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Spatial-bisection acuity in infantile nystagmus
Vision Research 64 (2012) 1–6
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Spatial-bisection acuity in infantile nystagmus Michael T. Ukwade a, Harold E. Bedell a,b,⇑ a b
College of Optometry, University of Houston, Houston, TX 77204-6052, USA Center for Neuro-Engineering and Cognitive Science, University of Houston, Houston, TX 77204-4005, USA
a r t i c l e
i n f o
Article history: Received 9 December 2011 Received in revised form 27 April 2012 Available online 14 May 2012 Keywords: Infantile nystagmus Spatial bisection Hyperacuity Image motion Motion smear Meridional anisotropy
a b s t r a c t This study measured spatial bisection acuity for horizontally and vertically separated line targets in five observers with infantile nystagmus syndrome (INS) and no obvious associated sensory abnormalities, and in two normal observers during comparable horizontal retinal image motion. For small spatial separations between the line targets, bisection acuity for both horizontally and vertically separated lines is worse in the observers with IN than normal observers. In four of the five observers with IN, bisection acuity for small target separations is poorer for horizontally compared to vertically separated lines. Because the motion smear generated by the retinal image motion during IN would be expected to influence horizontally separated targets, the degradation of bisection acuity for both vertical and horizontally separated lines indicates that a sensory neural deficit contributes to impaired visual functioning in observers with idiopathic IN. Ó 2012 Elsevier Ltd. All rights reserved.
1. Introduction Infantile nystagmus syndrome (INS) is a condition characterized by incessant rhythmic eye movements, predominantly in the horizontal plane. The eye movements in INS typically are interrupted by brief periods referred to as foveation periods, during which the eye velocity is only a few deg/s or less, and the target of regard is imaged on or near the fovea (Dell’Osso & Daroff, 1975; Dell’Osso et al., 1992). Some individuals with INS, for example, those with albinism or rod monochromacy, have demonstrable abnormalities of the afferent visual system (Abadi & Bjerre, 2002; Cogan, 1967). Persons with so-called idiopathic infantile nystagmus (IN) exhibit no detectable abnormalities in the eye or the afferent visual pathways. Nevertheless, persons with idiopathic IN typically have visual acuity within the range of 20/20 to 20/100 (Abadi & Bjerre, 2002; Hanson et al., 2006) and elevated thresholds on several other visual spatial tasks (Abadi & Sandikcioglu, 1975; Bedell, 2006; Bedell & Loshin, 1991; Bedell & Ukwade, 1997; Goddé-Jolly & Larmande, 1973; Guo et al., 1989; Liu & Yang, 1997; Ukwade & Bedell, 1999; Ukwade, Bedell, & White, 2002). The eye movements of persons with nystagmus are accompanied by motion of the retinal image, which is known to degrade visual acuity in persons with normal vision (Brown, 1972; Chung & Bedell, 2003; Demer & Amjadi, 1993; Westheimer & McKee, 1975). In persons with IN, visual acuity typically varies with the parameters of eye movement, most notably the duration of the ⇑ Corresponding author at: College of Optometry, University of Houston, Houston, TX 77204-6052, USA. Fax: +1 713 743 2053. E-mail address: [email protected] (H.E. Bedell). 0042-6989/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.visres.2012.05.004
foveation periods (Abadi & Worfolk, 1989; Bedell, 2000; Cesarelli et al., 2000; Dell’Osso & Daroff, 1975; Sheth et al., 1995; Simmers, Gray, & Winn, 1999). A correlation exists also between visual acuity and the position variability of the foveation periods, that is, the standard deviation of the eye position during foveation periods during several seconds of continuous viewing (Bedell, White, & Abplanalp, 1989; Cesarelli et al., 2000). Acuity has been proposed to depend on the variability of the eye velocity during foveation periods as well (Dell’Osso & Jacobs, 2002; Dell’Osso et al., 1992; Sheth et al., 1995). Similar relationships exist between the duration and the variability of the foveation periods and acuity for other spatial tasks (Bedell & Ukwade, 1997; Dickinson & Abadi, 1985; Ukwade & Bedell, 1999). Because of the relatively slow temporal response of the visual system (e.g., Cogan, 1992; Efron, 1970), rapid motion of the retinal image produces motion smear, which in turn impacts negatively on aspects of spatial visual performance (Chung & Bedell, 1998; Morgan & Benton, 1989; Ramamurthy, Bedell, & Patel, 2005). For example, Morgan and Benton found that normal observers’ spatial-interval acuity is degraded by constant-velocity retinal image motion that is parallel to the direction of the target separation. The velocity of motion at which spatial-interval acuity becomes impaired is proportional to the separation between the targets, which is consistent with the expected effect of motion blur. More recently, Chung, LaFrance, and Bedell (2011) simulated the retinal image motion of observers with IN in normal observers and showed that the intervals of retinal image motion between the simulated foveation periods contribute to a degradation of visual acuity. Nevertheless, it remains unclear whether the image motion that accompanies the slow-phase eye movements of observers
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M.T. Ukwade, H.E. Bedell / Vision Research 64 (2012) 1–6
with IN results in a similar reduction of visual acuity, as observers with IN report a much smaller extent of perceived motion smear than normal observers during comparable retinal motion (Bedell & Bollenbacher, 1996; Bedell & Tong, 2009). The issue that we address here is whether the impaired spatial vision in persons with idiopathic IN is attributable solely to the presence of retinal image motion, or whether a sensory deficit contributes also to the reduction of visual performance in these individuals. Two approaches can be used to evaluate this issue. The first is to eliminate the retinal image motion in persons with nystagmus, for example, by presenting a visual target for such a brief duration that no appreciable retinal image motion can occur. Abadi and King-Smith (1979) found that contrast sensitivity for a vertical line flashed for only a fraction of a ms, a duration too brief to produce any appreciable motion smear, is reduced in patients with IN compared to normal observers. The measured reduction of contrast sensitivity therefore can be attributed to a sensory deficit. A second way to evaluate whether a sensory deficit exists in observers with idiopathic IN is to assess the visual performance of normal observers in the presence of target motion that simulates the retinal image motion in observers with IN (Bedell, 2006; Bedell & Ukwade, 1997; Chung & Bedell, 1995, 1996, 1997; Currie, Bedell, & Song, 1993; Dickinson & Abadi, 1985; Ukwade & Bedell, 1999). This strategy reveals the magnitude of visual impairment that is attributable specifically to the retinal image motion in observers with IN. Any additional impairment that exists in persons with idiopathic IN can be ascribed to the presence of a sensory abnormality. In the current study, we measured spatial-bisection acuity in persons with IN and in normal observers under comparable conditions of horizontal retinal image motion. Under optimal conditions, spatial bisection acuity is highly precise in normal observers (Andrews & Miller, 1978; Bedell, Johnson, & Barbeito, 1985; Klein & Levi, 1985; Stevens & Ducasse, 1912). A comparison between the bisection acuity of persons with IN and normal observers for targets that are separated in the direction of retinal image motion specifies the magnitude of the acuity loss in IN that is not attributable directly to the motion of the retinal image. In addition, because retinal image motion orthogonal to the direction of target separation should produce little or no degradation from motion smear, bisection acuity for vertically separated targets should approximate that in the absence of retinal image motion. Any impairment of bisection acuity in the observers with IN in this viewing condition therefore is not readily attributable to image motion. The results of both of the above comparisons indicate that a sensory abnormality contributes to the degradation of spatial vision in persons with idiopathic IN.
2. Methods 2.1. Observers Two young adult normal observers and five persons with idiopathic IN participated in this study, consequent upon their written informed consent. A third young normal observer provided confirmatory data for a subset of the experimental conditions. The normal observers demonstrated good ocular motility and achieved at least 20/20 visual acuity with appropriate optical correction. None of the observers with IN had any co-existing ocular or visual conditions. The clinical characteristics of the observers with IN are summarized in Table 1. As shown in the Table, the predominant waveforms of the IN observers include pendular and jerk waveforms, among others (Dell’Osso & Daroff, 1975). Tabulated values for the average amplitude and frequency of nystagmus and for the average duration of the foveation periods were determined from 10 to 20 s epochs of horizontal eye position that were recorded by infrared
limbal tracking while the observer viewed a small fixation target at 3.75 m in the straight-ahead direction. As will be discussed in Section 4 below, the observers’ nystagmus included small vertical and torsional components as well. The foveation periods were identified as intervals in the horizontal waveform when the eye velocity was slower than approximately 4 deg/s and the eye position was within a spatial window of ± 2 deg. The eye-movement parameters listed in Table 1 should be viewed as approximations, as the characteristics of IN may vary according to the visual task and the motivational state of the observer (Abadi & Dickinson, 1986; Cham, Anderson, & Abel, 2008; Dell’Osso & Daroff, 1975; Tkalcevic & Abel, 2005; Wiggins et al., 2007). However, all of the observers with IN as well as all of the normal observers had participated previously in psychophysical studies. Except for one of the normal observers, the observers were naive to the details of the experiment. 2.2. Stimuli and instrumentation The stimulus consisted of three bright (luminance = 100 cd/m2) horizontal or vertical lines, presented on a Hewlett Packard 1311B oscilloscope at a refresh rate of 240 Hz. Each line was 30 min arc long and, nominally, 0.2 min arc wide. The rest of the oscilloscope face was dark and the viewing duration was unlimited. The distance between the two outer, flanking lines of the three-line bisection stimulus ranged from 10 to 320 min arc, such that the mean separation between the central line and each of the 2 flanking lines varied between 5 and 160 min arc. On each trial, the central line was presented at one of 7 locations with respect to the midpoint between the two flanking lines. Using a joystick, the observer indicated whether the central line was either to the left or right, or above or below, of the midpoint position. Observers viewed the line stimuli through a mirror haploscope, which has been described in detail elsewhere (Ukwade & Bedell, 1999). Each channel of the haploscope contains one fixed and one moveable mirror. The moveable mirrors were mounted on matched G325D galvanometers and controlled by a pair of CCX650 Scanner controllers, both obtained from General Scanning, Inc. The controllers received input voltages that determined the mirror positions from a D/A card in a PC-compatible system. Horizontal retinal image motion of the bisection target was produced in the normal observers by oscillating the moveable mirrors around their vertical axes. Repetitive ramp motion of the haploscope mirrors approximated the image motion produced by a jerk IN waveform with an amplitude of 8° and a temporal frequency of 4 Hz. Because normal observers are unable to track this amplitude and frequency of motion (Wheeless, Cohen, & Boynton, 1967; Winterson & Steinman, 1978), we assume that the resulting retinal image motion closely approximated the motion produced by the oscillating mirrors. Previously, we found that the amplitude, frequency and type of the simulated IN waveform has relatively little impact on normal observers’ visual performance. Rather, visual acuity and contrast sensitivity depend primarily on the characteristics of the foveation periods, both when nystagmus image motion is simulated in normal observers and when measurements are made in observers with IN (Bedell, 2006; Chung & Bedell, 1995; Currie, Bedell, & Song, 1993; Dell’Osso & Jacobs, 2002; Dickinson & Abadi, 1985; Sheth et al., 1995). Accordingly, the simulated jerk IN waveform in the current study included a simulated foveation period which, during each block of 70 trials, had a duration of 20, 40, 80 or 120 ms. Position variability was not included in the simulated IN waveforms, as Badcock and Wong (1990) showed that small amounts of position jitter have little influence on spatial-interval acuity in normal observers. Fig. 1 shows samples of the simulated IN waveforms with 20 and 120 ms foveation durations.
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M.T. Ukwade, H.E. Bedell / Vision Research 64 (2012) 1–6 Table 1 Visual characteristics of subjects with infantile nystagmus.
3.0
120
19.0
26.2
Pendular with fov saccades
4.7
2.8
60
44.5
15.2
0.159
Jerk left
7.7
5.0
64
44.5
30.9
20/100
0.803
Pendular
10.8
3.0
36
241.1
100.7
20/50
0.336
Bi-dir jerk
4.6
1.8
71
54.6
13.8
Snellen acuity
JH
RE: plano LE: plano RE: +0.25 0.50 080 LE: +0.25 sphere RE: 3.00 1.75 005 LE: 3.00 1.00 003 RE: +5.25 4.00 180 LE: +4.00 3.50 168 RE: +2.00 1.75 155 LE: +2.25 1.50 177
27
20/20
0.195
Jerk left
16
20/25
0.114
24
20/30
17 27
FR MiS a
3.0
Age (yrs)
AJ
Optimal vertical bisection (arc sec)
Average foveation duration (ms)
Refractive error
CN
Optimal horizontal bisection (arc sec)
Average IN frequency (Hz)
Subject
Psychometric acuitya(LogMAR)
Predominant IN waveform
Average IN amplitude (deg)
Psychometric acuity was assessed using Landolt ring charts with controlled contour interaction (Flom, 1966).
2.3. Experimental procedures Because visual hyperacuities improve with practice (e.g., Fahle, Edelman, & Poggio, 1995; McKee & Westheimer, 1978), each observer received practice sessions using the bisection stimuli prior to the start of the experiment. Data collection commenced for each observer when additional practice produced no further improvement in bisection acuity. Spatial-bisection acuities were determined by probit analysis and correspond to a change from 50% to 84% on the psychometric function, generated using the method of constant stimuli. The psychometric functions plotted the percentage of ‘‘central-line-right-of-midpoint,’’ or ‘‘central-lineabove-the-midpoint,’’ responses against the position of the central line. The bisection acuities that are presented below for each observer, target orientation, and line separation represent the average of at least two replications per condition. 3. Results 3.1. Normal observers during simulated IN motion During image motion simulating an 8 deg, 4 Hz horizontal jerk nystagmus, normal observers’ bisection acuity for horizontally separated lines is best for an inter-line separation of 5 or 10 arc min (dashed lines in Fig. 2). For these small separations, bisection acuity improves systematically with the duration of the simulated foveation periods, from approximately 20 arc sec when the simulated foveation duration is 20 ms to approximately 10 arc sec when the simulated foveation duration is 120 ms (r = 0.93, p = 0.0008). When the horizontal inter-line separation exceeds 10 arc min, bisection acuity worsens approximately in proportion to the separation between the lines. The bisection acuity during horizontal image motion is slightly better for vertically than for horizontally separated lines (paired tdf=4 = 4.61, p = 0.010). For example, for lines that are separated vertically by 5 arc min, bisection acuity has an average value of 5.0 arc sec when the simulated foveation duration is 120 ms, compared to 9.1 arc sec when the lines are separated horizontally. For inter-line separations larger than 5 arc min, the advantage of vertically compared to horizontally separated lines for bisection acuity is smaller. In the absence of imposed image motion, the normal observers’ bisection acuity was essentially identical for horizontally and vertically separated targets (data not shown). 3.2. Observers with infantile nystagmus For the observers with horizontal idiopathic IN, spatial-bisection acuity for widely spaced (physically stationary) lines also worsens
approximately in proportion to the separation between the lines (Fig. 2). When the separation between the lines is reduced, the spatial-bisection acuity of the observers with IN either levels off, similar to the normal observers, or worsens. Except for observer JH, bisection acuity is poorer for horizontally than for vertically separated lines in the observers with IN, especially when the separation between the lines is small. The plots of spatial bisection acuity shown for the observers with IN in Fig. 2 are color coded to match the plots of the normal observers, when determined for a similar simulated foveation duration (see Table 1). For comparable conditions of retinal image motion, it is clear from the figure that the bisection acuity of the observers with IN typically is worse than that of the normal observers, for both vertically and horizontally separated line targets. The degradation of bisection acuity in the observers with IN compared to normal is most noticeable and consistent when the inter-line separation is small. The optimal values of horizontal bisection acuity for the observers with IN are related to their psychometrically measured visual acuities (rdf=3 = 0.978, p = 0.001; Table 1).
4. Discussion For vertically separated lines that are separated by 5 arc min, the average bisection acuity of the two normal observers is 5 arc sec, corresponding to 1/60th of the inter-line separation. For inter-line separations greater than approximately 5–10 arc min, the normal observers’ bisection acuity worsens approximately in proportion to the separation between the lines. Both of these results are consistent with data published previously by other investigators (e.g. Andrews & Miller, 1978; Bedell, Johnson, & Barbeito, 1985; Klein & Levi, 1985; Stevens & Ducasse, 1912). No horizontal–vertical anisotropy in bisection acuity existed when the normal observers were tested without imposed target motion. However, during horizontal motion that approximates the retinal image motion of observers with IN, normal observers’ bisection acuity is roughly 0.2 log units poorer for horizontally compared to vertically separated lines. Recently, Chung, LaFrance, and Bedell (2011) reported that the introduction of image motion to simulate that during IN slow phases degrades the visual acuity of normal observers by a similar amount. Earlier, Morgan and Benton (1989) showed that image motion parallel to the direction of target separation impairs spatial-interval acuity, a task that is closely related to bisection acuity. Like these previous authors, we attribute the degradation of acuity during horizontal target motion to the presence of motion smear. Specifically, we assume that spatial-bisection acuity, like other spatial-vision functions, is influenced by the physical motion of the retinal image, rather than
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Fig. 1. The horizontal angular position of the spatial bisection target is depicted as a function of time, when presented to normal observers during simulated jerk IN. The top and bottom panels show simulated IN waveforms with 20- and 120-ms foveation durations, respectively.
by the observer’s perception of motion. The reason for this distinction is that observers with INS typically do not report the perception of oscillopsia, despite the more-or-less incessant retinal image motion that accompanies their rhythmic eye movements, (e.g., Abadi, Whittle, & Workfolk, 1999; Kommerell, Horn, & Bach, 1986; Leigh et al., 1988; Tkalcevic & Abel, 2005). This assumption that spatial vision depends on retinal rather than perceived motion seems reasonable because it is difficult to appreciate how visual information can be recovered, once it is excluded from the spatio-temporal window of visibility (Watson, Ahumada, & Farrell, 1986) as the result of retinal image motion. Despite similar motion of the retinal image, the bisection acuity of observers with IN is worse than normal observers for horizontally-separated lines, especially when the inter-line separation is small. Consequently, bisection acuity is better for vertically compared to horizontally separated lines in four of the five observers with IN, especially for small inter-line separations. This outcome is consistent with the meridional anisotropy that is reported for other visual functions in observers with IN, including line detection (Abadi & King-Smith, 1979); grating contrast sensitivity (Abadi & Sandikcioglu, 1975; Bedell, 2006; Bedell & Loshin, 1991) Vernier acuity (Bedell & Ukwade, 1997), stereoacuity (Ukwade & Bedell, 1999) and motion detection (Bedell, 1992; Bedell, Sridhar, & Queener, in press; Shallo-Hoffmann et al., 1998). As horizontal image motion does not produce an anisotropy of normal observers’ acuity for horizontally vs. vertically oriented Vernier targets (Bedell & Ukwade, 1997), it is not clear that the meridional anisotropy of bisection acuity exhibited by the majority of the observers with IN can be attributed wholly to the retinal image motion that accompanies their nystagmus eye movements. Even so, all five of the observers with IN demonstrated poorer bisection acuity, compared to the normal observers, for vertically separated targets with small inter-line separations (Fig. 2, bottom). Previously, we measured the torsional and vertical components of nystagmus for 4 of the five observers in this study (JH, CN, AJ, FR)
Fig. 2. Spatial bisection acuity, in arc sec, is plotted against the average angular separation between the central line and the two outside flanking lines of the bisection target. Data for horizontally and vertically separated bisection targets are shown in the upper and lower panels, respectively. The inset in the upper panel illustrates the spatial layout of a horizontally separated bisection target. In each panel, the dashed lines without symbols are the average data for two normal observers during horizontal image motion to simulate a jerk IN waveform with one of four different foveation periods, i.e., violet: 20 ms; blue: 40 ms; green: 80 ms; red: 120 ms. The circles connected by solid lines are the bisection acuities for five different observers with IN. The color coding reflects each observer’s average foveation duration, i.e., observer FR (36 ms): blue; observer CN (60 ms): turquoise; observer AJ (64 ms): teal; observer MiS (71 ms): green; observer JH (120 ms): red. Error bars were omitted from the plots to prevent clutter. The average SEs for the two normal observers and for each of the observers with IN are 0.1 log units, for both horizontally and vertically separated bisection targets.
using the search-coil technique (Bedell et al., 2008). For these four observers, the amplitude of the torsional component of nystagmus ranged from 1.1 to 3.7 deg. For targets imaged on or near the fovea, the slight resulting rotations of the line targets would generate minimal motion smear and would be expected to exert little or no effect on either vertical or horizontal bisection acuity. In the same observers, the vertical component of nystagmus ranged in amplitude from 0.1 deg in observers JH and CN, which is comparable to the amplitude of normal observers’ eye movements during fixation, to between 0.6 and 0.7 deg in observers AJ and FR. If the duration of visual persistence is assumed to be approximately 125 ms (e.g., Efron & Lee, 1971), a vertical component of nystagmus with an amplitude of 0.65 deg and a frequency of 4 Hz would be expected to generate approximately 20 min arc of vertical motion smear, which potentially could interfere with bisection acuity for a range of small vertical inter-line separations. In agreement with this possibility, observer AJ exhibits poor bisection acuity for a vertical inter-line separation of 5 min arc and observer FR has the worst measured bisection acuities for vertical inter-line separations of 10 and 20 min arc. On the other hand, observers AJ and JH have essentially identical bisection acuities for vertical inter-line separations between 10 and 80 min arc, even though
M.T. Ukwade, H.E. Bedell / Vision Research 64 (2012) 1–6
the vertical component of observer JH’s nystagmus is only approximately 0.1 deg. Moreover, bisection acuity for a vertical inter-line separation of 80 min arc is approximately two times worse than normal for all of the observers with nystagmus except MiS. These considerations indicate that the degradation of bisection acuity for vertically separated targets cannot be attributed completely to the presence of vertical retinal image motion in the observers with IN. Taken together, the results obtained for horizontally and vertically separated lines imply that a neural sensory abnormality contributes to the impairment of bisection acuity in observers with idiopathic IN. We conclude that the presence of incessant retinal image motion during visual development is likely to produce neuronal changes that underlie, at least in part, this impairment of visual performance. A comparable conclusion was reached also by previous authors, who either measured visual functions in observers with IN in the absence of retinal image motion (Abadi & King-Smith, 1979; Shallo-Hoffmann et al., 1998), or compared the visual functions of persons with IN and normal observers during comparable motion of the retinal image (e.g., Bedell, 2000, 2006). Acknowledgment This research was supported in part by Research Grant, R01 EY05068, and Core Center Grant, P30 EY07551, from the National Eye Institute. References Abadi, R. V., & Bjerre, A. (2002). Motor and sensory characteristics of infantile nystagmus. British Journal of Ophthalmology, 86, 1152–1160. Abadi, R. V., & King-Smith, P. E. (1979). Congenital nystagmus modifies orientational detection. Vision Research, 19, 1409–1411. Abadi, R. V., & Sandikcioglu, M. (1975). Visual resolution in congenital pendular nystagmus. American Journal of Optometry & Physiological Optics, 52, 573–581. Abadi, R. V., Whittle, J. P., & Workfolk, R. (1999). Oscillopsia and tolerance to retinal image movement in congenital nystagmus. Investigative Ophthalmology & Visual Science, 40, 339–345. Abadi, R. V., & Worfolk, R. (1989). Retinal slip velocities in congenital nystagmus. Vision Research, 29, 195–205. Abadi, R. V., & Dickinson, C. M. (1986). Waveform characteristics in congenital nystagmus. Documenta Ophthalmologica, 64, 153–167. Andrews, D. P., & Miller, D. T. (1978). Acuity for spatial separation as a function of stimulus size. Vision Research, 18, 615–619. Badcock, D. R., & Wong, T. R. (1990). Resistance to positional noise in human vision. Nature, 343, 554–555. Bedell, H. E. (1992). Sensitivity to oscillatory target motion in congenital nystagmus. Investigative Ophthalmology & Visual Science, 33, 1811–1821. Bedell, H. E. (2000). Perception of a clear and stable visual world with congenital nystagmus. Optometry & Vision Science, 77, 573–581. Bedell, H. E. (2006). Visual and perceptual consequences of congenital nystagmus. Seminars in Ophthalmology, 21, 91–95. Bedell, H. E., & Bollenbacher, M. A. (1996). Perception of motion smear in normal observers and in persons with congenital nystagmus. Investigative Ophthalmology & Visual Science, 37, 188–195. Bedell, H. E., Tong, J., Patel, S. S., & White, J. M. (2008). Perceptual influences of extraretinal signals for normal eye movements and infantile nystagmus. In Leigh, R. J., & Devereaux, M. W. (Eds.), Advances in understanding the mechanisms and treatment of infantile forms of nystagmus (pp. 11–22). Oxford University Press. Bedell, H. E., Sridhar, D., & Queener, H. M. (in press). Aspects of visual perception in infantile nystagmus. In Harris, C. M., & Gottlob, I. (Eds.), Challenging nystagmus: Proceedings of the 2nd nystagmus network international workshop, Abingdon, UK, 2–5 September 2009. Cardiff, UK: Clyvedon Press. Bedell, H. E., Johnson, M. H., & Barbeito, R. (1985). Precision and accuracy of oculocentric direction for targets of different luminances. Perception & Psychophysics, 38, 135–140. Bedell, H. E., & Loshin, D. S. (1991). Interrelations between measures of visual acuity and parameters of eye movement in congenital nystagmus. Investigative Ophthalmology & Visual Science, 32, 416–421. Bedell, H. E., & Tong, J. (2009). Asymmetrical perception of motion smear in infantile nystagmus. Vision Research, 49, 262–267. Bedell, H. E., & Ukwade, M. T. (1997). Sensory deficits in idiopathic congenital nystagmus. In V. Lakshminarayanan (Ed.), Basic and clinical applications of vision science (pp. 251–255). Dordrecht, Netherlands: Kluwer. Bedell, H. E., White, J. M., & Abplanalp, P. L. (1989). Variability of foveations in congenital nystagmus. Clinical Vision Sciences, 4, 247–252.
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Vision Research journal homepage: www.elsevier.com/locate/visres
Spatial-bisection acuity in infantile nystagmus Michael T. Ukwade a, Harold E. Bedell a,b,⇑ a b
College of Optometry, University of Houston, Houston, TX 77204-6052, USA Center for Neuro-Engineering and Cognitive Science, University of Houston, Houston, TX 77204-4005, USA
a r t i c l e
i n f o
Article history: Received 9 December 2011 Received in revised form 27 April 2012 Available online 14 May 2012 Keywords: Infantile nystagmus Spatial bisection Hyperacuity Image motion Motion smear Meridional anisotropy
a b s t r a c t This study measured spatial bisection acuity for horizontally and vertically separated line targets in five observers with infantile nystagmus syndrome (INS) and no obvious associated sensory abnormalities, and in two normal observers during comparable horizontal retinal image motion. For small spatial separations between the line targets, bisection acuity for both horizontally and vertically separated lines is worse in the observers with IN than normal observers. In four of the five observers with IN, bisection acuity for small target separations is poorer for horizontally compared to vertically separated lines. Because the motion smear generated by the retinal image motion during IN would be expected to influence horizontally separated targets, the degradation of bisection acuity for both vertical and horizontally separated lines indicates that a sensory neural deficit contributes to impaired visual functioning in observers with idiopathic IN. Ó 2012 Elsevier Ltd. All rights reserved.
1. Introduction Infantile nystagmus syndrome (INS) is a condition characterized by incessant rhythmic eye movements, predominantly in the horizontal plane. The eye movements in INS typically are interrupted by brief periods referred to as foveation periods, during which the eye velocity is only a few deg/s or less, and the target of regard is imaged on or near the fovea (Dell’Osso & Daroff, 1975; Dell’Osso et al., 1992). Some individuals with INS, for example, those with albinism or rod monochromacy, have demonstrable abnormalities of the afferent visual system (Abadi & Bjerre, 2002; Cogan, 1967). Persons with so-called idiopathic infantile nystagmus (IN) exhibit no detectable abnormalities in the eye or the afferent visual pathways. Nevertheless, persons with idiopathic IN typically have visual acuity within the range of 20/20 to 20/100 (Abadi & Bjerre, 2002; Hanson et al., 2006) and elevated thresholds on several other visual spatial tasks (Abadi & Sandikcioglu, 1975; Bedell, 2006; Bedell & Loshin, 1991; Bedell & Ukwade, 1997; Goddé-Jolly & Larmande, 1973; Guo et al., 1989; Liu & Yang, 1997; Ukwade & Bedell, 1999; Ukwade, Bedell, & White, 2002). The eye movements of persons with nystagmus are accompanied by motion of the retinal image, which is known to degrade visual acuity in persons with normal vision (Brown, 1972; Chung & Bedell, 2003; Demer & Amjadi, 1993; Westheimer & McKee, 1975). In persons with IN, visual acuity typically varies with the parameters of eye movement, most notably the duration of the ⇑ Corresponding author at: College of Optometry, University of Houston, Houston, TX 77204-6052, USA. Fax: +1 713 743 2053. E-mail address: [email protected] (H.E. Bedell). 0042-6989/$ - see front matter Ó 2012 Elsevier Ltd. All rights reserved. http://dx.doi.org/10.1016/j.visres.2012.05.004
foveation periods (Abadi & Worfolk, 1989; Bedell, 2000; Cesarelli et al., 2000; Dell’Osso & Daroff, 1975; Sheth et al., 1995; Simmers, Gray, & Winn, 1999). A correlation exists also between visual acuity and the position variability of the foveation periods, that is, the standard deviation of the eye position during foveation periods during several seconds of continuous viewing (Bedell, White, & Abplanalp, 1989; Cesarelli et al., 2000). Acuity has been proposed to depend on the variability of the eye velocity during foveation periods as well (Dell’Osso & Jacobs, 2002; Dell’Osso et al., 1992; Sheth et al., 1995). Similar relationships exist between the duration and the variability of the foveation periods and acuity for other spatial tasks (Bedell & Ukwade, 1997; Dickinson & Abadi, 1985; Ukwade & Bedell, 1999). Because of the relatively slow temporal response of the visual system (e.g., Cogan, 1992; Efron, 1970), rapid motion of the retinal image produces motion smear, which in turn impacts negatively on aspects of spatial visual performance (Chung & Bedell, 1998; Morgan & Benton, 1989; Ramamurthy, Bedell, & Patel, 2005). For example, Morgan and Benton found that normal observers’ spatial-interval acuity is degraded by constant-velocity retinal image motion that is parallel to the direction of the target separation. The velocity of motion at which spatial-interval acuity becomes impaired is proportional to the separation between the targets, which is consistent with the expected effect of motion blur. More recently, Chung, LaFrance, and Bedell (2011) simulated the retinal image motion of observers with IN in normal observers and showed that the intervals of retinal image motion between the simulated foveation periods contribute to a degradation of visual acuity. Nevertheless, it remains unclear whether the image motion that accompanies the slow-phase eye movements of observers
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with IN results in a similar reduction of visual acuity, as observers with IN report a much smaller extent of perceived motion smear than normal observers during comparable retinal motion (Bedell & Bollenbacher, 1996; Bedell & Tong, 2009). The issue that we address here is whether the impaired spatial vision in persons with idiopathic IN is attributable solely to the presence of retinal image motion, or whether a sensory deficit contributes also to the reduction of visual performance in these individuals. Two approaches can be used to evaluate this issue. The first is to eliminate the retinal image motion in persons with nystagmus, for example, by presenting a visual target for such a brief duration that no appreciable retinal image motion can occur. Abadi and King-Smith (1979) found that contrast sensitivity for a vertical line flashed for only a fraction of a ms, a duration too brief to produce any appreciable motion smear, is reduced in patients with IN compared to normal observers. The measured reduction of contrast sensitivity therefore can be attributed to a sensory deficit. A second way to evaluate whether a sensory deficit exists in observers with idiopathic IN is to assess the visual performance of normal observers in the presence of target motion that simulates the retinal image motion in observers with IN (Bedell, 2006; Bedell & Ukwade, 1997; Chung & Bedell, 1995, 1996, 1997; Currie, Bedell, & Song, 1993; Dickinson & Abadi, 1985; Ukwade & Bedell, 1999). This strategy reveals the magnitude of visual impairment that is attributable specifically to the retinal image motion in observers with IN. Any additional impairment that exists in persons with idiopathic IN can be ascribed to the presence of a sensory abnormality. In the current study, we measured spatial-bisection acuity in persons with IN and in normal observers under comparable conditions of horizontal retinal image motion. Under optimal conditions, spatial bisection acuity is highly precise in normal observers (Andrews & Miller, 1978; Bedell, Johnson, & Barbeito, 1985; Klein & Levi, 1985; Stevens & Ducasse, 1912). A comparison between the bisection acuity of persons with IN and normal observers for targets that are separated in the direction of retinal image motion specifies the magnitude of the acuity loss in IN that is not attributable directly to the motion of the retinal image. In addition, because retinal image motion orthogonal to the direction of target separation should produce little or no degradation from motion smear, bisection acuity for vertically separated targets should approximate that in the absence of retinal image motion. Any impairment of bisection acuity in the observers with IN in this viewing condition therefore is not readily attributable to image motion. The results of both of the above comparisons indicate that a sensory abnormality contributes to the degradation of spatial vision in persons with idiopathic IN.
2. Methods 2.1. Observers Two young adult normal observers and five persons with idiopathic IN participated in this study, consequent upon their written informed consent. A third young normal observer provided confirmatory data for a subset of the experimental conditions. The normal observers demonstrated good ocular motility and achieved at least 20/20 visual acuity with appropriate optical correction. None of the observers with IN had any co-existing ocular or visual conditions. The clinical characteristics of the observers with IN are summarized in Table 1. As shown in the Table, the predominant waveforms of the IN observers include pendular and jerk waveforms, among others (Dell’Osso & Daroff, 1975). Tabulated values for the average amplitude and frequency of nystagmus and for the average duration of the foveation periods were determined from 10 to 20 s epochs of horizontal eye position that were recorded by infrared
limbal tracking while the observer viewed a small fixation target at 3.75 m in the straight-ahead direction. As will be discussed in Section 4 below, the observers’ nystagmus included small vertical and torsional components as well. The foveation periods were identified as intervals in the horizontal waveform when the eye velocity was slower than approximately 4 deg/s and the eye position was within a spatial window of ± 2 deg. The eye-movement parameters listed in Table 1 should be viewed as approximations, as the characteristics of IN may vary according to the visual task and the motivational state of the observer (Abadi & Dickinson, 1986; Cham, Anderson, & Abel, 2008; Dell’Osso & Daroff, 1975; Tkalcevic & Abel, 2005; Wiggins et al., 2007). However, all of the observers with IN as well as all of the normal observers had participated previously in psychophysical studies. Except for one of the normal observers, the observers were naive to the details of the experiment. 2.2. Stimuli and instrumentation The stimulus consisted of three bright (luminance = 100 cd/m2) horizontal or vertical lines, presented on a Hewlett Packard 1311B oscilloscope at a refresh rate of 240 Hz. Each line was 30 min arc long and, nominally, 0.2 min arc wide. The rest of the oscilloscope face was dark and the viewing duration was unlimited. The distance between the two outer, flanking lines of the three-line bisection stimulus ranged from 10 to 320 min arc, such that the mean separation between the central line and each of the 2 flanking lines varied between 5 and 160 min arc. On each trial, the central line was presented at one of 7 locations with respect to the midpoint between the two flanking lines. Using a joystick, the observer indicated whether the central line was either to the left or right, or above or below, of the midpoint position. Observers viewed the line stimuli through a mirror haploscope, which has been described in detail elsewhere (Ukwade & Bedell, 1999). Each channel of the haploscope contains one fixed and one moveable mirror. The moveable mirrors were mounted on matched G325D galvanometers and controlled by a pair of CCX650 Scanner controllers, both obtained from General Scanning, Inc. The controllers received input voltages that determined the mirror positions from a D/A card in a PC-compatible system. Horizontal retinal image motion of the bisection target was produced in the normal observers by oscillating the moveable mirrors around their vertical axes. Repetitive ramp motion of the haploscope mirrors approximated the image motion produced by a jerk IN waveform with an amplitude of 8° and a temporal frequency of 4 Hz. Because normal observers are unable to track this amplitude and frequency of motion (Wheeless, Cohen, & Boynton, 1967; Winterson & Steinman, 1978), we assume that the resulting retinal image motion closely approximated the motion produced by the oscillating mirrors. Previously, we found that the amplitude, frequency and type of the simulated IN waveform has relatively little impact on normal observers’ visual performance. Rather, visual acuity and contrast sensitivity depend primarily on the characteristics of the foveation periods, both when nystagmus image motion is simulated in normal observers and when measurements are made in observers with IN (Bedell, 2006; Chung & Bedell, 1995; Currie, Bedell, & Song, 1993; Dell’Osso & Jacobs, 2002; Dickinson & Abadi, 1985; Sheth et al., 1995). Accordingly, the simulated jerk IN waveform in the current study included a simulated foveation period which, during each block of 70 trials, had a duration of 20, 40, 80 or 120 ms. Position variability was not included in the simulated IN waveforms, as Badcock and Wong (1990) showed that small amounts of position jitter have little influence on spatial-interval acuity in normal observers. Fig. 1 shows samples of the simulated IN waveforms with 20 and 120 ms foveation durations.
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M.T. Ukwade, H.E. Bedell / Vision Research 64 (2012) 1–6 Table 1 Visual characteristics of subjects with infantile nystagmus.
3.0
120
19.0
26.2
Pendular with fov saccades
4.7
2.8
60
44.5
15.2
0.159
Jerk left
7.7
5.0
64
44.5
30.9
20/100
0.803
Pendular
10.8
3.0
36
241.1
100.7
20/50
0.336
Bi-dir jerk
4.6
1.8
71
54.6
13.8
Snellen acuity
JH
RE: plano LE: plano RE: +0.25 0.50 080 LE: +0.25 sphere RE: 3.00 1.75 005 LE: 3.00 1.00 003 RE: +5.25 4.00 180 LE: +4.00 3.50 168 RE: +2.00 1.75 155 LE: +2.25 1.50 177
27
20/20
0.195
Jerk left
16
20/25
0.114
24
20/30
17 27
FR MiS a
3.0
Age (yrs)
AJ
Optimal vertical bisection (arc sec)
Average foveation duration (ms)
Refractive error
CN
Optimal horizontal bisection (arc sec)
Average IN frequency (Hz)
Subject
Psychometric acuitya(LogMAR)
Predominant IN waveform
Average IN amplitude (deg)
Psychometric acuity was assessed using Landolt ring charts with controlled contour interaction (Flom, 1966).
2.3. Experimental procedures Because visual hyperacuities improve with practice (e.g., Fahle, Edelman, & Poggio, 1995; McKee & Westheimer, 1978), each observer received practice sessions using the bisection stimuli prior to the start of the experiment. Data collection commenced for each observer when additional practice produced no further improvement in bisection acuity. Spatial-bisection acuities were determined by probit analysis and correspond to a change from 50% to 84% on the psychometric function, generated using the method of constant stimuli. The psychometric functions plotted the percentage of ‘‘central-line-right-of-midpoint,’’ or ‘‘central-lineabove-the-midpoint,’’ responses against the position of the central line. The bisection acuities that are presented below for each observer, target orientation, and line separation represent the average of at least two replications per condition. 3. Results 3.1. Normal observers during simulated IN motion During image motion simulating an 8 deg, 4 Hz horizontal jerk nystagmus, normal observers’ bisection acuity for horizontally separated lines is best for an inter-line separation of 5 or 10 arc min (dashed lines in Fig. 2). For these small separations, bisection acuity improves systematically with the duration of the simulated foveation periods, from approximately 20 arc sec when the simulated foveation duration is 20 ms to approximately 10 arc sec when the simulated foveation duration is 120 ms (r = 0.93, p = 0.0008). When the horizontal inter-line separation exceeds 10 arc min, bisection acuity worsens approximately in proportion to the separation between the lines. The bisection acuity during horizontal image motion is slightly better for vertically than for horizontally separated lines (paired tdf=4 = 4.61, p = 0.010). For example, for lines that are separated vertically by 5 arc min, bisection acuity has an average value of 5.0 arc sec when the simulated foveation duration is 120 ms, compared to 9.1 arc sec when the lines are separated horizontally. For inter-line separations larger than 5 arc min, the advantage of vertically compared to horizontally separated lines for bisection acuity is smaller. In the absence of imposed image motion, the normal observers’ bisection acuity was essentially identical for horizontally and vertically separated targets (data not shown). 3.2. Observers with infantile nystagmus For the observers with horizontal idiopathic IN, spatial-bisection acuity for widely spaced (physically stationary) lines also worsens
approximately in proportion to the separation between the lines (Fig. 2). When the separation between the lines is reduced, the spatial-bisection acuity of the observers with IN either levels off, similar to the normal observers, or worsens. Except for observer JH, bisection acuity is poorer for horizontally than for vertically separated lines in the observers with IN, especially when the separation between the lines is small. The plots of spatial bisection acuity shown for the observers with IN in Fig. 2 are color coded to match the plots of the normal observers, when determined for a similar simulated foveation duration (see Table 1). For comparable conditions of retinal image motion, it is clear from the figure that the bisection acuity of the observers with IN typically is worse than that of the normal observers, for both vertically and horizontally separated line targets. The degradation of bisection acuity in the observers with IN compared to normal is most noticeable and consistent when the inter-line separation is small. The optimal values of horizontal bisection acuity for the observers with IN are related to their psychometrically measured visual acuities (rdf=3 = 0.978, p = 0.001; Table 1).
4. Discussion For vertically separated lines that are separated by 5 arc min, the average bisection acuity of the two normal observers is 5 arc sec, corresponding to 1/60th of the inter-line separation. For inter-line separations greater than approximately 5–10 arc min, the normal observers’ bisection acuity worsens approximately in proportion to the separation between the lines. Both of these results are consistent with data published previously by other investigators (e.g. Andrews & Miller, 1978; Bedell, Johnson, & Barbeito, 1985; Klein & Levi, 1985; Stevens & Ducasse, 1912). No horizontal–vertical anisotropy in bisection acuity existed when the normal observers were tested without imposed target motion. However, during horizontal motion that approximates the retinal image motion of observers with IN, normal observers’ bisection acuity is roughly 0.2 log units poorer for horizontally compared to vertically separated lines. Recently, Chung, LaFrance, and Bedell (2011) reported that the introduction of image motion to simulate that during IN slow phases degrades the visual acuity of normal observers by a similar amount. Earlier, Morgan and Benton (1989) showed that image motion parallel to the direction of target separation impairs spatial-interval acuity, a task that is closely related to bisection acuity. Like these previous authors, we attribute the degradation of acuity during horizontal target motion to the presence of motion smear. Specifically, we assume that spatial-bisection acuity, like other spatial-vision functions, is influenced by the physical motion of the retinal image, rather than
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Fig. 1. The horizontal angular position of the spatial bisection target is depicted as a function of time, when presented to normal observers during simulated jerk IN. The top and bottom panels show simulated IN waveforms with 20- and 120-ms foveation durations, respectively.
by the observer’s perception of motion. The reason for this distinction is that observers with INS typically do not report the perception of oscillopsia, despite the more-or-less incessant retinal image motion that accompanies their rhythmic eye movements, (e.g., Abadi, Whittle, & Workfolk, 1999; Kommerell, Horn, & Bach, 1986; Leigh et al., 1988; Tkalcevic & Abel, 2005). This assumption that spatial vision depends on retinal rather than perceived motion seems reasonable because it is difficult to appreciate how visual information can be recovered, once it is excluded from the spatio-temporal window of visibility (Watson, Ahumada, & Farrell, 1986) as the result of retinal image motion. Despite similar motion of the retinal image, the bisection acuity of observers with IN is worse than normal observers for horizontally-separated lines, especially when the inter-line separation is small. Consequently, bisection acuity is better for vertically compared to horizontally separated lines in four of the five observers with IN, especially for small inter-line separations. This outcome is consistent with the meridional anisotropy that is reported for other visual functions in observers with IN, including line detection (Abadi & King-Smith, 1979); grating contrast sensitivity (Abadi & Sandikcioglu, 1975; Bedell, 2006; Bedell & Loshin, 1991) Vernier acuity (Bedell & Ukwade, 1997), stereoacuity (Ukwade & Bedell, 1999) and motion detection (Bedell, 1992; Bedell, Sridhar, & Queener, in press; Shallo-Hoffmann et al., 1998). As horizontal image motion does not produce an anisotropy of normal observers’ acuity for horizontally vs. vertically oriented Vernier targets (Bedell & Ukwade, 1997), it is not clear that the meridional anisotropy of bisection acuity exhibited by the majority of the observers with IN can be attributed wholly to the retinal image motion that accompanies their nystagmus eye movements. Even so, all five of the observers with IN demonstrated poorer bisection acuity, compared to the normal observers, for vertically separated targets with small inter-line separations (Fig. 2, bottom). Previously, we measured the torsional and vertical components of nystagmus for 4 of the five observers in this study (JH, CN, AJ, FR)
Fig. 2. Spatial bisection acuity, in arc sec, is plotted against the average angular separation between the central line and the two outside flanking lines of the bisection target. Data for horizontally and vertically separated bisection targets are shown in the upper and lower panels, respectively. The inset in the upper panel illustrates the spatial layout of a horizontally separated bisection target. In each panel, the dashed lines without symbols are the average data for two normal observers during horizontal image motion to simulate a jerk IN waveform with one of four different foveation periods, i.e., violet: 20 ms; blue: 40 ms; green: 80 ms; red: 120 ms. The circles connected by solid lines are the bisection acuities for five different observers with IN. The color coding reflects each observer’s average foveation duration, i.e., observer FR (36 ms): blue; observer CN (60 ms): turquoise; observer AJ (64 ms): teal; observer MiS (71 ms): green; observer JH (120 ms): red. Error bars were omitted from the plots to prevent clutter. The average SEs for the two normal observers and for each of the observers with IN are 0.1 log units, for both horizontally and vertically separated bisection targets.
using the search-coil technique (Bedell et al., 2008). For these four observers, the amplitude of the torsional component of nystagmus ranged from 1.1 to 3.7 deg. For targets imaged on or near the fovea, the slight resulting rotations of the line targets would generate minimal motion smear and would be expected to exert little or no effect on either vertical or horizontal bisection acuity. In the same observers, the vertical component of nystagmus ranged in amplitude from 0.1 deg in observers JH and CN, which is comparable to the amplitude of normal observers’ eye movements during fixation, to between 0.6 and 0.7 deg in observers AJ and FR. If the duration of visual persistence is assumed to be approximately 125 ms (e.g., Efron & Lee, 1971), a vertical component of nystagmus with an amplitude of 0.65 deg and a frequency of 4 Hz would be expected to generate approximately 20 min arc of vertical motion smear, which potentially could interfere with bisection acuity for a range of small vertical inter-line separations. In agreement with this possibility, observer AJ exhibits poor bisection acuity for a vertical inter-line separation of 5 min arc and observer FR has the worst measured bisection acuities for vertical inter-line separations of 10 and 20 min arc. On the other hand, observers AJ and JH have essentially identical bisection acuities for vertical inter-line separations between 10 and 80 min arc, even though
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the vertical component of observer JH’s nystagmus is only approximately 0.1 deg. Moreover, bisection acuity for a vertical inter-line separation of 80 min arc is approximately two times worse than normal for all of the observers with nystagmus except MiS. These considerations indicate that the degradation of bisection acuity for vertically separated targets cannot be attributed completely to the presence of vertical retinal image motion in the observers with IN. Taken together, the results obtained for horizontally and vertically separated lines imply that a neural sensory abnormality contributes to the impairment of bisection acuity in observers with idiopathic IN. We conclude that the presence of incessant retinal image motion during visual development is likely to produce neuronal changes that underlie, at least in part, this impairment of visual performance. A comparable conclusion was reached also by previous authors, who either measured visual functions in observers with IN in the absence of retinal image motion (Abadi & King-Smith, 1979; Shallo-Hoffmann et al., 1998), or compared the visual functions of persons with IN and normal observers during comparable motion of the retinal image (e.g., Bedell, 2000, 2006). Acknowledgment This research was supported in part by Research Grant, R01 EY05068, and Core Center Grant, P30 EY07551, from the National Eye Institute. References Abadi, R. V., & Bjerre, A. (2002). Motor and sensory characteristics of infantile nystagmus. British Journal of Ophthalmology, 86, 1152–1160. Abadi, R. V., & King-Smith, P. E. (1979). Congenital nystagmus modifies orientational detection. Vision Research, 19, 1409–1411. Abadi, R. V., & Sandikcioglu, M. (1975). Visual resolution in congenital pendular nystagmus. American Journal of Optometry & Physiological Optics, 52, 573–581. Abadi, R. V., Whittle, J. P., & Workfolk, R. (1999). Oscillopsia and tolerance to retinal image movement in congenital nystagmus. Investigative Ophthalmology & Visual Science, 40, 339–345. Abadi, R. V., & Worfolk, R. (1989). Retinal slip velocities in congenital nystagmus. Vision Research, 29, 195–205. Abadi, R. V., & Dickinson, C. M. (1986). Waveform characteristics in congenital nystagmus. Documenta Ophthalmologica, 64, 153–167. Andrews, D. P., & Miller, D. T. (1978). Acuity for spatial separation as a function of stimulus size. Vision Research, 18, 615–619. Badcock, D. R., & Wong, T. R. (1990). Resistance to positional noise in human vision. Nature, 343, 554–555. Bedell, H. E. (1992). Sensitivity to oscillatory target motion in congenital nystagmus. Investigative Ophthalmology & Visual Science, 33, 1811–1821. Bedell, H. E. (2000). Perception of a clear and stable visual world with congenital nystagmus. Optometry & Vision Science, 77, 573–581. Bedell, H. E. (2006). Visual and perceptual consequences of congenital nystagmus. Seminars in Ophthalmology, 21, 91–95. Bedell, H. E., & Bollenbacher, M. A. (1996). Perception of motion smear in normal observers and in persons with congenital nystagmus. Investigative Ophthalmology & Visual Science, 37, 188–195. Bedell, H. E., Tong, J., Patel, S. S., & White, J. M. (2008). Perceptual influences of extraretinal signals for normal eye movements and infantile nystagmus. In Leigh, R. J., & Devereaux, M. W. (Eds.), Advances in understanding the mechanisms and treatment of infantile forms of nystagmus (pp. 11–22). Oxford University Press. Bedell, H. E., Sridhar, D., & Queener, H. M. (in press). Aspects of visual perception in infantile nystagmus. In Harris, C. M., & Gottlob, I. (Eds.), Challenging nystagmus: Proceedings of the 2nd nystagmus network international workshop, Abingdon, UK, 2–5 September 2009. Cardiff, UK: Clyvedon Press. Bedell, H. E., Johnson, M. H., & Barbeito, R. (1985). Precision and accuracy of oculocentric direction for targets of different luminances. Perception & Psychophysics, 38, 135–140. Bedell, H. E., & Loshin, D. S. (1991). Interrelations between measures of visual acuity and parameters of eye movement in congenital nystagmus. Investigative Ophthalmology & Visual Science, 32, 416–421. Bedell, H. E., & Tong, J. (2009). Asymmetrical perception of motion smear in infantile nystagmus. Vision Research, 49, 262–267. Bedell, H. E., & Ukwade, M. T. (1997). Sensory deficits in idiopathic congenital nystagmus. In V. Lakshminarayanan (Ed.), Basic and clinical applications of vision science (pp. 251–255). Dordrecht, Netherlands: Kluwer. Bedell, H. E., White, J. M., & Abplanalp, P. L. (1989). Variability of foveations in congenital nystagmus. Clinical Vision Sciences, 4, 247–252.
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