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1From the University of Leicester, Ophthalmology Group, Faculty of Medicine and Biological Sciences, Leicester, United Kingdom; and the 2University Hospital of Leicester, NHS Trust, Leicester, United Kingdom.
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Abstract |
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METHODS. Monocular torsional eye movements were recorded from 30 subjects between 19 and 72 years of age. Constant-velocity rotary stimuli in clockwise and counterclockwise directions were used to elicit tOKN at 40°/s and 400°/s.
RESULTS. The number of subjects in whom tOKN could not be detected increased with age and was consistent in both directions of stimulation and at both angular velocities of stimulation.
CONCLUSIONS. tOKN appears to fail increasingly with age, in contrast to previous reports of horizontal and vertical OKN systems. This indicates that the ability to respond to rotary motion is more sensitive to the effects of aging.
In contrast, the horizontal OKN response has been widely investigated with age and has been shown to undergo a mild but significant deterioration.2 3 4 5 This has been attributed to age-related degeneration in cortical areas responsible for motion perception and in the retinogeniculate pathway,6 though degeneration of ocular motor areas cannot be ruled out. The effect of vertical OKN has also been investigated.7 Similarly, OKN responses in elderly subjects have been found to be inferior to those in younger subjects.
OKN in the horizontal and vertical directions can be influenced by components of the voluntary pursuit system. Therefore, it has been postulated that the effects of aging on the pursuit system could influence the OKN system.3 Published reports in this area generally agree that the pursuit system deteriorates with age.3 5 7 8 9 tOKN, however, is purely reflexive and is not influenced by a pursuit mechanism because little or no movement occurs at the fovea when a subject fixates the stimulus.10 It would be of additional interest, therefore, to see how the tOKN system compares with previously published results on horizontal and vertical OKN.
We examined the monocular tOKN response in a group of healthy subjects between 19 and 72 years of age by testing eye rotation in intorsion and extorsion directions in response to 40°/s and 400°/s stimulation.
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Subjects and Methods |
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Responses from the right eye were recorded unless visual acuity was less than 6/9 (20/30) or eye movement recording quality was lower than 0.5, in which case the left eye was used (n = 3; torsional eye movement recording quality is defined in Data Analysis). The study received local ethical approval and was performed with consent after explanation of the nature and possible consequences of the study. The study was performed in accordance with tenets of the Declaration of Helsinki.
Eye Movement Recording
Eye movements were measured in three dimensions using a video-oculography technique (VOG) at a sampling rate of 50 Hz (Strabs system; Sensomotoric GmbH, Teltow, Germany). The equipment consisted of infrared video cameras fitted to a face mask attached to the head with a rubber strap (Fig. 1) . Pupil tracking was used to derive horizontal and vertical movements. A segment of the iris was tracked to measure torsional eye movements. The system has a spatial resolution of 0.03°, 0.02°, and 0.1° and a linearity of ±3.8%, ±3.2%, and ±1.4% full-scale reading for horizontal, vertical, and torsional eye movements, respectively (company specifications). The range of linear measurement was ±25°, ±20°, and ±18° for horizontal, vertical, and torsional eye movements, respectively. Noise for the setup was estimated from the torsional recordings as 0.1° to 0.2°/s root mean square for torsional angle and 0.1° to 0.15°/s root mean square for torsional velocity. The digitized ASCII file output for horizontal vertical and torsional data was converted to software files (Spike 2; Cambridge Electronic Design, Cambridge, UK) for analysis.
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A five-point calibration of each eye was performed monocularly, with the nonviewing eye covered before the testing procedure began. Subjects fixated points centrally, 15° in depression, right gaze, in elevation, and left gaze. Recordings were taken monocularly, and a cover was used for the nonviewing eye during testing. Torsional measurements were calibrated within the VOG setup, determined from rotations of the iris. The torsional angle was defined with reference to the initial image measured when the experiment was set up.
The experimental stimulus was projected onto a 1.75 x 1.17-m rear projection screen using an LCD projector (resolution 1024 x 768 pixels; model EMP 703; Epson, Long Beach, CA). Stimuli were generated using a visual stimulus projector (VSG 2/5; Cambridge Research Systems, Rochester, UK) and consisted of a rotating sinusoidal grating pattern of 90° cycle size subtending 50.8° in diameter (Fig. 1) . The luminance of the grating pattern varied from 0.45 to 23.0 cd/m2, giving a luminance contrast of 96%. The stimulus revolved around its central axis at 40°/s and 400°/s in clockwise and counterclockwise directions. The subjects were asked to stare at the center of the stimulus keeping it in focus. Each stimulus was presented for 30 seconds, followed by a blank phase of 15 seconds during which the subject was asked to fixate a black screen.
Four of the subjects who showed no responses at 40°/s and 400°/s (all men; aged 56, 59, 63, and 72 years) were tested across a wider range of stimulus velocities—20°/s, 100°/s, 200°/s, 800°/s, and 1000°/s—in both directions.
Data Analysis
A section of the iris, the "signature segment," was selected from a reference video frame to include significant landmarks in the iris from which luminance levels were measured. Torsional eye position was derived from angular displacement of the defined segment. To estimate the angular displacement, the luminance levels from subsequent video frames were cross-correlated for the corresponding segment with the original signature segment. The cross-correlation value also provided a measure of correspondence between the signature segment and the subsequent image that was used as an estimate of the quality of the recording. Only data that exceeded a torsional quality of 0.5 were used for analysis (a correlation close to 1 implied the best data quality). Poor-quality data could result from an iris segment without many landmarks and changing pupil size because of altered illumination, leading to changes in the position of landmarks. They could also result when the pupil was not accurately detected because of small size or interference from surrounding ocular structures (e.g., dark eyelashes, lashes with heavy eye makeup, droopy eye lids). Subjects were instructed to "open their eyes wide" when it was considered from online displays of the eyes that it was possible the eyelids were occluding the recording. A drop in torsional quality of the data in the blank phase, caused by changing pupil size, meant that measurement of torsional optokinetic afternystagmus was unreliable. Torsional quality of the data during measurement of tOKN did not significantly change with age in the study (linear regression: r2 = 0.02, P = 0.2).
Smoothed velocity traces of the torsional data were created using a simple five-point low-pass differentiator filter (linear). A velocity threshold of 10°/s was used as a default to determine saccades in the torsional recording. Because the level of noise varied, depending on the quality of the torsional recording, the velocity threshold could be adjusted manually (invariably reduced) to just exceed the noise level evident in the smoothed velocity trace. The mean velocity threshold selected across all subjects was 6.98°/s (SD 1.79°/s). This equates to discrimination of saccades of 0.55° or larger (determined from peak velocity/amplitude characteristics for the setup). For a mean beat frequency of 1.46 Hz (the mean of the subjects showing tOKN in this study), this approximated to a slow-phase velocity of 0.80°/s.
For subjects classified as responders, the mean velocity over a minimum of 10 slow phases from each 30-second trace was used to give the mean slow-phase velocity (MSPV) for each stimulus. Because MSPVs were not normally distributed across the subjects, median values were used for analysis. Subjects classified as nonresponders had no slow phases within the 30-second analysis section. One subject was excluded from the original study group of 31 subjects because the quality trace of the torsional segment fluctuated during testing; hence, a constant noise-free recording was difficult to achieve.
As monocular eye movements were recorded, the relative direction of rotation of the eye differed according to which eye was fixing (e.g., clockwise stimulation to the right eye produced a slow phase that extorted the right eye and intorted the left eye and vice versa). To avoid misinterpretation, the direction of the eye rotation and the velocity of the stimulus were defined in relation to intorsion/extorsion of the viewing monocular eye.
Statistical Analysis
Changes in the proportion of nonfunctional tOKN with age were analyzed using logistic regression. The odds ratio in this analysis was used to estimate the risk of being a nonresponder with age. The correlation between MSPV and age in subjects with measurable responses was also analyzed using the simple linear regression (Pearson product-moment correlation coefficient).
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Results |
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Of the four older subjects (aged 56, 59, 63, and 72 years) tested at further stimulus velocities of 20°/s, 100°/s, 200°/s, 800°/s, and 1000°/s, the subjects aged 63 and 72 years demonstrated no detectable response when eye movement traces were analyzed across all stimulus velocities. The 56-year-old subject responded only at the stimulus velocity of 20°/s, in the counterclockwise direction, with an MSPV of 0.88°/s, and the 59-year-old subject responded at stimulus velocities of 200°/s in the clockwise direction and 20°/s in the counterclockwise direction, with MSPVs of 1.04°/s and 0.7°/s, respectively.
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Discussion |
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In a prospective cross-sectional study (249 subjects; age range, 18 days-89 years), horizontal OKN mean gain has been shown to undergo a small but significant decline after age 50.2 This is in agreement with other studies comparing younger subjects with older subjects; superior horizontal OKN gains were always observed in the younger subjects.3 4 5 Similarly, vertical OKN was also reduced in healthy elderly subjects (mean age, 70 ± 8 years), who had lower tracking gain and greater phase lag than healthy young subjects (mean age, 30 ± 6 years).7
The contrasting feature between our results and previous studies on horizontal and vertical OKN, however, is that the tOKN response was virtually undetectable in elderly subjects (older than 65 years; median age, 68), with only 1 in 10 demonstrating a response. The lack of response in the older subjects was also consistent when other stimulus velocities were used to assess the tOKN response in four subjects who originally did not respond to stimuli rotating at 40°/s or 400°/s. The older subjects, aged 63 and 72 years, did not show any response to other stimulus velocities, whereas the two younger subjects, aged 56 and 59, showed minimal response to stimuli rotating at 20°/s and 200°/s. Although previous studies showed reduced horizontal and vertical OKN gain in the elderly, a response was still evident.
Possible explanations for this could be that tOKN response has a very small gain (eye velocity in relation to stimulus velocity), with stimuli up to 200°/s yielding a maximum response of approximately 3°/s.1 Stimulus velocities of 40°/s and 400°/s were considered suitable for use because these had previously elicited a good response that was easily differentiated from the normally occurring noise in the recording.1 However, it is possible that tOKN responses are closer to threshold than horizontal and vertical OKN responses, making them more sensitive to aging. Another possibility is that tOKN responses are present in the elderly but fall below the level of system noise. In general, VOG yields larger signal-to-noise ratios than torsion for horizontal and vertical eye movement recordings.
The tOKN response is essentially involuntary and not influenced by voluntary pursuit mechanisms. In general, we have limited capacity to make voluntary torsional eye movements in the primary position, though one early previous report by Balliet and Nakayama11 in 1974 suggests that, with training, torsional pursuit can be generated voluntarily. The torsional "pursuit" they describe, however, does not involve the classic pursuit mechanism of tracking a single object of interest. Rather, it is driven by the alignment of static stimuli spanning the visual field. It is possible that tOKN is more prone to deterioration with age than horizontal and vertical OKN because pursuit cannot contribute to its generation.
Although the pursuit mechanism has been shown to decrease with age along the horizontal and vertical meridians,3 7 12 recent findings from a longitudinal study in healthy elderly persons (older than 75 years)13 describes horizontal smooth pursuit gains at two different velocities as not greatly affected by aging. In comparison, horizontal OKN measures showed a gradual significant age-related decline over a 9-year follow-up period. It is possible that the rates of horizontal and vertical OKN decline could be slowed by contribution of the pursuit system; tOKN shows a sharper decline.
The importance of higher cortical pathways compared with subcortical (retinogeniculate) pathways used for motion detection have been investigated.6 Subjective measures of motion perception and objective measures of horizontal motion detection when viewing a random dot display were investigated in subjects from 19 to 92 years of age. Interestingly, the authors found an age-related linear decrease in objective OKN responses and a subjective increase in the motion perception thresholds; however, they did not find an association between the two factors, suggesting that aging affects the neural mechanisms behind motion perception and motion detection at different cortical and subcortical levels.
The effects of aging on torsional eye movements generated through vestibular stimulation have also been described. Jahn et al.14 measured torsional eye movements with VOG during stimulation of the vestibular nerve through galvanic vestibular stimulation (GVS) in 57 healthy subjects aged 20 to 69 years. They found that the magnitude of induced static ocular torsion and torsional nystagmus increased from the fourth to the sixth decade but decreased in the seventh decade. Listing’s plane, the axis of rotation that governs the torsional position of the eye at all gaze positions,15 has also been examined with respect to age. It was found that torsional position was more variable in older subjects (i.e., Listing plane was thicker) than in younger subjects when the whole body was repositioned to different static roll-and-pitch positions.16
In conclusion, we have shown for the first time an age-related deterioration of the tOKN responses in healthy subjects between 19 and 72 years of age. The responses appeared to be virtually eliminated in subjects older than 65 years of age.
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Footnotes |
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Submitted for publication July 17, 2007; revised September 10 and October 8, 2007; accepted December 12, 2007.
Disclosure: S.J. Farooq, None; I. Gottlob, None; S. Benskin, 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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