Download Static accommodation in congenital nystagmus.

Static Accommodation in Congenital Nystagmus
Editha Ong, Kenneth]. Ciuffreda, and Barry Tannen
Purpose. To conduct a comparative study of static accommodative function between individuals with normal vision (n = 10) and patients with congenital nystagmus (n = 12).
Methods. The component contribution to monocular steady-state accommodation (slope of the
accommodative stimulus/response function, accommodative controller gain, tonic accommodation, and depth-of-focus) was assessed subjectively using a Hartinger coincidence-optometer, except for depth-of-focus, which was determined psychophysically.
Results. The group mean slope for the patients with nystagmus was not significantly different
from that found in the normal subjects. However, their variability was markedly increased.
Therefore, the patients with nystagmus were divided into three subgroups with regard to the
normal accommodative stimulus/response function slope criterion. The majority of patients
with nystagmus (n = 10) exhibited slopes that were outside of normal limits, being greater than
(n = 4) or less than (n = 6) the normal range. Depth-of-focus was the only parameter found to
be significantly different between the normal and the nystagmus groups. When the nystagmus
group was divided with respect to etiology—ie, albinotic (n = 4) versus idiopathic (n = 8)—
there were no significant differences found for the various accommodative parameters.
Conclusions. We speculate that the primary component contributing to the anomalous accommodative behavior was the increased depth-of-focus, with this perhaps being related to abnormal fixational eye movements and eccentric fixation, and more generally related to overall
reduced sensitivity resulting from the early abnormal visual experience. Invest Ophthalmol Vis
Sci. 1993;34:194-204.
.Accommodation refers to the ability to alter the
dioptric power of the crystalline lens to maximize retinal-image contrast and clarity. It is influenced by a
variety of stimulus parameters, including target vergence, contrast, spatial frequency composition, eccentricity, and retinal-image motion.1 Studies that have
investigated the relation between accommodation and
stimulus parameter effectiveness in individuals with
normal vision have demonstrated that an optimal acFrom SUNY/State College of Optometry, Department of Vision Sciences,
New York, Neiu York.
This research was supported in part by the Schnunnacfier Institute for
Vision Research.
Submitted for publication: January 16, 1992; accepted June 26, 1992.
Proprietary interest category: N.
Reprint requests: Editha Ong, SUNY/State College of Optometry,
Department of Vision Sciences, 100 East 24th St., New York, NY 10010.
commodative stimulus is represented by a stationary,
high-contrast square-wave grating positioned at the
fovea.1 Introduction of sub-optimal stimulus conditions, such as increased target motion, may adversely
affect the quality of the retinal image and reduce accommodative accuracy.23
Of particular interest in the present study was the
clinical condition of nystagmus. It exists in approximately 0.025% of the general population.4 Nystagmus
frequently is of an idiopathic, congenital origin and is
characterized by a binoculaiiy conjugate, involuntary
rhythmic oscillation of the eyes. This abnormal movement is broadly classified into pendular or jerk waveforms.5'6 The former type is characterized by an oscillation that has similar velocities in each direction,
whereas the latter is characterized by markedly unequal velocities in each direction that consist of a slow
194
Investigative Ophthalmology & Visual Science, January 1993, Vol. 34, No. 1
Copyright © Association for Research in Vision and Ophthalmology
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Static Accommodation in Congenital Nystagmus
error-producing component followed by a fast errorcorrecting saccade. Either type of eye movement waveform can be quantified in terms of parameters such as
amplitude, frequency, intensity, maximum slow-phase
velocity, and foveation duration.7"10
As a result of these abnormal eye movements, retinal-image motion is considerably increased in patients
with nystagmus. This motion typically exhibits maximum velocities that exceed 3 deg/sec,9 which have
been shown to impair a variety of vision functions,
including visual acuity,11 threshold contrast perception,12 and visual discrimination.13 Such abnormal retinal-image motion also may cause the attenuation or
even elimination of the high spatial frequency components of a square-wave-type target such as a clinical
Snellen test letter, effectively "smearing" its sharp
borders.14 Such motion also may decrease apparent
target contrast.2 Moreover, most patients with nystagmus exhibit reduced sensory-based visual acuity15 and
motor-based eccentric fixation.16 Any of the above
factors have the potential to degrade the quality of the
retinal image enough to reduce accommodative stimulus effectiveness.
Relatively little is known about the overall visual
performance in nystagmus; this is especially true regarding accommodative ability. Ciuffreda and Goldrich17 measured the steady-state accommodative stimulus/response function and found increased accommodative error. However, only a single subject was
tested, and average accommodative error was the sole
parameter considered. Dickinson18 reported that accommodation followed the typical stimulus/response
curve in her five patients with congenital nystagmus
tested. However, no data or analysis was provided.
Therefore, the present study was conducted to investiTABLE l.
Subject
VN1
VN2
VN3
VN4
VN5
VN6
VN7
VN8
VN9
VN10
Mean
±SEM
195
gate more comprehensively, and in a relatively large
group of subjects, the components of steady-state accommodative function in nystagmus.
MATERIALS AND METHODS
The subjects consisted of 10 individuals with normal
vision and 12 patients with congenital nystagmus (8
idiopathic patients, 4 albinos). The normal group consisted of faculty and students from SUNY/State College of Optometry. Their ages ranged from 21-34 yr,
with a mean of 28 yr. All had a corrected Snellen visual
acuity of at least 20/20 in the tested eye, with a mean
spherical equivalent refractive error of —1.51 ± 0.46
D (standard error of the mean). The male-female ratio
was 3:7. None of the subjects reported or had evidence of ocular, systemic, or neurologic disease. The
group of patients with nystagmus was recruited from
the Oculomotor Diagnostic and Biofeedback Therapy
Clinic and the Low Vision Clinic at SUNY/State College of Optometry. Their ages ranged from 17-40 yr,
with a mean of 30 yr. The corrected Snellen visual
acuity ranged from 20/20 to 20/200. The mean spherical equivalent refractive error for the tested eye was
— 1.40 ± 0.69 D (SEM), with a preponderance of withthe-rule astigmatism (x = —2.18 D X 5), as has been
found by others.1019 The male-female ratio was 11:1.
This much higher incidence of males in the nystagmus
population is consistent with previous studies.4519
Both groups of subjects had amplitudes of accommodation measured with the subjective clinical "pushup" technique20 of at least 1 D beyond the highest
dioptric stimulus level tested to minimize response saturation effects.21 Clinical data for each of the subjects
are presented in Tables 1 and 2. Informed consent
Summary of Clinical and Experimental Results of Normal Subjects
Age
(yr)
Refractive State
(Right Eye; diopters)
21
-1.50 sph
Piano
-4.00 sph with -0.75 cyl X 180
-0.50 sph
-2.25 sph
-1.00 sph
-1.75 sph
Piano
-3.25 sph
-1.00 cyl X 90
— 1.51 sph eq
0.46
22
23
25
28
28
31
32
34
34
28
1.55
VA
20/20
20/15
20/15
20/20
20/15
20/15
20/15
20/15
20/15
20/20
—
Est
Ace
S/R
Slope
0.80
0.72
0.69
0.69
0.80
0.67
0.67
0.80
0.69
0.66
0.72
0.02
Abso
DF
(±D)
TA
(D)
0.48
0.69
0.87
0.74
0.18
0.32
0.31
0.54
0.28
0.40
0.48
0.07
0.83
0.25
1.27
1.60
1.27
1.81
2.08
1.79
2.42
2.38
1.57
0.22
AE
ACG
(3D)
6.53
12.95
7.01
0.68
0.43
0.68
0.06
1.02
0.28
0.08
0.39
0.40
0.50
0.45
0.09
—
1.93
17.56
3.99
3.14
2.07
4.82
6.67
1.77
VA, Snellen visual acuity. VN, visually normal. Est Ace S/R Slope, estimated accommodative stimulus/response slope. DF, depth of focus.
TA, tonic accommodation. ACC, accommodative controller gain. Abso AE, absolute accommodative error at 3 D stimulus level, sph, sphere,
cyl, cylinder, sph eq, spherical equivalent.
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Investigative Ophthalmology & Visual Science, January 1993, Vol. 34, No. 1
196
TABLE 2.
Summary of Clinical and Experimental Results in Patients With Nystagmus
Nystagmus
Accommoaanon
Subject/
Age
(yr)
Refractive
State
(Right Eye;
diopters)
Max
Slow
Der
Ecc
Phase
Visual
Fix
Vel
Acuity
Amp. Freq Int
(RE) Type (deg) (deg) (Hz) (deg-Hz) (deg/sec)
20/100 Jerk
1 A/30*ft +2.00 - 4 . 5 0 X5
1B/32ft - 1 . 7 5 - 2 . 2 5 X180 20/60 jerk
lC/38f
ID/20
2A/23
2B/39*ft
3A/17
3B/24
3C/27*
3D/30f
3E/38*f
3F/40
Mean
±SEM
+0.25
+ 1.50-1.00 +5.00 -0.75 -3.50 +0.75 -1.25-3.00 -3.00 -
1.25 XI80
4.50 X180
2.50 X10
2.00 X20
1.50 X180
1.50 X180
1.00 X135
2.25 X70
0.75 XI80
20/60
20/70
20/40
20/100
20/100
20/30
20/200
20/30
20/100
20/20
-1.40 sph eq 20/80
—
0.69
Jerk
jerk
Jerk
Jerk
Jerk
Jerk
Pend
Pend
Jerk
Jerk
—
—
0.91
2.39
—
—
0.58
1.18
—
0.39
6.49
0.76
0.04
0.25
1.44
0.67
2.09 4.70
5.12 3.25
2.20 2.60
9.82
16.64
5.72
41.80
72.44
20.00
—
—
—
—
3.27
5.96
1.72
4.77
11.11
1.29
2.42
1.46
5.22
3.87
2.43
4.23
4.77
4.05
2.39
3.15
17.07
23.07
4.18
20.18
52.99
5.22
5.78
4.60
32.91
57.35
10.58
45.55
139.40
17.56
19.67
8.94
3.76 3.70
0.88 0.30
15.02
4.33
42.38
11.44
Est
Fov
Dur
(ms)
Est
Ace
Abso
AE
S/R DF TA
Slope (±D) (D) ACG (3D)
1.08
0.93
1.18
0.96
0.70
0.76
0.48
0.52
0.59
0.21
0.47
0.56
0.83
1.97
0.19
0.40
0.69
2.31
2.07
1.16
1.41
0.76
0.59
0.93
1.89
0.58
2.88
0.17
1.41
1.13
0.95
2.75
0.60
1.28
1.38
1.56
3.68 1.86
0.11
0.68
30.18 0.25
3.62 0.19
—
0.08
12.55 1.09
2.17 0.43
2.31 2.71
1.46 1.11
5.04 0.25
9.46 0.02
96 0.70
17.98 0.08
1.11
0.20
1.38
0.24
7.83 0.73
3.05 0.24
150
113
—
—
48
50
178
40
27
60
160
134
—
—
* Indicates albinos.
f Received auditory biofeedback training.
X Indicates the presence of strabismus.
Subject subgroups: IA-D (high slopes); 2A-B (normal slopes); 3A-D (low slopes).
Der Ecc Fix, derived eccentric fixation. Amp., amplitude. Freq, frequency. Int, intensity. Max Slow-Phase Vel, maximum slow-phase velocity.
Est Fov Dur, estimated foveation duration. Esi Ace S/R slope, estimated accommodative stimulus/response slope. DF, depth of focus. TA,
tonic accommodation. ACG, accommodative controller gain. Abso. AE, absolute accommodative error at 3 D stimulus level, sph, sphere, cyl,
cylinder, sph eq, spherical equivalent.
from all subjects was obtained before the experiment
began and after a full description of the procedures
had been given. The tenets of the Declaration of Helsinki were followed, and institutional human experimentation committee approval was obtained.
Steady-state accommodation was measured monocularly in the right eye using a subjective Hartinger
coincidence-optometer based on the Scheiner's principle22 (Fig. 1). This optometer recently was shown to
provide readings identical to that found using an
open-field, infrared recording optometer with Snellen-type visual stimuli.23 Appropriate refractive correction was placed in the spectacle plane over the right
eye, whereas the left eye was fully occluded during the
experimental session. Head movement was restrained
by a chin and headrest assembly. The optometer target
consisted of two sets of three vertically oriented, dimly
illuminated bars (1.6° vertical, 0.8° horizontal) viewed
under approximately open-looped conditions afforded by the 1 mm exit pupil of the optometer.
After a period of total darkness for 5 min to allow
any accommodative hysteresis effects to dissipate, pretask tonic accommodation was assessed in total darkness except for the dim open-loop optometer bars.24'25
To minimize potential proximal influences, the subjects were instructed to "gaze beyond" the optometer
bars into the distance.25 The two sets of optometer bar
targets initially were displaced in alternating lateral di-
rections by the experimenter. They then were gradually moved toward each other, until precise vertical
alignment of the bars was reported by the subject
upon depression of a hand-held clicker, with this value
representing the refractive state of the eye (ie, pre-task
tonic accommodation).
The accommodative stimulus/response function
l. Schematic diagram of the experimental apparatus
used to measure accommodation (top view, not drawn to
scale). HO, Hartinger coincidence-optometer. AS, accommodative stimulus. RSC, reduced Snellen chart. BL, Badal's
lens. HSM, half-silvered mirror. FLA, field-limiting aperture. EP, eye patch. Inset shows the Snellen chart target.
The two sets of optometer bars are optically superimposed
on a letter from the reduced Snellen chart.
FIGURE
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Static Accommodation in Congenital Nystagmus
then was generated using a target that consisted of a
high-contrast, reduced Snellen visual acuity chart (total angular extent = 3°) with letters ranging from 20/
40 to 20/200. This chart was incorporated into Badal's
system, which ensured that retinal-image size and illumination remained constant.22 The Snellen chart (luminance = 50 cd/m2) was illuminated with a tungsten
filament lamp and was reflected into the eye by a partially silvered mirror. The subjects were instructed to
fixate a letter from the row of letters that was at or one
line above their visual resolution limit. The position of
the optometer bars then was adjusted until they were
immediately adjacent to the fixated letter (Fig. 1, inset). The subjects were instructed to keep the letter in
focus at all times, but to refrain from exerting any
special effort21; patients with nystagmus were told to
refrain from adopting any learned or trained strategy
to control their eye movements.817 While attempting
to maintain accurate fixation and focus, the subject's
task was to report vertical alignment of the optometer
bars. This value represented the steady-state accommodative response. The dioptric stimulus levels generally were 0, 1, 2, 2.5, 3, 4, 5, 5.5, and 6 D, although
most subjects did not receive all stimuli because of
amplitude limitations.
The order of stimulus presentation, as well as initial offset magnitude and direction of the optometer
targets, were randomized. Brief rest periods between
measurements were provided, wherein the subjects
were instructed to gaze and focus upon a set of vertical
1 cycle per degree black-and-white square-wave gratings that subtended an angle of 5° outside the instrument located 3 feet from the subject to minimize fatigue and accommodative hysteresis effects. Immediately after the accommodative stimulus/response
function was measured, post-task tonic accommodation was obtained to assess possible hysteresis effects.
Six measurements were taken at each stimulus condition and referenced to the corneal plane to approximate their ocular accommodation. From this information, the slope over the linear region (excluding the <2
D nonlinear region)22 of the accommodative stimulus/
response function (closed-loop system gain) could be
determined.
The patients with nystagmus who underwent 5-15
wk of previous successful biofeedback training (n
= 6),8>17>26 were, in addition, re-assessed at accommodative stimuli levels of 0 and 2.5 D. However, they
were now explicitly instructed to adopt whatever strategy they learned during their biofeedback training to
stop or reduce their abnormal eye movements. Aside
from this difference in the instruction set to this subgroup of patients with nystagmus, the experimental
procedures were identical to the above.
Depth-of-focus for each subject was measured subjectively using the apparatus shown in Figure 2.22>27>28
197
UB
T
' T
4.
BL
EP
FLA
FIGURE 2. Schematic diagram of the experimental apparatus
used to measure depth-of-focus (top view, not drawn to
scale). UB, uniformly illuminated diffuse background. T,
target. BL, Badal's lens. FLA,field-limitingaperture. EP,
eye patch. Target configuration is shown in inset.
It consisted of a back-illuminated, high-contrast complex target presented within Badal's optical system.
Target configuration was composed of black-andwhite pie-shaped sectors arranged in a circular fashion
(Fig. 2, inset). The sectors subtended an angle of 48 at
their extreme peripheral ends and tapered to a fine
point (<1.5 min arc) centrally. Moreover, they were
superimposed on three black concentric circles of increasing diameters, with the inner, middle, and outermost circles subtending angles of 2.0°, 4.8°, and 8.0°,
respectively. The target was physically divided, with
the two vertical halves juxtaposed to one another. The
left hemifield was fixed at a stimulus value of 1.5 D,
whereas the proximal/distal dioptric position of the
right half could be adjusted manually by the experimenter. The subject's head and chin were positioned
in their respective rests. The left eye was fully occluded; the right eye viewed the target through the
appropriate refractive correction in the spectacle
plane. The left and right targets initially were positioned in the same optical plane (1.5 D). The subject
was instructed to fixate and to keep in focus the central portion of the inner circle and nearby pie-sectors
on the stationary target. The experimenter then very
slowly (approximately 0.05 D/sec) displaced the right
half of the target in one direction, proximally or distally, until the subject indicated with a hand-held
clicker slight blur of the immediate right side while
maintaining fixation and clarity of focus on the central
left half.
The initial direction of displacement of the right
half of the target was randomized. The measurements
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Investigative Ophthalmology & Visual Science, January 1993, Vol. 34, No. 1
198
DF
ACG
/
AS
AE1
_
—
/
FIGURE 3. Block diagram of the static model of the accommodative system. The difference
between the accommodative stimulus (AS) and accommodative response (AR) is the accommodative error (AE). DF represents one-half the depth-of-focus, ACG is the accommodative
controller gain, and TA is tonic accommodation. AE1 is the output of AE after DF; the
PLANT represents the peripheral accommodative apparatus. (Adapted from Hung and
Semmlow, 1980.)
were repeated for a total of two readings in each direction. They were averaged and converted to diopters to
obtain the total depth-of-focus. These data, including
the tonic accommodation values, were used to calculate the accommodative controller gain (open-loop
system gain) based on the model equation:
judged to be stationary by direct visual inspection of
the eye movement records. This represented baseline/
foveation6 and was averaged across 15 cycles of nystagmus.
accommodative controller gain
The accommodative findings for each of the subjects
are presented in Tables 1 and 2. Group mean accommodative stimulus/response functions for the normal
subjects and the patients with nystagmus are shown in
Figure 4. Regression analysis over the linear range of
the functions indicated that the slope was 0.72 ± 0.02
(SEM) with a range of 0.66-0.80 for the normal subjects and 0.70 ± 0.08 (SEM) with a range of 0.21-1.18
= (accommodative response
— tonic accommodation)/
(final steady-state accommodative error
- 1/2 depth of focus)
(Fig. 3)29 for data points in the linear response range
of the accommodative stimulus/response function.
Eye movement records were obtained independently for each patient with nystagmus at the Oculomotor Diagnostic and Biofeedback Therapy Clinic at
SUNY/State College of Optometry. Horizontal eye
position was measured objectively using the infrared
reflection technique (0.25° resolution, ±8° linearity)30 and recorded on a three-channel strip chart recorder (0-40 Hz bandwidth). Calibration was performed using a three-point paradigm (5° left, center,
5° right); the error in calibration, and in the estimate
of eccentric fixation, was approximately 0.25°-0.5°.
Amplitude and frequency were obtained from noncontinuous samples of the eye movement records that
totaled at least 11-38 sec and 28-58 sec, respectively.
Intensity was calculated by multiplying the amplitude
by its frequency.7'31 Maximum slow-phase velocity, on
the other hand, was obtained as the average from discrete portions of records from at least 10-17 sec. Estimated (motor-based) eccentric fixation was derived
from taking the time-average position of the eye during the nystagmus slow-phase,16 with the mean being
obtained from random samples that totaled 15 beats.
Estimated foveation duration was taken as the time
interval per nystagmus beat during which the eye was
RESULTS
GROUP ACCOMMODATIVE STIMULUS/RESPONSE CURVES
1:1 .
— *) Normals:
y= 0.72x + 0.51
r= 0.95
- - • ) Nystagmats:
y= 0.70x + 0.32
r= 0.68
4
5
6
7
8
9
10
11
ACCOMMODATIVE STIMULUS
(Diopters)
FIGURE 4. Group accommodative stimulus/response functions for the subjects with normal vision and patients with
nystagmus. The corresponding symbols, linear regression
functions, and correlations are as indicated. Sample size for
the normal group was 10; sample size for the patients with
nystagmus was at least 9 for all the closed symbol data and
equal to or less than 5 for the open symbol data. The 1:1 line
is the theoretical accommodative demand line. Symbols and
error bars represent the group mean ± 1 SEM.
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Static Accommodation in Congenital Nystagmus
199
ABNORMAL NYSTAGMUS SUBGROUPS
of the normal subjects (F = 24.24, df = 11,9, P
< 0.005). The nystagmus accommodative data therefore were divided into subgroups according to a slope
criterion (Fig. 5). A plot for a representative subject
from each subgroup also is shown in Fig. 6. The individual slopes for the first subgroup (n = 4) were at
least 3 SEMs greater than the mean slope of the normal group. The second subgroup (n = 2) consisted of
individuals whose slope was within ±3 SEMs of the
normal group mean. The last nystagmus subgroup (n
= 6) had individual slopes that were at least 3 SEMs
below that of the normal subjects' mean value. Nystagmus slope means were 1.04, 0.73, and 0.47 for subgroups 1, 2, and 3, respectively. A one-way analysis of
variance confirmed that the accommodative response
differences among the normal group and the three
nystagmus subgroups were significant (F = 28.11, df
= 3,18, P < 0.001). Furthermore, Tukey's honesty significant difference (HSD) test indicated that significant differences existed between all groups (P < 0.05),
except (as expected) the second nystagmus subgroup
and the normal group.
Both inter- and intra-subject response variability
were greater in the patients with nystagmus than in the
normal subjects. Regarding inter-subject variability,
the group mean SEM was 0.13 D ± 0.02 for the normal subjects (across all stimulus levels) and 0.24 D
± 0.03 for the patients with nystagmus (across a stimulus range of 0-5 D). With respect to intra-subject variability, the patients with nystagmus showed an increased mean and range of SDs for far and near tar-
ACCOMMODATIVE STIMULUS/RESPONSE CURVES
1:1.
it
): y= 0.97x - 0.13 (n=4)
(A): y= 0.50x + 0.77 (n=6)
2
3 4 5 6 7 8 9
ACCOMMODATIVE STIMULUS
(Diopters)
10
11
FIGURE 5. Plots of the a b n o r m a l nystagmus s u b g r o u p s . Subg r o u p mean data are s u p e r i m p o s e d on c o r r e s p o n d i n g linear
regression lines. Closed circles and o p e n triangles r e p r e s e n t
s u b g r o u p s whose slopes are, respectively, greater o r less
than the slope of the normal subjects r e p r e s e n t e d by the
dashed line. T h e nystagmus s u b g r o u p linear regression
functions are as indicated. T h e slope values are slightly different from those given in " R e s u l t s " because of the averaging process. Sample sizes are as indicated. Symbols and e r r o r
bars r e p r e s e n t the s u b g r o u p mean ± 1 SEM.
for the patients with nystagmus. This difference in
slope was not significant (t-test, P > 0.05). However,
the group variability in slope (ie, SEM) for the patients
with nystagmus was significantly greater (4X) than that
O
•l-H
3
Post-TA
Pre-TA
CO
o
8
9
CO
w
6
NSG2A
NSG3A
B
52Q
•IAS*
O
2
o
u
o
6. Plots of representative subjects from each diagnostic subgroup. VN, visually
normal. NSC 1B, 2A, 3A, nystagmus subgroups with correspondingly high, normal, and
low accommodative slopes. 1:1
line represents the theoretical
accommodative demand line.
FIGURE
4
Port-TA
Pw-TA
a
ACCOMMODATIVE STIMULUS (Diopters)
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9
200
Investigative Ophthalmology & Visual Science, January 1993, Vol. 34, No. 1
2.5
w
I
20
Normals (N=10)
Nystagmats (N=12)
a 2 1.5
^s
1>0
s
^
S
o.o
0
iJili
1
2
2.5
3
4
5
5.5
8
ACCOMMODATIVE STIMULUS
(Diopters)
FIGURE 7. Histogram of the group mean absolute accommodative error as a function of accommodative stimulus level.
Bar graphs and error bars represent the group mean + 1
SEM. No data for stimulus levels 2.5 and 5.5 D were obtained for the normal subjects.
gets in each subject. They exhibited a mean SD of 0.42
D (range 0.09-1.03) and 0.36 D (range 0.12-0.63) for
accommodative stimulus levels 0 and 3 D, respectively.
In contrast, the normal subjects exhibited a mean SD
of 0.24 D (range 0.12-0.34) and 0.25 D (range 0.090.47) for accommodative stimulus levels 0 and 3 D,
respectively.
The mean absolute accommodative error for the
normal subjects and patients with nystagmus is shown
in Figure 7. It was 50% greater in the patients with
nystagmus than in the normal subjects. However, only
at stimulus levels of 1, 4, and 6 D was the mean absolute accommodative error significantly greater in the
patients with nystagmus (t-test, P < 0.01).
In addition to the accommodative slope and related absolute accommodative error, other accommodative parameters investigated included accommodative controller gain (ACG), tonic accommodation
(TA), and depth-of-focus (DF; Fig. 2). The corresponding group mean (±1 SEM) ACG, TA, and '/2DF
were 6.67 ± 1.77, 1.57 ± 0.22 D and 0.48 ± 0.07 D,
respectively, for the normal subjects and 7.83 ± 3.05,
1.38 ± 0.24 D, and 1.11 ± 0.20 D, respectively, for the
patients with nystagmus. These are graphically presented in Figure 8. The only parameter with a significant group mean difference was depth-of-focus (t
= —2.75, P < 0.02). The one-way analysis of variance
between the normal subjects and the nystagmus subgroups also revealed a significant difference only for
DF (F = 3.23, df = 3,18, P < 0.05). However, Tukey's
HSD test showed no significant difference. This lack
of subgroup significance appears to have resulted
from the relatively low probability of our analysis of
variance test (P = 0.046) and the reduced power of the
post-hoc comparison analysis with the reduced sample
sizes.
There was no significant correlation between
slope of the accommodative stimulus/response function and the other accommodative parameters (P
> 0.05). Correlation performed between each of the
four accommodative parameters and the six eye movement parameters indicated that significant correlations were found only between ACG and nystagmus
frequency (r = -0.71, P < 0.05) and between ACG
and foveation duration (r = +0.74, P < 0.05). A lack of
significant correlation (P > 0.05) was found between
the four accommodative parameters and the clinically
derived Snellen visual acuity.
The eye movement results for each of the patients
with nystagmus are presented in Table 2. Eye movement parameter values were determined for the patients with nystagmus based on objective recordings.
The means (±1 SEM) of amplitude, frequency, intensity, maximum slow-phase velocity, derived eccentric
fixation, and estimated foveation duration were: 3.76°
± 0.88°, 3.70 ± 0.30 Hz, 15.02 ± 4.33 deg-Hz, 42.38
±11.44 deg/sec, 1.44° ± 0.67°, and 96 ± 17.98 ms.
Significant positive correlations were found between
Snellen acuity and eye movement amplitude (r = 0.70,
P < 0.02), intensity (r = 0.69, P < 0.02), maximum
slow-phase velocity (r = 0.72, P < 0.02), and derived
eccentric fixation (r = 0.80, P < 0.02).
For the patients with nystagmus who underwent
successful auditory biofeedback training (n = 6),
group mean accommodative responses increased in
magnitude by approximately 25% (from 1.78 ± 0.18 D
to 2.25 ± 0.30 D) and 35% (from 1.96 ± 0.37 D to 2.66
Normals (N=10)
Nystagmats (N=12)
III I
AS/R
SLOPE
DF
TA
ACG/10
ACCOMMODATIVE PARAMETER
FIGURE 8. Plot of the group data for the different accommodative parameters. AS/R slope, accommodative stimulus/response slope in the linear range. DF, one-half depth-of-focus. TA, tonic accommodation. ACG, accommodative controller gain. Units for DF and TA are in diopters. Plotted is
the mean + 1 SEM. Sample sizes are as indicated, except for
ACG, where n = 9.
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Static Accommodation in Congenital Nystagmus
± 0.40 D) at the retested stimulus levels of 0 D and 2.5
D, respectively. Group mean absolute accommodative
error for the zero diopter stimulus level increased with
biofeedback training (from 1.78 ± 0.18 D to 2.25
± 0.30 D), whereas it decreased slightly (from 0.83
± 0.24 D to 0.66 ± 0.28 D) for the 2.5 D stimulus level.
However, the group mean pre/post-dioptric differences were not significant at either stimulus level (ttest, P > 0.05).
A separate analysis also was conducted in which
the nystagmus group was subdivided with respect to
etiology into idiopathic patients and albinos. There
was no significant difference between the two subgroups for the four accommodative parameters (t-test,
P ~2i 0.15). Therefore, both groups contributed to the
overall finding of increased depth-of-focus in the patients with nystagmus. Lack of difference in the four
accommodative parameters also was true when the
above two subgroups were compared with the normal
subjects (Tukey's HSD, P > 0.05). This is consistent
with our earlier analysis of variance result when the
three nystagmus slope-derived subgroups were compared with the normal subjects. Finally, when the albinos were excluded, there was significant correlation
between slope and ACG (r = +0.78, P < 0.05).
DISCUSSION
The present finding of abnormal accommodative behavior in the majority of patients with nystagmus is not
completely surprising. This initially might be attributed to their general overall increase in retinal-image
motion. The abnormal eye movements, in and of
themselves, present a less than ideal situation for appropriate stimulation of the accommodative system.
Eye movements result in smearing of the target's
edges, adversely affecting its retinal contrast gradient.232 This also reduces the target's high spatial frequency components.2'32'33 Previous work34"37 has demonstrated that the absence of higher-order, odd-harmonics may adversely affect the accuracy of static and
dynamic accommodation,1432'33 preventing the system
from "fine-tuning" its accommodative response.35
More specifically, what is the effect of the jerk
nystagmus slow-phase on steady-state accommodative
accuracy? First, there is the continuous increase in
slow-phase velocity. Recent results in individuals with
normal vision have shown that retinal-image motion
greater than approximately 10°/sec (range 6-12°/
sec) was sufficient to degrade accommodation, with
the response approaching the tonic accommodative
level.2-3 Therefore, the period of extended foveation
(^5°/sec) plus the subsequent slow-phase component
(5-10°/sec) can provide some degree of blur stimulation to the accommodative system. This is consistent
with the work of others regarding detailed vision tasks,
201
such as visual acuity.49 However, for nondetailed vision tasks, such as detecting a flash of light38 or target
motion,39 the entire slow-phase period may be useful.
Second, there is the continuous increase in retinal
eccentricity. Eye movements cause the retinal image to
impinge upon different retinal loci at various times
during the slow phase of the nystagmus, with these
foveal and near eccentric retinal loci continually
changing the effective accommodative stimulation,
hence increasing accommodative variability.l'24'40'41
This is consistent with the increased response variability found in the present group of patients with nystagmus. As a result of this, the retinal image would impinge, on average, at a peripheral locus that produces
slightly reduced accommodative gain compared to the
fovea.22-24 Using a time-average definition, essentially
all patients with nystagmus would exhibit some degree
of (motor-based) eccentric fixation,16 with the present
group of patients with nystagmus showing a mean (derived) eccentric fixation of 1.4°. However, the effect
of eccentric stimulation depends upon nystagmus
slow-phase velocity. Only when the velocity is less than
10°/sec, with the target still providing some degree of
accommodative stimulus effectiveness, would eccentricity also contribute to the reduced accommodation.
Above 10°/sec, the retinal-image motion is too rapid
to provide much stimulation to the accommodative
system, regardless of the degree of eccentric retinal
stimulation2; thus, the accommodative response would
transiently and passively drift to its tonic level. This
demonstrates the presence of a critical and complex
velocity/eccentricity interaction. A similar argument
regarding constantly changing retinal image velocity
and eccentricity can be made for the subjects with
pendular nystagmus.
The patients who reduced their nystagmus using a
strategy learned during prior eye movement auditory
biofeedback treatment showed little consistent improvement in accommodative accuracy, although
there was a tendency for the mean accommodative
error to decrease by approximately 0.20 D at near.
Note that despite the presence of eye movements that
constantly displaced the eyes away from the object of
regard, there also were compensatory saccadic eye
movements in the opposite direction. These corrective
eye movements function to re-establish foveation.
These periods of foveation, albeit of short duration
(27-178 ms; mean 96 ms), apparently were sufficient
to enable the subject to assess accommodative stimulus magnitude, detect the accommodative error, and
respond within the tolerance imposed by the quality of
the retinal image and subsequent neurosensory processing limitations. Furthermore, each of these patients already had consistent periods of extended foveation (x = 107 ms; n = 5) without biofeedback.
Therefore, it is not surprising that the improved fixa-
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Investigative Ophthalmology & Visual Science, January 1993, Vol. 34, No. 1
tional ability with biofeedback had only a relatively
small positive impact on steady-state accommodative
accuracy, because the biofeedback did not necessarily
enable them to attain an average slow-phase velocity of
less than 10°/sec most of the time.
We speculate that the degradation effects of eye
movements during the early development of the visual
system must have imposed critical limitations on its
sensory development. This is evident from our data
that show a significantly increased depth-of-focus for
the group of patients with nystagmus. Furthermore,
the increased depth-of-focus also may explain the atypical response profiles of the patients with nystagmus.
Because the accommodative system under monocular
viewing conditions responds primarily to defocus
blur,1 an increased depth-of-focus would mean that an
object can be moved within a greater range of distances before it is perceived as out-of-focus, and therefore be capable of driving the accommodative system.
Within the depth-of-focus range, the system essentially
is in the open-loop mode and receives no feedback
regarding its response accuracy.4243 Thus, the patients
with nystagmus could respond in either direction—ie,
exhibit considerable over-accommodation or underaccommodation relative to that of normal subjects
without inducing a perceptible change in the quality of
the retinal image. This has been suggested in normal
subjects,14 wherein accommodation was less accurate
and responded in either direction to sub-optimal blur
stimuli consisting of low spatial frequency sinusoids.
In other words, the accommodative system responded
in an even-error manner,44 considering only blur magnitude and not direction. The direction of the static
error then may be regarded as somewhat inconsequential, because it would not adversely affect retinalimage quality in any perceptually unique manner.
The rationale behind the patients with nystagmus
assuming a particular directional accommodative response is only speculative at this point. Under-accommodation relative to the normal subjects is expected
and is more consistent with typical findings from investigations in patients who manifest various ocular
abnormalities (eg, amblyopia), because nonoptimal visual systems generally demonstrate reduced accommodative function.22 Over-accommodation, on the
other hand, may reflect an unconscious effort by the
patient with nystagmus under everyday binocular conditions to try to "see better," which then is carried into
the monocular experimental paradigm to induce more
(perhaps voluntary convergence-accommodation) accommodation. The latter would lead to increased convergence that might dampen the nystagmus.815 This
also may explain why accommodative responses increased in magnitude at the two tested dioptric levels
when the subjects were instructed to adopt the strategy they learned during previous auditory biofeedback
training sessions. Alternatively, and perhaps more
likely, the patients with nystagmus may find the target
difficult to accommodate upon because of their increased retinal-image motion; therefore, they may exert more attention and effort to focus accurately, the
result being blur-induced accommodative overdrive.
The absence of a significant correlation between
most accommodation and eye movement parameters
may be due to the complexity of the dynamic interactions of the eye movement parameters. As a result,
demonstrating the isolated effects of any single component may be difficult, although it has been suggested
that waveform, and thus foveation duration, may indicate a person's visual capability, with pendular waveforms exhibiting the smallest percent foveation time
per cycle.45 The present results revealed a significant
correlation between ACG and foveation duration,
which is consistent with the above idea. In addition,
the two patients with nystagmus who exhibited pendular waveforms in the present study were classified as
belonging to the subgroup characterized by their
slopes being significantly less than normal limits.
Our findings suggest that the abnormal underlying neurology is responsible for the anomalous accommodative behavior in congenital nystagmus. The latter
could be attributed to the abnormal visual experience
resulting from the onset of nystagmus very early in life.
The presence of these abnormal eye movements, especially at critical stages of development, perhaps coupled with the high uncorrected astigmatism exhibited
by most patients with nystagmus, have been suggested
to produce neural deficits.4546 Eye movements result
in increased retinal-image motion. This, as an isolated
entity, reduces the quality of the retinal image. Because of the degraded retinal image, the developing
and immature visual neurologic system does not have
the opportunity to "fine-tune" and develop maximally, resulting in its impaired sensory development.
The findings of increased depth-of-focus in the present subjects and poorer contrast sensitivity for patterns lying orthogonal to the primary direction of
oscillation47-48 support this notion.
It is conceivable that accommodative function also
would be impaired after such abnormal rearing conditions. Apparently, the normal development of the visual system of a patient with nystagmus is disrupted at
this early stage and remains somewhat immature
throughout life. However, the degree of such disruption in albinos, with their congenitally maldeveloped
fovea and already poor neurosensory system, is predicted to be less. Therefore, even if the nystagmoid eye
movements were now controlled and reduced to
within normal limits, the accommodative function of
patients with nystagmus, although it may improve
slightly,17 would not necessarily normalize, because accommodative accuracy will not be any better than that
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Static Accommodation in Congenital Nystagmus
203
delimited by the underlying suboptimally developed
neurologic substrate.
Key Words
16.
accommodation, eye movements, depth-of-focus, nystagmus, retinal-image motion.
A cknowledgments
17.
We thank Drs. R. Cole and S. G. Goldrich for their assistance in providing us with some of the subjects and their
related clinical records.
18.
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