exclude amblyopia, binocular vision defects, or any underlying ocular motility problems such as microstrabismus. No manifest strabismus was detected on performing a cover test. Tables 1 and 2 summarize the results of visual assessment for each volunteer for experiments 1 and 2. All volunteers had a best-corrected visual acuity of 0.0 logMAR (20/20) or better in each eye, with a difference of no more than 1 logMAR line between the two eyes. All volunteers achieved binocular vision of 60 seconds of arc or better using the TNO test for stereoscopic vision (Richmond Products, Albuquerque, NM). Contact lenses were used to obtain best correction when necessary to assist eye movement recordings (n = 5). The study received local ethical approval and was conducted in accordance with the tenets of the Declaration of Helsinki with the consent of volunteers after an explanation of its nature and possible consequences.
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-corrected using a photometer (OptiCAL; Cambridge Research Systems). Eye movements were recorded using a high-resolution pupil tracker at a sample rate of 250 Hz (EyeLink I; SensoMotoric Instruments GmbH, Berlin, Germany). The eye tracker has a resolution of 0.005° and a range of ±30° with a noise level of less than 0.01° RMS within this range (company specifications). Eye data were calibrated using a series of nine fixation points, projected individually in the shape of a 3 x 3 grid, ±20° wide and ±17.5° high. The calibration was repeated until the error between two measurements at any point was less than 1° or the average error for all points was less than 0.5°. A drift correction was also performed before each trial. Eye tracker recordings were converted offline to Spike2 neurophysiological software system files for subsequent analysis (Cambridge Electronic Design, Cambridge, UK).
All subjects viewed the OKN stimulus at 330 mm (resulting in a visual field of ±22.4° height and ±28.9° width) monocularly while their eye movements were recorded for a period of 20 seconds. A square black card (60 x 90 mm) was mounted on the front surface of the camera to occlude the nonviewing eye but still allow recordings of eye movements (data not analyzed). Head movements were minimized with the use of a chin rest, though the eye tracker (EyeLink; SR Research, Osgoode, ON, Canada) provided head movement–compensated gaze data. The stimuli consisted of a sinusoidally modulated contrast grating (spatial frequency, 0.1 cyc/deg; peak-to-peak contrast, 50%; luminance, 13.37–39.89 cd/m2) moving at a linear velocity of 40°/s. Stimulus contrast and velocity were selected to allow comparison with our previous findings.4 All luminance readings for experiments 1 and 2 were recorded with a radiometer (IL1700, R #106 radiance barrel, SEE038 detector; International Light, Newburyport, MA) with a photopic filter that matches the CIE V(
) photopic curve to within 1% total area error. The stimulus was applied moving in four directions—up, down, nasally, and temporally—with right eye viewing and left eye viewing. When measuring look OKN, the subject was instructed to actively fix and follow individual OKN target stripes, whereas when examining stare OKN, the subject was encouraged to look toward the center of the screen while keeping the stripes in focus. All stimuli were presented in a random fashion, and there was a gap of at least 15 seconds between each test stimulus.
Mean slow-phase velocity (MSPV) was calculated from the total distance traveled per total time taken during the slow phases. This method was used in preference to the mean of each slow-phase velocity to prevent measurement distortion by short, less consistent, slow phases. The gain was the ratio of MSPV/stimulus velocity.
Experiment 2
Nine healthy volunteers (1 man, 8 women; age range, 24–45 years; mean age, 32.1 ± 6.7 years) were recruited for the second experiment. Only the right eye of each subject was investigated (contact lenses worn by two volunteers). Following the methodology and recording techniques used in experiment 1, stare OKN responses in four directions were compared, with stimulus parameters varied, as follows: velocity, 20°/s and 40°/s; contrast, 50% and 100%, where luminance is from 13.37 to 39.89 cd/m2 for 50% contrast and from 0.10 to 53.16 cd · s/m2 for 100% contrast; and grating luminance modulation, sine wave and square-modulated contrast. All combinations of these three parameters were tested using a stimulus covering the extent of the CRT screen. In addition, the two stimulus velocities and contrasts were also tested using a circular vignetted stimulus (diameter, 22.4°; background luminance, 11.60 cd · s/m2) but using only the sine wave-modulated grating.
Statistical Analysis
Asymmetries were compared using the general linear model, with participants introduced as random factors using SPSS (Chicago, IL) software, version 11. Pearson correlation was used to estimate consistency of gains between look and stare OKN and with either eye open. Asymmetry indices were calculated using the following equations:
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For experiment 2, a linear mixed model was used with either OKN gain or asymmetry index as the dependent variable and including all the parameters as fixed factors to investigate the most potent effects on OKN asymmetries. Coefficients of variation (%) were calculated to estimate between-subject and within-subject variability.
| Results |
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None of the parameters had a significant effect on either horizontal asymmetry indices (F = 0.002, P = 0.96 for velocity; F = 2.00, P = 0.16 for contrast; F = 0.76, P = 0.38 for grating modulation; F = 0.02, P = 0.89 for field shape) or vertical asymmetry indices (F = 0.02, P = 0.87 for velocity; F = 0.41, P = 0.52 for contrast; F = 0.81, P = 0.37 for grating modulation; F = 0.14, P = 0.70 for field shape).
Given the large number of different stimulus parameters, we might predict high within-subject variation of OKN gain; however, within-subject and between-subject variations were similar in magnitude. Within-subject coefficients of variation were 22.1%, 22.1%, 21.9%, and 21.7% for upward, downward, nasal, and temporal directions, respectively. Between-subject variations were similar but slightly higher than within-subject variations for downward, nasal, and temporal OKN gains (coefficients of variation were 26.8%, 27.8%, and 29.8%, respectively) but lower for upward OKN gain (coefficient of variation was 16.9%). Similarly, between-subject variation for asymmetry indices was still relatively high at 70% to 80% of within-subject variation (vertical asymmetry index: within = 12.8%, between = 9.8%; horizontal asymmetry index: within = 12.3%, between = 8.5%).
Relatively high between-subject variation can be seen in Figure 7 , in which asymmetry indices for all combinations of stimuli are grouped for each volunteer (arranged in order of mean asymmetry index). The figure illustrates that vertical and horizontal asymmetries are often consistent in the same person even when using a variety of stimulus designs. For example, the volunteers on the left of the graph tended to show asymmetry indices above 0.5 (upward > downward and nasalward > temporalward) for most trials, whereas volunteers on the right of the graph tended to show asymmetry indices below 0.5 for most trials. This pattern was observed for both vertical and horizontal indices, though the correlation between individual vertical and horizontal indices (means of all values) was not significant (P = 0.06). Preponderance for horizontal or vertical asymmetry was not correlated to interindividual differences in visual acuity between pairs of eyes, eye dominance, or stereoscopic vision (Table 2) .
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| Discussion |
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When all subjects were grouped together, we found no evidence of a consistent horizontal or vertical OKN asymmetry in healthy adults for either look or stare OKN with any combination of velocity, contrast, luminance modulation of grating, or field shape. Although an absence of horizontal OKN asymmetry was expected, the absence of vertical asymmetry was surprising because most of the published literature suggests an upward asymmetry in adults with normal vision (Proudlock FA, et al. IOVS 2001;42:ARVO Abstract 300).5 7 9 10 11 12 13 14 15 16 With the use of EOG, Tashahaki et al.7 found an upward asymmetry in adults with target stimuli of 70°/s and greater, whereas LeLiever et al.10 found an upward preference for target velocities below 70°/s. More sensitive magnetic search coil techniques used by van den Berg et al.5 found an upward asymmetry with target velocities ranging from 9°/s to 57°/s. Ogino et al.9 found an upward asymmetry for target velocities ranging from 30°/s to 90°/s, with a maximum response at velocities of 30°/s to 40°/s. Wei et al.13 14 also found a consistent vertical asymmetry at 40°/s. In recent studies using videooculography, Garbutt et al.11 found an upward preference for stimuli velocities of 10°/s to 50°/s, and Proudlock et al. (IOVS 2001;42:ARVO Abstract 300) found the same for velocities of 10°/s, 20°/s, and 40°/s. The relative contribution of the peripheral and central retina on vertical OKN has been investigated by Murasugi et al.,16 who found an upward preference with target velocities ranging from 10°/s to70°/s for large field targets (61° x 64°). This asymmetry tended to be exaggerated by biasing stimulation of the peripheral retina and diminished by biasing stimulation of the central retina. Clémant et al.12 are the only investigators of look OKN vertical asymmetry, and they found an upward preference at 39°/s and 51°/s.
A few authors have reported asymmetries with preference to stimuli moving in a downward direction,17 20 21 though these studies only used small sample sizes. Several older studies were unable to identify any vertical OKN asymmetry.2 18 22 Collins et al.18 and Calhoun et al.22 did not find asymmetry in normal adult volunteers using EOG recording techniques. However, Hainline et al.,2 using infrared recording techniques and a test velocity of 7°/s, found upward OKN asymmetry in healthy infants (younger than 114 days of age) but not in adults. The incongruity in results from previous studies may be attributed, in part, to the use of different recording techniques. In particular, some authors report that EOG results are susceptible to artifact from eyelid movement. Some of the ambiguity in previous data could be addressed by a meta-analysis of the amassed vertical OKN literature.
Studies using full-field or near full-field stimulation tended to find a clearer preference for upward stimulation,5 7 9 10 12 13 probably because of greater stimulation of the peripheral retina, which Murasugi et al.16 have shown results in exaggerated upward bias of vertical OKN. The field size used in the present study was 57.8° x 44.8°. Use of larger visual field sizes with the current set-up is limited by physical restrictions imposed by the arrangement of the cameras on the eye tracker. Although a large amount of peripheral retina is stimulated with a visual field of this size, using a larger visual field size might have resulted in an upward vertical bias.
The novel finding in this study was the propensity individuals showed for a certain direction and degree of vertical asymmetry rather than the vertical asymmetry of the group as a whole. This is most clearly seen from the strong correlation in vertical asymmetry index for volunteers viewing with either right or left eye. Because vertical eye movements are conjugate, the comparison of left eye viewing and right eye viewing allowed comparison of intrasubject and intersubject variability. This has not been investigated in earlier studies. The cause of the idiosyncratic nature of vertical OKN is unclear.
The consistency of vertical asymmetry indices was also observed between look and stare OKN responses. This was evident even though look OKN is more vertically symmetrical than stare OKN. The greater symmetry of look OKN may be attributed to the larger gains observed for look OKN, which might have resulted because of the link—well developed in humans—between look OKN and smooth pursuit. Interestingly, look and stare OKN are more strongly associated when they follow stimuli moving downward rather than stimuli moving upward or even nasalward or temporalward. OKN responses in humans are usually generated from global motion (called optic flow) caused by locomotion through space (walking and running in humans). During natural locomotion, downward motion is often the strongest stimulus because of the proximity of the ground.23
Although there is a general consensus that horizontal stare OKN is symmetrical in healthy persons (Proudlock FA, et al. IOVS 2001;42:ARVO Abstract 300),2 4 5 6 7 8 some display a propensity for preference toward temporalward or nasalward moving stimuli, which can be consistent despite varying stimulus parameters (Fig. 7) . Horizontal stare OKN asymmetry did not appear to be consistent for left eye viewing and right eye viewing (Fig. 4 , bottom right graph), suggesting that idiosyncratic traits in horizontal asymmetries could be independent for either eye.
OKN responses to vertically moving stimuli appear to be more sensitive to changes in stimulus parameters than horizontally moving stimuli (stimulus velocity, shape of field, contrast and grating contrast profile, in decreasing order of effect). However, none of these parameters had a significant effect on vertical or horizontal asymmetry overall. Interestingly, vertical and horizontal asymmetries were relatively robust to influences of different stimulus parameters.
In summary, though we found no horizontal and vertical OKN asymmetries when volunteers were grouped together, vertical OKN was characterized by idiosyncratic asymmetries that remained consistent for an individual. In addition, we found that look and stare OKN gains were strongly associated for stimuli moving in the downward direction.
| Footnotes |
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Submitted for publication June 22, 2007; revised August 6, and September 11, 2007; accepted December 12, 2007.
Disclosure: C.M. Knapp, None; I. Gottlob, None; R.J. McLean, None; F.A. Proudlock, None
The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked "advertisement" in accordance with 18 U.S.C.
1734 solely to indicate this fact.
Corresponding author: Frank A. Proudlock, University of Leicester, Ophthalmology Group, Faculty of Medicine and Biological Sciences, Robert Kilpatrick Clinical Sciences Building, Leicester Royal Infirmary, PO Box 65, Leicester LE2 7LX, UK;fap1{at}le.ac.uk.
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C. M. Knapp, I. Gottlob, R. J. McLean, S. Rafelt, and F. A. Proudlock Effect of distance upon horizontal and vertical look and stare OKN J Vis, November 1, 2009; 9(12): 23 - 23. [Abstract] [Full Text] [PDF] |
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