Abstract
purpose. Accommodative effort during nearwork is thought to be a causative
factor in the development of myopia. It has been proposed that an
anomaly in autonomic control may be a precursor to the development of
myopia. In the present study the closed-loop accommodation response
after variations in fixation period was investigated in emmetropes,
early-onset myopes and late-onset myopes to determine characteristics
of reflex accommodation for each refractive group.
methods. Closed-loop accommodation responses were measured in a group of
emmetropes (n = 7), early-onset myopes
(n = 7), and late-onset myopes (n = 7)
by use of a dynamic tracking infrared optometer. A variation in
fixation period (10 seconds, 60 seconds, and 180 seconds) before an
accommodative step was used to stimulate the accommodation control
mechanism differentially.
results. Group results of accommodative response times showed that late-onset
myopes were significantly affected by the duration of fixation before
the change in stimulus vergence. Accommodative response times after 3
minutes of sustained near vision were significantly longer than those
observed for other groups for the near-to-far condition. Reaction time
appears to be independent of refractive grouping, prior fixation
period, and direction of step change.
conclusions. Late-onset myopes showed significantly extended accommodation response
times after a sustained near vision task that was demonstrable under
well-controlled experimental conditions. The extended response times
observed in the present study were consistent with previous reports of
refractive shifts in late-onset myopes and early-onset myopes and
provide a corollary between reflex and adaptive components of the
accommodation response. Potential mechanisms are discussed in an
attempt to explain the resultant hysteresis under closed-loop viewing
conditions.
The association between sustained nearwork requiring high levels
of ocular accommodation and the development of myopia has been well
documented.
1 2 Epidemiologic studies have also shown a
correlation between the amount of nearwork and the onset and subsequent
progression of myopia.
3 4 As a result of these
observations, the increased accommodative effort required during
nearwork has been proposed as a causative factor in the development of
myopia. However, the relationship between accommodative demand and
myopia is complex, because there is invariably a link between the
hereditary basis of myopia and environmental factors. Both
genetic
5 and environmental considerations
6 may therefore influence the development of myopia, although the
relative significance of each of these determinants remains uncertain.
Animal
7 and human
8 studies indicate that
myopia is caused by an increase in the axial component of the eye that
is not neutralized by a concomitant change in corneal curvature. It has
been suggested that corneal curvature and refractive error development
are not related, because the cornea reaches adult curvature by the age
of 3 years.
9 However, the exact nature of the structural
changes that occur in the posterior segment of a myopic eye remains a
matter of conjecture, with a number of models proposed.
10
The development of myopia in the older eye generally has no clear
hereditary basis
1 and provides an opportunity to identify
the interaction between ocular accommodation and its environment,
because the onset of myopia is usually associated with increased
occupational demands. Although there is no consensus regarding the
basis for development of myopia, there is increasing awareness that
prolonged and frequent close work is associated with the type of myopia
that emerges relatively late in life (>15 years).
1 11 This type of refractive error is classified as late-onset myopia
(LOM),
12 which is generally assumed to be environmental in
origin rather than caused by hereditary influences.
1 If
performing sustained nearwork is a significant factor in the
development of myopia, it should be possible to demonstrate variations
in the characteristics of the accommodative response for different
refractive groups.
In the absence of visual cues the accommodation mechanism adopts
an open-loop resting position that is known as tonic accommodation
(TA). Several studies have used measures of TA to differentiate between
refractive groups, because the open-loop accommodative level may
indicate differences in the neurologic input to the ciliary
muscle.
13 14 It has been shown that LOMs have a more
distant TA than early-onset myopes (EOMs), emmetropes (EMMs), or
hyperopes (HYPs).
13 The speed of accommodation regression
back to a person’s TA subsequent to opening the accommodation loop has
also been investigated.
15 The time course of regression
has been used to specify the magnitude of accommodative adaptation or“
hysteresis” induced by a particular closed-loop
task.
11 These measures of post-task open-loop adaptation
have been used to provide an insight into the characteristics of
ciliary muscle innervation for the closed-loop accommodative
response.
11 13 14 15
Variations in the accommodation response have also been reported
between refractive groups under static closed-loop conditions. For
example, myopic children have been shown to accommodate significantly
less to real targets than emmetropic children.
16 Measurement of stimulus–response curves in university students showed
that LOMs have a shallower stimulus–response gradient than EOMs, EMMs,
and HYPs.
12 Significant differences among refractive
groups have also been found in measures of amplitude of accommodation,
with LOMs having the largest amplitude followed by EOMs, EMMs, and
HYPs.
17
Recent work has shown LOMs and EOMs to be significantly more
susceptible to nearwork-induced transient myopia (0.36 D and 0.34 D,
respectively) after a 10-minute period of sustained near vision than
EMMs (0.09 D) or HYPs (0.01 D).
18 This nearwork-induced
transient myopia was found to have a much slower decay back to the
baseline distance refractive error in LOMs compared with EOMs (time
constant: LOMs, 63 seconds; EOMs, 35 seconds). It is clear that myopes
show increased adaptation under closed-loop conditions. However, the
method used did not allow measurement of accommodation during the
initial reflex blur-induced phase of the response.
18
Few studies have been published on the characteristics of reflex
closed-loop accommodation dynamics as a function of refractive
group.
19 20 21 22 The results of these studies do not provide a
consensus about refractive group–dependent effects on reflex dynamic
accommodation.
A refraction-dependent trend was reported for accommodative reaction
times with HYPs (431 msec) demonstrating the longest time followed by
MYPs (393 msec), and EMMs (327 msec).
19 Accommodative
velocity was also found to be faster for EMMs (5.69 D/t) than
either MYPs (2.84 D/t) or HYPs (1.47 D/t).
19 Conversely,
it has been reported that accommodative reaction time is significantly
increased in MYPs relative to HYPs and that the speed of the
accommodative response is slower in MYPs in a sample of 128 students
aged between 10 and 19 years.
20 Continuous ultrasonic
biometry in 12 EMMs and 12 MYPs demonstrated that the response time for
negative accommodation was faster than for positive accommodation in
both EMMs and MYPs.
21 In addition, the response times for
MYPs were faster than for EMMs for 2-D and 4-D stimulus steps, but
slower for a 6-D stimulus step. In contrast, Schaeffel et
al.
22 found no relation between accommodative peak
velocity and refractive state in a sample of 19 subjects. The
apparently contradictory findings may be caused in part by
inappropriate classification of myopia (studies have tended to classify
myopia as a single group irrespective of the age of onset or the state
of progression
23 ) and differences in method among the
studies.
To demonstrate differences in reflex closed-loop accommodation, it is
necessary to consider carefully the characteristics of the control
system to allow suitable viewing conditions to be used. In the young
accommodating eye the parasympathetic and sympathetic components of the
autonomic nervous system provide the central and peripheral control
processes that ensure the accuracy of the accommodation
response.
2 Control of accommodation is mediated primarily
by parasympathetic input to ciliary smooth muscle.
24 However, evidence exists supporting sympathetic innervation of ciliary
muscle.
25 26 27 28 It has been proposed that a precursor to the
development of myopia may be an anomaly in the autonomic control of
near vision.
29
Although several studies have identified differences in the
characteristics of accommodation between refractive groups under
open-loop conditions, there is no evidence to indicate that differences
in reflex accommodation performance are observed under solely
closed-loop dynamic conditions. Investigation of the temporal
closed-loop accommodation response offers the opportunity to determine
the characteristics of reflex accommodation for different refractive
groups in the presence of variable external loads.
The purpose of this study was to investigate the characteristics of
reflex closed-loop accommodation after variations in prior fixation
period for EMMs, EOMs, and LOMs.
Reaction and response times of the EMMs and EOMs in the present
study, under monocular viewing conditions, are consistent with previous
reports of accommodation dynamics in adults.
33 34 The
reaction time is approximately 250 msec and appears to be independent
of step direction and prior fixation period. Step changes in stimulus
vergence for all refractive groups after fixation periods less than 1
minute produced a completed accommodation response in approximately 1
second, which is likely to be mediated by the fast-acting
parasympathetic branch of the autonomic mechanism.
Accommodation responses for LOMs were found to be significantly
affected by the duration of fixation before the change in stimulus
vergence. Responses after 10 seconds of fixation before the stimulus
step were in the normal range of values and similar to those observed
in EMMs and EOMs. However, the accommodative responses after the
3-minute task were significantly longer than those observed in the
other refractive groups for the near-to-far condition, indicating an
adaptive component to the response.
The initial reflex accommodation response is driven by blur-induced
changes that occur with step shifts in stimulus vergence. The
accommodation control mechanism then acts to optimize retinal image
contrast. Under closed-loop conditions this reflex action limits the
potential for accommodative adaptation to a zone within the ocular
depth-of-focus,
35 and any adaptation effect is therefore
likely to be small in magnitude. In addition, the duration of post-task
adaptation is short under closed-loop viewing until the necessity for
feedback is removed. When the accommodation response falls within the
envelope of the depth-of-focus, it may then be possible to identify the
adaptive shift in the response.
18
Under open-loop conditions there have been reports
13 36 indicating a significant magnitude of adaptation in LOMs after
sustained near tasks, because the response is not constrained by
retinotopic factors. However, natural viewing is a closed-loop
activity, and it is therefore necessary to consider the potential for
variation in control of accommodation for different refractive groups
under habitual viewing conditions.
Recent evidence suggests that closed-loop post-task adaptation after
sustained near vision results in a small but significant shift in
distance refractive error in both LOMs and EOMs, although different
time constants between the groups were observed.
18 The
post-task adaptation reported is within the normal ocular
depth-of-focus
35 and represents a shift in the baseline
distance refractive error after a rapid initial reflex accommodation
response that acts to minimize retinal blur. The method and
instrumentation used did not allow initial response times to be
determined, because the sampling period was too long to record this
aspect of accommodation. The small but significant refractive shift
reported for LOMs and EOMs under closed-loop conditions is consistent
with the extended response times observed in the present study,
providing a corollary between the reflex and adaptive components of the
accommodative response.
Previous studies have been equivocal on the relationship between
response dynamics and refractive error.
19 20 21 22 This may be
in part because of inappropriate classification of refractive error but
is likely to be confounded by the use of inappropriate or inconsistent
fixation periods before the step in stimulus
vergence.
19 20 21 22 A recent study
23 suggested
that anomalies of accommodation associated with myopia may be analyzed
more effectively by classifying myopia in terms of progression rather
than in relation to age of onset. The LOMs in the present study were
all progressing myopes, which may have facilitated a positive result.
We have demonstrated that a relationship between response times and
refractive error exists but is only evident under well-controlled
experimental conditions. It is not clear whether the differences
observed in reflex closed-loop responses represent a primary anomaly or
merely occur as an indirect consequence of differences in accommodative
gain. When TA is modeled by slow, leaky integrators, the reduced gain
observed in myopes tends to lead to an increase in TA.
37 Open-loop hysteresis therefore represents a symptom of accommodation
inaccuracy. The extended response times reported in the present study
under reflex closed-loop conditions may represent an additional symptom
of accommodative inaccuracy in LOMs.
Correction of LOMs with lenses requires subjects to exercise a greater
accommodative effort for near vision compared with the uncorrected
state. Furthermore, the lag of accommodation at near is known to be
greater in LOMs,
12 23 resulting in retinal defocus, which
may be a myogenic factor. The process of active emmetropization has
been shown to detect and compensate for focusing errors, but
intervention may disrupt this mechanism.
38 The hysteresis
that may occur with increased parasympathetic activity, in the absence
of adequate inhibitory sympathetic activity and the effects of retinal
defocus, may induce an additional increase in the level of manifest
myopia. Recent mathematical modeling supports the development of myopia
over a period when related to sustained nearwork.
39
Post-task hysteresis has been reported previously
11 to be
greater in LOM and is confirmed by the results of the present study.
Sustained near vision requiring high levels of parasympathetic input
should stimulate the inhibitory sympathetic mechanism
29 and prevent accommodative adaptation. It has been suggested that a
deficit in inhibitory sympathetic innervation may be a factor that
predisposes subjects to accommodative adaptation and may act as a
precursor to the development of myopia. It is interesting to speculate
that subjects in the LOM group may not have this inhibitory input and
may therefore demonstrate adaptation under both open- and closed-loop
stimulus conditions.
The relationship between post-task hysteresis and the development of
myopia is unknown, but the mechanism has to be related to the increase
in vitreous chamber depth, because this component is the principal
determinant of myopia. Previous evidence has been presented showing an
increase in vitreous chamber pressure during accommodation in monkeys
and humans.
40 The increase in intraocular pressure has
been suggested to cause the increase in vitreous chamber depth and thus
in axial myopia.
41 The extended duration of
parasympathetic tone subsequent to prolonged nearwork, observed in the
LOMs,
36 and the chronic accommodative hysteresis caused by
slower response times may support this mechanism of axial elongation.
In a study in kittens
42 it has been demonstrated that
small chronic amounts of accommodation can cause axial elongation.
It is clear that further investigations are required before any
unambiguous conclusions can be drawn on potential precursors to and the
mechanism of myopic development. Longitudinal studies on accommodation
dynamics and adaptation combined with biometric data may provide
further insight into the long-term consequences of sustained visual
tasks. There is also a need to obtain a better understanding of the
precise function and action of autonomic innervation in ocular
accommodation, which may be achieved using pharmacological methods.
Reprint requests: Helena M. Culhane, Department of Optometry, University of Bradford, Richmond Road, Bradford, West Yorkshire, BD7 1DP UK.
Submitted for publication October 20, 1998; revised February 23, 1999;
accepted March 25, 1999.
Proprietary interest category: NNE.
Table 1. Demographic and Clinical Data
Table 1. Demographic and Clinical Data
Group | Mean Age (y) | Mean Spherical Equivalent Refraction (D) | Gender |
EMM | 23.00 ± 2.65 | +0.10 ± 0.33 | 1 Man, 6 women |
EOM | 22.43 ± 2.30 | −4.50 ± 1.83 | 2 Men, 5 women |
LOM | 23.57 ± 1.90 | −2.02 ± 0.96 | 4 Men, 3 women |
Table 2. Reaction Times for Each Refractive Group after Three Prior Fixation
Periods
Table 2. Reaction Times for Each Refractive Group after Three Prior Fixation
Periods
Step Modulation | EMM | | | EOM | | | LOM | | |
| 10 sec | 60 sec | 180 sec | 10 sec | 60 sec | 180 sec | 10 sec | 60 sec | 180 sec |
2–4D | 0.25 ± 0.05 | 0.25 ± 0.02 | 0.25 ± 0.06 | 0.31 ± 0.03 | 0.24 ± 0.01 | 0.31 ± 0.14 | 0.18 ± 0.07 | 0.26 ± 0.11 | 0.32 ± 0.08 |
4–2D | 0.22 ± 0.07 | 0.21 ± 0.06 | 0.20 ± 0.05 | 0.29 ± 0.09 | 0.22 ± 0.08 | 0.24 ± 0.02 | 0.21 ± 0.09 | 0.25 ± 0.09 | 0.19 ± 0.06 |
Table 3. Response Times for Each Refractive Group as a Function of Prior
Fixation Period
Table 3. Response Times for Each Refractive Group as a Function of Prior
Fixation Period
Step Modulation | EMM | | | EOM | | | LOM | | |
| 10 sec | 60 sec | 180 sec | 10 sec | 60 sec | 180 sec | 10 sec | 60 sec | 180 sec |
2–4D | 0.76 ± 0.18 | 1.00 ± 0.17 | 1.12 ± 0.39 | 0.95 ± 0.18 | 1.35 ± 0.14 | 1.28 ± 0.18 | 1.28 ± 0.10 | 1.28 ± 0.35 | 1.29 ± 0.39 |
4–2D | 0.76 ± 0.16 | 1.10 ± 0.47 | 1.18 ± 0.37 | 0.93 ± 0.22 | 1.09 ± 0.38 | 1.19 ± 0.35 | 0.88 ± 0.20 | 1.34 ± 0.50 | 2.12 ± 0.28 |
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