(Investigative Ophthalmology and Visual Science. 2001;42:1495-1498.)
© 2001
by The Association for Research in Vision and Ophthalmology, Inc.
Spatial Localization after Different Types of Retinal Detachment Surgery
Clifford R. Weir1,
Marie Cleary2,3,
Stuart Parks1,
Tom Barrie1,
Harold M. Hammer1 and
John Murdoch1
1 From the Tennent Institute of Ophthalmology and the
2 Department of Orthoptics, Gartnavel General Hospital, Glasgow, Scotland, United Kingdom; and the
3 Department of Vision Sciences, Glasgow Caledonian University, Scotland, United Kingdom.
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Abstract
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PURPOSE. To compare the effect on spatial localization of two different forms of
surgery for primary rhegmatogenous retinal detachment.
METHODS. Two groups of 30 patients (one group undergoing conventional external
scleral-buckling procedures, the other undergoing vitrectomy
procedures) were recruited. They pointed at targets appearing on a
computer touchscreen without being able to see their hands, while
viewing targets with the non–surgically treated eye. The sizes of the
horizontal pointing errors were recorded on three separate occasions:
before surgery, on the first postoperative day, and approximately 10
days later.
RESULTS. On the first postoperative day a significant change in localization of
2.9 ± 0.9° [SD]) was observed in the scleral-buckling group,
compared with 1.3 ± 0.6° in the vitrectomy group. These changes
resolved by the second postoperative assessment.
CONCLUSIONS. These results, particularly in patients in the scleral-buckling group
in whom greater manipulation of the extraocular muscles inevitably
occurs, are consistent with an alteration in the extraretinal
eye position information that is used in spatial localization.
This is likely to be a consequence of modified efference copy
and/or extraocular muscle proprioception.
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Introduction
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The ability to locate the position of objects in the
surrounding visual world (spatial localization) is an important aspect
of normal visual function. For this to occur with precision the brain
must know the direction in which a person is looking, and it depends to
a large extent on visual (i.e., retinal) input for this information.
However, because the eyes are able to move within the orbits, retinal
information by itself is not adequate to specify this visual direction.
Further nonvisual (i.e., extraretinal) information regarding the
position of the eyes is required to interpret the retinal data and thus
determine the direction of gaze. It is believed that this extraretinal
eye position information is obtained from two distinct extraretinal
sources: monitoring of the motor command sent to the extraocular
muscles (efference copy or corollary discharge1
2
) and
extraocular muscle proprioception.3
However, the relative
contribution of each has been an issue of great controversy for many
years.4
5
6
The task of pointing at targets in surrounding space is an established
method for assessing spatial localization, particularly if subjects are
unable to see the pointing hand.7
8
9
10
11
Integration of the
retinal and extraretinal information from the sources outlined in the
prior paragraph enables the location of the object of interest to be
determined with accuracy. To reach out, or point to this object, an
appropriate motor command is sent to the arm and hand, which allows the
efficient performance of the task. Patients who undergo conventional
scleral-buckling surgery for retinal detachment have been shown to make
errors when asked to perform such tasks of spatial localization, while
viewing targets with the surgically treated eye.12
These
changes are attributed to alterations in extraocular muscle
proprioception, as a consequence of the perioperative manipulation of
the muscles.
However, the visual information available to these patients in the
immediate postoperative period (i.e., acuity and field of vision) must
also have altered. This is likely to contribute more to these errors
than the change in proprioception. A more interesting finding is the
postoperative localization shifts found in 4 of 10 of these patients
when they were tested while viewing with the fellow non–surgically
treated eye. It is reasonable to assume that under these circumstances,
modified extraocular muscle proprioception from the surgical eye
influences the central interpretation of gaze direction, particularly
because it is known that eye position information from both eyes is
used for this very purpose.7
11
13
If this were the case,
then patients who undergo retinal detachment surgery that does not
directly involve manipulating the extraocular muscles (i.e.,
vitrectomy) would not be expected to demonstrate any localization
changes after surgery when viewing with the fellow nonsurgical eye. To
test this hypothesis a comparison of the effect on spatial localization
of two different surgical procedures for primary rhegmatogenous retinal
detachment—conventional external scleral-buckling surgery and
vitrectomy—was made.
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Methods
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All procedures conformed to the Declaration of Helsinki for
research involving human subjects. Ethics committee approval was
obtained, and informed consent was given in all cases. This was a
comparative nonrandomized prospective study that was undertaken during
a 6-month period from April to October 2000, within the Vitreo-retinal
Service at the Tennent Institute of Ophthalmology, Gartnavel General
Hospital, Glasgow, Scotland, United Kingdom.
Protocol
The testing protocol was very similar to that described in a
previous study.11
Subjects were seated and viewed a
computer touchscreen (luminance 57 candelas
[cd]/m2; IBM, Greenock, UK) from a distance of
40 cm. Their heads were stabilized with chin rests and cheek pads.
Pictures of three vertical poles were presented on the screen: in the
center and 15° to the left and to the right of center (Fig. 1)
. A red target (a ball, 1.5 cm in diameter, luminance 45
cd/m2) appears on the top of one pole, and the
subject is asked to touch the screen at the bottom of the pole on which
the ball has landed, with the outstretched index finger of the dominant
hand. The ball then moves randomly to the top of another pole, and the
subject is asked to touch the location of this pole.
No limit of time was placed on the pointing response. The target was
presented on 10 separate occasions to each pole, and the location of
each pointing response was stored online for later analysis. The
disparity between the true location and the mean touched location of
the 10 presentations was taken as the horizontal pointing error for
that pole. A trial run was allowed in which the subjects could
initially visualize the pointing hand to enable them to become familiar
with the testing procedure. A cardboard sheet covered with black cloth
was then used to mask the lower part of the screen, thereby preventing
the pointing hand’s being seen. The subjects were allowed to practice
with this in place before the formal testing session began. Each
subject was tested before surgery (either the day before or the day of
surgery) and again on the first postoperative day. A further test was
performed on the first follow-up clinic visit, approximately 10 days
later. All subjects were tested with appropriate refractive correction,
while viewing monocularly with the nonsurgical eye, with the surgical
eye patched during this time. The differences between the mean pointing
errors recorded before surgery, on the first postoperative day and at
the subsequent follow-up visit were then calculated for individual
subjects for each pole. Statistical analysis was performed by computer
(Prism software; GraphPad, San Diego, CA).
Subjects
Sixty patients who underwent surgery for primary rhegmatogenous
retinal detachment participated in the study and were divided into two
groups of 30 as follows: group 1: those who underwent primary external
scleral-buckling surgery (mean age 48 ± 17 [SD] years; range,
19–83 years); group 2: those who underwent primary vitrectomy (mean
age, 55 ± 15 years; range, 23–73 years). Their clinical details
are summarized in Table 1
. The choice of surgical procedure to be performed was decided
by one of the vitreoretinal surgeons (HMH, TB, or JM) and was dependent
on the requirements of individual patients.
The number of subjects necessary to detect a difference between the two
groups with a power of 90% at the 5% significance level was
determined using a power calculation.14
The SD required
for this calculation was derived from a pilot study. None of the
subjects had any ophthalmic history of note and no medical history that
could have affected their ocular motility or pointing responses. Visual
acuities were recorded with appropriate refractive correction using the
log minimum angle of resolution (MAR) crowded test at a distance
of 3 m.15
Surgical Procedure
All surgery was performed with patients under general
anesthesia. The conventional external scleral-buckling procedures
consisted of drainage of subretinal fluid and application of
cryotherapy in the region of the retinal break(s), to create an
adhesion between the sensory retina and the underlying retinal pigment
epithelium. Silicone explants were placed overlaying the retinal
break(s) and oriented either circumferentially (n = 25)
or radially (n = 5). An encircling band was also used
when appropriate (n = 12). Intravitreal gas was used to
effect temporary internal tamponade as required. All four of the rectus
muscles were slung to aid movement of the eye. The vitrectomy
procedures consisted of a standard three-port pars plana approach, with
internal drainage of subretinal fluid, followed by fluid–gas exchange.
External cryotherapy was applied in the region of the retinal hole(s).
No muscle slings or external buckles were used in the vitrectomy group.
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Results
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All subjects were able to perform the test without difficulty on
each occasion. Normality testing confirmed a gaussian distribution of
the data allowing parametric statistical tests to be performed. The
macula was detached in 16 patients and attached in 14 in the
scleral-buckling group and was detached in 23 patients and attached in
7 in the vitrectomy group. Before surgery, the visual acuity of the
surgical eyes ranged from 0.025 log units to hand movements in the
scleral-buckling group and from 0.15 log units to perception of light
in the vitrectomy group. The mean visual acuity of the fellow
nonsurgical eyes was 0.02 ± 0.09 (SD) log units in the
scleral-buckling group and 0.04 ± 0.11 log units in the
vitrectomy group. The mean visual acuity of the nonsurgical eye did not
change in the postoperative period. The mean length of time between the
first and second postoperative assessments was 10.3 ± 1.9 (SD)
days in the scleral-buckling group and 9.8 ± 2.1 days in the
vitrectomy group.
Analysis of variance showed that the pointing responses for individual
subjects to each of the three poles were similar during each testing
session (F = 0.55, P = 0.74). In view of this, the
data were collapsed to obtain a single value of the mean pointing
response for each patient for that particular testing session. In the
scleral-buckling group there was a significant shift in spatial
localization of 2.9 ± 0.9° (SD; 95% confidence interval
2.4–3.2°) on the first postoperative day (Fig. 2)
. This was statistically significant (P < 0.0001,
t = 17.9; one-sample t-test). In the
vitrectomy group there was also a significant shift in spatial
localization of 1.3 ± 0.6°; 95% confidence interval
1.1–1.5°) on the first postoperative day (P <
0.0001, t = 12.3; Fig. 2
). A comparison of the changes
in localization observed in each of these two groups at this time
showed that they were significantly different from each other
(P < 0.0001, t = 8.55; unpaired
t-test). At the subsequent follow-up assessment 10 days
later, these changes had returned toward preoperative values in both
groups of patients (Fig. 2)
. For example, there was a small,
nonsignificant difference between the preoperative and second
postoperative testing sessions of 0.5 ± 0.7° (P = 0.25, t = 1.2) in the scleral-buckling group and
0.4 ± 0.6° (P = 0.35, t = 0.95)
in the vitrectomy group. There was no significant difference between
the changes observed in each group (P = 0.14,
t = 1.4). No correlation was found between the age or
refractive errors of the patients and the size of localization shifts.
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Figure 2. Comparison of changes in localization between the preoperative and
first postoperative testing sessions (filled
bars) and between the preoperative and second postoperative
testing sessions (open bars) for both patient groups.
Error bars, SD.
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Discussion
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This study demonstrates that spatial localization in patients with
primary rhegmatogenous retinal detachment alters significantly more
after external scleral-buckling procedures compared with vitrectomy
procedures, when viewing with the nonsurgical eye. The technique we
used is a recognized method for assessing
localization.7
8
9
10
11
Although a randomized study would have
been optimal, it was not feasible, because the decision about the type
of surgery to be performed was determined by the clinical status of
each patient.
The results from the scleral-buckling group are consistent with those
previously reported by Campos et al.,12
not only in the
size of the localization shifts, but also in the time taken for the
observed changes to return to their preoperative values, approximately
10 days later. However, they noted alterations in only 4 of 10 patients
when testing the fellow non–surgically treated eye. In contrast, we
noted changes in all subjects who underwent scleral-buckling surgery,
ranging from 1.3° to 4.6°. It is possible that this difference is
related to the more sensitive technique we used, in which pointing
responses were recorded on a computer touchscreen, rather than the
method Campos et al.12
describe, in which the position of
the target was indicated on a piece of paper. The pointing changes we
found in this group are of a similar magnitude to those in previous
studies in which extraocular muscle proprioception was manipulated
experimentally, resulting in mean localization shifts of
2.5°16
and 2.98°.17
They are also in
keeping with the findings of Steinbach and Smith8
who
observed changes after strabismus surgery, results that were attributed
to modified afferent feedback from the extraocular muscles of the
surgically treated eye.
To the best of our knowledge alterations in spatial localization after
vitrectomy procedures for retinal detachments have not been reported
previously. Why should these changes occur after a procedure that does
not appear to involve the extraocular muscles directly? As was
discussed in the introduction the viewer relies on a combination of
both retinal (visual) and extraretinal information to determine the
location of targets with respect to himself or herself. Because all the
patients were tested with the surgical eye patched, and because the
visual acuity of the nonsurgical eye remained the same after surgery,
then an alteration in retinal information is unlikely to account for
the results. This indicates that a nonvisual (i.e., extraretinal)
signal has influenced spatial localization in the fellow eye. As was
outlined earlier, there are two possible sources of this extraretinal
information: efference copy and extraocular muscle proprioception.
Could the efferent copy of the oculomotor command change after
vitrectomy? This is possible, particularly because ocular motility
problems have been reported after this procedure.18
However, it should be noted that these changes were recorded several
months after surgery, and little is known about ocular motility in the
immediate postoperative period. In addition, our testing was performed
monocularly, when viewing with the normal fellow eye, and according to
Walls,19
the visual system monitors only the efference
command sent to the dominant eye. Bridgeman4
also supports
the concept that there is only one copy of the efferent command.
Because there is no reason to believe that the motility of the
nonsurgical eye has changed, we cannot be sure whether efference copy
influenced the extraretinal eye position signal under the circumstances
of our testing procedure.
The other possible source of the modified extraretinal information is
extraocular muscle proprioception. Although no muscle slings or scleral
buckles were used during the vitrectomy procedures, a degree of
manipulation and rotation of the globe during surgery is inevitable.
This may have produced swelling and inflammation in the periorbital
tissues in proximity to the extraocular muscles, which in turn could
have caused an alteration in proprioceptive feedback. It is also
conceivable that periorbital, rather than extraocular, muscle receptors
may be the source of this modified afferent signal.20
However, there is little direct evidence to support the existence of
such receptors.
Although we cannot discount the role of efference copy after
vitrectomy, the balance of evidence suggests that the changes in
spatial localization we observed are related to an alteration in a
nonvisual feedback signal derived from the surgical eye. The most
likely source of such a signal is extraocular muscle sensory receptors.
Although the prime concern in patients who undergo any form of retinal
detachment surgery is successful reattachment of the retina with
improved visual function, in our experience some patients report
difficulty in judging the position of objects relative to themselves.
Although this is likely to be related to reduced acuity in the affected
eye, combined with postoperative inflammation and mydriasis, our
findings suggest that particularly after scleral-buckling procedures,
modified extraocular muscle proprioception could be a contributory
factor immediately after surgery. What effect these and other surgical
procedures involving the extraocular muscles, have on other aspects of
visual function, such as oculomotor control, is not known, but perhaps
warrants further assessment.
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Footnotes
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Supported by The Keeler Scholarship (Royal College of Ophthalmologists) and The W. H. Ross Foundation, Scotland.
Submitted for publication November 28, 2000; revised February 15, 2001; accepted February 23, 2001.
Commercial relationships policy: N.
The publication costs of this article were defrayed in part by page charge payment. This article must therefore be marked "advertisement" in accordance with 18 U.S.C. 
1734 solely to indicate this fact.
Corresponding author: Clifford R. Weir, Tennent Institute of Ophthalmology, Gartnavel General Hospital, 1053 Great Western Road, Glasgow G12 0YN, Scotland, UK. cliff{at}weir88.freeserve.co.uk
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Abstract
Introduction
