Current Biology 23, 1663–1669, September 9, 2013 ª2013 Elsevier Ltd All rights reserved
056
Rapid and Persistent Adaptability
of Human Oculomotor Control in Response
to Simulated Central Vision Loss
MiYoung Kwon,1,4,* Anirvan S. Nandy,3,* and Bosco S. Tjan1,2
1Department of Psychology
2Neuroscience Graduate Program
University of Southern California, Los Angeles, CA 90089, USA
3Systems and Computational Neurobiology Laboratories, the
Salk Institute for Biological Studies, La Jolla, CA 92037, USA
4Schepens Eye Research Institute, Department of
Ophthalmology, Harvard Medical School, Boston,
MA 02114, USA
Summary
The central region of the human retina, the fovea, provides
high-acuity vision. The oculomotor system continually
brings targets of interest into the fovea via ballistic eye move-
ments (saccades). Thus, the fovea serves both as the locus
for fixations and as the oculomotor reference for saccades.
This highly automated process of foveation is functionally
critical to vision and is observed from infancy [1, 2]. How
would the oculomotor system adjust to a loss of foveal vision
(central scotoma)? Clinical observations of patients with
central vision loss [3, 4] suggest a lengthy adjustment period
[5], but the nature and dynamics of this adjustment remain
unclear. Here, we demonstrate that the oculomotor system
can spontaneously and rapidly adopt a peripheral locus for
fixation and can rereference saccades to this locus in nor-
mally sighted individuals whose central vision is blocked
by an artificial scotoma. Once developed, the fixation locus
is retained over weeks in the absence of the simulated sco-
toma. Our data reveal a basic guiding principle of the oculo-
motor system that prefers control simplicity over optimality.
We demonstrate the importance of a visible scotoma on the
speed of the adjustment and suggest a possible rehabilita-
tion regimen for patients with central vision loss.
We simulated a central scotoma in six normally sighted young
adults using a gaze-contingent display while the subjects per-
formed a demanding visual search task. The simulated sco-
toma appeared as a visible gray disc and blocked the screen
content at and around the center of gaze. A separate group
of six normally sighted subjects participated in a control
experiment in which they performed the identical task without
a simulated scotoma. The task alternated between two main
components (Figure 1A): (1) object following, in which subjects
maintained fixation on an object as it was randomly reposi-
tioned on the screen against either a uniform or cluttered back-
ground, and (2) visual search, in which subjects searched for
the target object shown in object following. Subjects were
instructed to perform the search task as quickly and accu-
rately as possible during the visual search phase. During the
initial period of the experiment, subjects were not told to use
a particular eccentric location to guide their eye movements
(free exploration).
*Correspondence: miyoungkwon02@gmail.com (M.K.), nandy@salk.edu
(A.S.N.)
http://dx.doi.org/10.1016/j.cub.2013.06.
Report
Rapid Development of Preferred Retinal Locus for Fixation
After having performed the experimental task with simulated
central scotoma for approximately 3 hr spread over 2 to
3 days (free exploration, Table S1 available online), all six sub-
jects in the experimental condition spontaneously followed the
jumping target with eccentric fixation, keeping it out of the
central scotoma (Figure S1).
Of the six subjects, five (two shown in Figure 2A) spontane-
ously formed a single preferred retinal locus (PRL) [6] for fixa-
tion near the border of the scotoma, whereas the sixth subject
developed two PRLs at roughly opposite sides of the scotoma
(S5 in Figure 2A). For the five single-PRL subjects, the variance
of the fixational PRL decreased rapidly during this free explo-
ration period (Figure 2B). The variance (defined as bivariate
contour ellipse area [BCEA]) measured at the end of this period
was significantly smaller than that at the beginning (54%
reduction, t(4) = 2.97, p < 0.05). Fixation stability continued to
improve with practice in the presence of the simulated
scotoma.
Rapid Development of Rereferenced Saccades near
the Fixational PRL
More importantly, for the five subjects with a single PRL, their
first saccade after each target movement placed the target at
or near their fixational PRL (Figures 3A and S2) and away from
the fovea, demonstrating a shift in oculomotor reference from
the fovea to the PRL. Similar to that of the fixational PRL, the
variance of the first saccade landing site (i.e., target location
on the retina after the first saccade following each target
movement) decreased rapidly (Figure 3B). The variance
(BCEA) of the first saccade landing site during the last block
of free exploration was reduced by 28% in comparison to
that of the first block (t(4) = 5.02, p < 0.05). This noticeable
change in the first saccade landing site after about 3 hr of
exposure to the simulated central scotoma demonstrates a
remarkable adaptability of the oculomotor system.
The variance of the first saccade landing site was signifi-
cantly larger than that of the fixational PRL, even for the last
block of the free exploration (t(4) = 2.98, p < 0.05). Oculomotor
rereferencing may require a longer time to fully develop. The
slower time course of saccadic rereferencing has been
observed in adult monkeys with bilateral foveal lesions [7].
Thus, it appears that the refinement of the fixational PRL pre-
ceded the refinement of saccade rereference.
Refinement of the Fixational PRL and Saccadic
Rereference after Explicit Training
Despite the rapid emergence of both fixational PRL and
saccade rereference with simulated central scotoma during
the free exploration, we observed that the variances of both
remained higher than those of the foveal viewing control sub-
jects (fixational PRL: t(8) = 2.70, p < 0.05; saccade rereference:
t(8) = 2.69, p < 0.05). We asked whether it would be possible to
further reduce the variances with explicit training. We dis-
played a small white cross at the retinal location of each
subject’s emerged fixational PRL (Figure 1B) and instructed
subjects to follow the target with this gaze marker (explicit
training). Otherwise, subjects performed the identical task as
Current Biology Vol 23 No 17
1664
A B
Free exploration
(i) Object following
with a blank background
(ii) Centering of gaze
(iii) Visual search
(iv) Object following
TI
M
with a cluttered
E
background
ment except that the color and luminance of the simulated scotoma was matched to those of the background. As a result, the simulated central scotoma
was invisible to the subjects. Then, subjects searched for the target object among an array of distracters presented against a uniform gray background. (For
ease of visibility in the figure, target objects and the gaze reference cross were rendered at 2.53 the size used in the experiment relative to the rest of the
displayed elements).
before. With 15 to 25 hr of such explicit training (Table S1), all
six subjects were able to refine their oculomotor control such
that the variances of the PRL, and the first saccade landing site
became comparable to those of the control subjects (Figures
2B and 3B). Contrary to conventional wisdom [8], we found
that, using an effective training regimen, the oculomotor con-
trol with peripheral vision can be as precise and accurate as
that with foveal vision.
Retention of the Learned PRL in the Absence
of the Simulated Scotoma
To investigate whether the learned fixational PRL and saccade
rereference could be retained over an extended period of time
without practice, subjects were recalled for a retention assess-
ment (retention, Table S1) at least 1 week (up to 1 month) after
completion of the explicit training. Subjects performed the
same task (visual search and object following in clutter) as
they did during the free exploration period of the experiment
without any gaze marker. Furthermore, to assess the robust-
ness of the adaptation, we also tested with an invisible
scotoma (in separate sessions, Figure 1C) during the object
following phase by matching the color and luminance of the
scotoma to those of the uniform gray background (invisible
scotoma, Table S1). All subjects retained the same PRLs,
even in the invisible central scotoma condition (Figures 2A
and 3A). However, the variances of both the fixational PRL
and first saccade landing site for the retention and invisible
scotoma conditions were larger in comparison to those
measured at the end of the explicit training period (p < 0.05,
both comparisons).
Changes in the Characteristics of Eye Movements during
PRL Development
The characteristics of eye movements covaried with the devel-
opment of PRL. We examined the time course of changes in
saccade latency, the number of saccades after each object
movement, and fixation duration during the object-following
component of the task. We found a significant decrease in
both saccade latency (42% reduction, Figure 4A) and the num-
ber of saccades (60% reduction, Figure 4B). The saccade la-
tency and number of saccades at the end of explicit training
became comparable to those of controls (saccade latency:
Figure 1. Task and Experiment Conditions
Explicit training (A) Task sequence during the free exploration
period. This sequence is an example of one trial.
+ There were 30 trials per block. Each trial was
comprised of four phases: object following
against a gray background (i), centering of gaze
(ii), searching for the target object presented in
the object following phase with an array of
C nontarget distracters (iii), and object following
Invisible scotoma
(i) Object following amidst a cluttered background (iv).
(B) An example of object following during the
(ii) Visual search
explicit training period. A small white cross
(w0.7 in height) appeared at each subject’s esti-
mated PRL. Subjects were instructed to use the
cross as a gaze reference point for fixation and
saccadic eye movements.
(C) Task sequence of the invisible scotoma
experiment. The first phase was identical to the
first object following phase of the main experi-
t(8) = 1.36, p = 0.21; number of saccades: t(8) = 1.30, p = 0.23).
Although there were no significant changes in fixation dura-
tion, there was a slight upward trend during the course of the
experiment (Figure 4C). The rate of change in both saccade la-
tency and the number of saccades mirrored those of the
refinement of the fixational PRL and the saccadic rereference:
a rapid decrease during the free exploration followed by a
persistent decrease during explicit training to levels that
were comparable to controls.
Changes in Visual Search Performance during PRL
Development
Performance during the visual search component of the task
also improved over the course of PRL development (Figure 5).
Search accuracy was high (w89% 6 2.1% SD, relative to the
chance level of 50%, Figure 5A) and remained unchanged
throughout the experiment. The average search time showed
a considerable decrease (42% reduction, Figure 5B) during
the free exploration period followed by a gradual decrease
during explicit training. A corresponding decrease was
observed in the number of saccades that was required to
find the target (60% reduction, Figure 5C). At the end of explicit
training, subjects were performing the search task as fast as
(t(8) = 20.94, p = 0.38) and with as few saccadic eye move-
ments as (t(8) = 1.30, p = 0.23) the foveal viewing controls.
Discussion
We found that a stable PRL spontaneously emerges within
hours of performing a visual task with a simulated central sco-
toma. Saccades were rereferenced to the PRL. The acquired
PRL was retained for at least 1 week, during which subjects
went about their daily lives with normal central vision. The
same PRL was used even when the simulated scotoma was
not visible. With explicit training using a gaze marker, the
fixation stability at the PRLs and the precision of the targeting
saccades became as good as those with normal foveal vision.
These findings imply a flexible and adaptive oculomotor
system. Akin to learning a motor skill such as riding a bicycle,
the system can rapidly develop a new motor plan even
with limited and sporadic exposure. Moreover, the motor plan
improves with use and is retained without continuous practice.
Rapid Adaptation of Saccades without Fovea
1665

A S2 S3 S5 B
15°
50

Variance (BCEA) of fixation (in deg2 )

10°
Average
5°
First block of 0°
40 Controls
free exploration

30

Last block of 20
free exploration
Retention
10

Explicit training 0
Invisible
Free Exploration Explicit Training Scotoma
-10
0 10 20 30 40 50 60 70 80 90
Block Number
Retention

Controls

Invisible scotoma
0.001 0.05 0.1
Probability Density

Figure 2. Development and Retention of Preferred Retinal Locus for Fixation

(A) Probability density maps of the retinal positions of a target object at fixation are shown for three of the six subjects. (Refer to Table S1 for the specific
number of blocks each subject performed in the different stages of the experiment.) From the top to bottom, the rows represent densities estimated from the
first and last blocks of the free exploration period, density estimated from the last block of the explicit training period, density estimated from all five to seven
blocks of the retention assessment, and density estimated from all five blocks when the scotoma was made invisible. The density of the fovea viewing
control experiment, averaged across all control subjects, is also shown. Data from the object following components with blank background and cluttered
background were combined. Each polar plot represents the visual field. The gray patch depicts the central scotoma. The red dot marks the location of peak
density, which we took as the estimated location of the fixational PRL. All six subjects exhibited a rapid and spontaneous emergence of fixational PRLs near
the border of the scotoma within 3 hr (eight to nine blocks). All subjects were able to further refine the precision of their fixational PRLs during a subsequent
explicit training period that lasted at least 15 hr (40 blocks). Not only was the PRL retained after being established, but the same PRL was also used when the
scotoma was made invisible.
(B) Variance of the fixational PRL as a function of block number. Variance was defined as the bivariate contour ellipse area (BCEA) that encompassed 68% of
fixations around the mean. The blue solid line indicates the average BCEA across all five subjects who spontaneously developed a single PRL (one subject,
shown here as S5, developed two PRLs); the shaded blue area indicates 61 SD of the BCEA, showing intersubject variability. The gray rectangular box rep-
resents the distribution of BCEA from the control subjects in the fovea viewing condition (61 SD). A gap of five blocks was inserted on the abscissa between
free exploration and explicit training to denote a break of 1 to 2 days from the experiment between these two stages. The BCEA of the fixation PRLs from the
five subjects with a single PRL decreased rapidly within a short period of time without explicit training. Explicit training reduced the BCEA to the range of
foveal fixation. It also eliminated one of the two PRLs of S5, as demonstrated in the retention test.

Our findings suggest that the oculomotor system prefers
developing a motor plan that is simple over one that may be
optimal with respect to saccade amplitude and accuracy.
With intact central vision, the fovea has the highest acuity
and, therefore, is a unique point in the visual field. The oculo-
motor system is presented with the simple goal of bringing
the high-resolution fovea to the target of interest. Losing
central vision eliminates this unique point. It is conceivable
that there exists a unique ‘‘best’’ point in the spared peripheral
retina for optimal form vision, and the location of this point may
be partly determined by oculomotor factors, such as fixational
drift, that contribute to spatiotemporal sensitivity [9, 10]. How-
ever, the difference in functional acuity between the best
peripheral point and the next best is likely to be small and
certainly smaller than the difference between normal fovea
and parafovea. Indeed, preliminary data from a recent study
showed that local acuity did not predict the location of PRL
in macular degeneration (MD) patients [11]. Hence, given a
target of interest, there are most likely multiple points (or
contours) on the peripheral retina that are equally adequate.
As such, the oculomotor system could choose a point that is
closest to the target in order to minimize saccade amplitude
and, thus, improve accuracy. Alternatively, it could choose
a point on the peripheral retina that avoids occluding the infor-
mative parts of the target with the scotoma (i.e., for reading
English text, placing the current word below the scotoma
could be advantageous). Despite these possibilities for an
on-demand variable fixation strategy that is perhaps more
efficient in terms of accuracy or information gain, the oculomo-
tor system opts for a strategy that is, from a control perspec-
tive, exceedingly simple: using a single point in the periphery
as the preferred locus for fixation. This amounts to adding a
constant vector offset to the existing oculomotor control
system.
Our observations are qualitatively different from what is
generally known as saccadic adaptation [12]. Saccadic adap-
tation is a continuous recalibration process that minimizes
the perceived saccade error; it is thought to be necessary for
adapting to an ever-changing oculomotor plan due to growth,
aging, and diseases. Saccadic adaptation, although rapid
in humans (in the order of a couple hundred saccades), is
magnitude and direction specific [13–15]. Establishing a PRL
Current Biology Vol 23 No 17
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A S2 S3 S5 B
15° 80
Average

first saccade landing site (in deg2 )

10°
5° 70
First block of 0° Controls
free exploration 60

Variance (BCEA) of
50

40
Last block of
free exploration 30 Retention

20

10
Explicit training
0 Invisible
Free Exploration Explicit Training Scotoma
-10
0 10 20 30 40 50 60 70 80 90
Block Number
Retention

Controls

Invisible scotoma
0.001 0.05 0.1
Probability Density

Figure 3. Development and Retention of Rereferenced Saccades Measured by the First Saccade Landing Site
(A) Probability density maps of the retinal position of a target object at the completion of the first saccade after target movement (same format as in
Figure 2A).
(B) Variance (BCEA) of the first saccade landing site as a function of block number (same format as in Figure 2B). The first saccade landing site after each
target movement was near the fixational PRL and distant from the fovea. Similar to the fixational PRL, the variance of the first saccade landing sites
decreased rapidly within a short period of time without explicit training, demonstrating a spontaneous shift in oculomotor reference from the fovea to
the PRL. With explicit training, the BCEA was further reduced to the normal range of intact foveal vision.

with saccadic adaptation would require one to adapt to a large,
if not infinite, number of magnitudes and directions. More
importantly, saccadic adaption affects the current state of
the oculomotor controller. It takes time to adapt and to recover
from adaptation. This contradicts the observations that (1) our
subjects’ normal foveation behavior was not affected by per-
forming the task with their PRL and that (2) subjects retained
their PRL between the daily experimental sessions and after
weeks of not performing the task. Hence, the development
of PRL that we observed is unlikely to be due to saccadic
adaptation.
Our results with simulated central scotoma echo some of the
clinical findings. A majority of MD patients with bilateral central
vision loss utilize a single PRL for viewing or fixating [16–18],
whereas some patients develop two or three task-dependent
PRLs [19]. A portion of these patients make saccades that
are rereferenced to their fixational PRLs [20]. Patients’ visual
performance is closely correlated with the establishment of a
stable PRL [17, 21, 22], further suggesting that variable fixation
is not an option used by the oculomotor system. However, un-
like MD patients, who apparently take months to develop PRLs
and rereference the oculomotor system to the PRLs [5], we
found that PRL development was rapid with a (visible) simu-
lated central scotoma. Our results are consistent with a report
of a similarly rapid development in the case of pursuit eye
movements with a sinusoidally moving target [23] and qualita-
tive accounts of the fast emergence of visual-field preference
for target identification [24, 25]. In contrast, although the natu-
ral development of PRLs may occur in some patients within
weeks of vision loss, saccade rereferencing to PRLs in macu-
lar patients is a slow process that has a median time ranging
from 1 to 6 months, depending on the age of MD onset [5].
The difference in the time courses between simulated and
real scotoma is even more remarkable when considering the
fact that the simulated scotoma in our experiment was
imposed for only about 1 hr per day. It is quite plausible that
the gradual deterioration of vision in MD patients interferes
with the development of adaptive oculomotor behavior. Age
may also be a contributing factor to the slow development.
Patients have better fixation stability if their central vision
loss occurred at an early age [20]. In a recent study, we found
that older adults were slower and used excessive eye move-
ments during a visual search task with simulated central sco-
toma [26], although the same study did not examine PRL
development. Another likely cause for the slow development
is that real scotomas are often invisible or with unclear bound-
ary [27–29]. A visible scotoma can provide accurate positional
feedback and, thus, may speed up PRL development. Given
our results of a robust development of PRL and oculomotor
rereferencing with a visible scotoma and the persistence of a
PRL even when the scotoma was rendered invisible, it might
be possible to speed up the process of PRL development in
patients by superimposing a simulated scotoma on the real
scotoma, thereby creating a visible border.
The remarkable ability of the oculomotor system to rapidly
adjust to an occluded central vision reveals a basic guiding
principle of oculomotor control. Given the time pressure
underlying saccadic eye movements, the system strives to
maintain simplicity—a new motor plan is formed by adding a
constant vector offset to the existing and well-practiced motor
plan. Our finding opens up the rich possibility of exploring
plasticity in the cortical and subcortical structures associated
Rapid Adaptation of Saccades without Fovea
1667
A Saccade latency
450
Saccade Latency (ms)
Invisible
350 Scotoma
250
150
Free
Explicit Training Retention
50 Exploration
0 10 20 30 40 50 60 70 80 90
Block Number
Figure 4. Changes in Eye Movement Characteristics during Object Following
(A) Median saccade latency (the time taken to make the first saccade upon object movement) as a function of block number (same format as in Figure 2B).
(B) Mean number of saccades per object movement (i.e., the number of corrective saccades plus one) as a function of block number.
(C) Mean duration of fixation between object movement as a function of block number. Error bars represent 61 SD.
with oculomotor control and in the visual areas that are retino-
topically associated with the newly formed PRL.
Experimental Procedures
Participants
We recruited 12 normally sighted subjects from the University of Southern
California campus (ages ranging from 19 to 30 years, one female). Six
subjects participated in the simulated scotoma experiments. The other six
subjects participated in the control experiment. They all had normal or cor-
rected-to-normal vision without known cognitive or neurological impair-
ments. The mean acuity (assessed with a lighthouse distance acuity chart)
was 20.1 logMar (Snellen 20/15). Subjects received monetary compensa-
tion for their participation. The experimental protocols were approved by
the internal review board of the University of Southern California, and written
informed consent was obtained from all subjects prior to the experiment.
Stimuli and Apparatus
All stimuli were high-contrast 24 bit RGB color images of indoor scenes and
objects. Images of 49 indoor scenes (1,024 3 768 pixels) were selected
from an image database [30]. Images of 140 objects (average diagonal size
of 2.4 with a range of 2 to 2.7 ) were selected from a commercially available
set of photographs of real objects at www.photos.com (now at www.
thinkstockphotos.com). The stimuli were generated and controlled with
MATLAB (version 7.9) and Psychophysics Toolbox extensions (Windows 7
OS) [31, 32] running on a Dell PC. The display was a 19’’ CRT monitor (refresh
rate, 85 Hz; resolution, 1,024 3 768). The stimuli were presented at a viewing
distance of 57 cm. The displayed scenes subtended visual angles of 39 3 29 .
Eye Movement Recoding and Simulated Scotoma
Subjects’ eye movements were monitored with an infrared video-based eye
tracker sampled at 2,000 Hz (EyeLink 1000 Tower Mount monocular
eyetracker, SR Research) with a maximum spatial resolution of 0.02 . A
nine-point calibration and/or validation sequence was performed at the
beginning of every block, and drift correction was made at the beginning
of every trial. Calibration and/or validation were repeated until the validation
error was smaller than 1 on average. The average gaze error was 0.5 ,
ranging from 0.1 to 1 . A gaze-contingent visual display was used to simu-
late central visual field loss in normally sighted subjects. This paradigm,
referred to as ‘‘artificial scotoma’’ [33], has been used in previous studies
to investigate various issues related to central field loss [23, 34, 35]. The
real-time gaze position was sent to the display computer through a high-
speed Ethernet link. The continuous gaze information was used to draw a
scotoma on the display screen at a refresh and update rate of 85 Hz. The
size and shape of the scotoma were derived from the visual field measure-
ment obtained from a patient with age-related MD [36]. The scotoma, as
shown in Figure 1A, was a nearly circular disc, subtended about 10 of visual
angle, and was rendered as a uniform gray patch (luminance 18 cd/m2) on
the screen. We also ran an invisible scotoma condition with a slightly lighter
gray patch, the luminance of which was matched to that of the gray
B Number of saccades C Fixation duration
Average
6
Fixation Duration (ms)
Controls
Number of Saccades
800
5
4 600
Invisible Invisible
3 Scotoma Scotoma
400
2
200
1
Free Free
Explicit Training Retention Explicit Training Retention
0 Exploration 0 Exploration
0 10 20 30 40 50 60 70 80 90 0 10 20 30 40 50 60 70 80 90
Block Number Block Number
background (22 cd/m2). The average delay between actual eye movement
and screen update was estimated to be approximately 10 ms (range from
2 ms to 15 ms on the basis of the eye data to frame time latencies that we
measured on the stimulus computer and on the manufacturer’s data on min-
imum eye data latency). The gaze position error (i.e., the difference between
target position and computed gaze position) was estimated during the nine-
point validation process. A chin-and-forehead rest was used throughout the
experiment in order to minimize head movements and trial-to-trial variability
in the estimate of gaze position. The emergence of an eccentric retinal locus
with rereferenced saccades observed in the free exploration period of the
experiment, in contrast to the normal foveating behavior observed in the
control experiment, served as confirmation that the slight amount of spatio-
temporal imprecision in the eye-tracking system was not sufficient to inter-
fere with the effectiveness of the simulated central scotoma.
Procedure
Subjects performed a demanding visual task in uninterrupted blocks of 30
trials each. On average, subjects took 30 hr to complete the entire experi-
ment (excluding breaks and calibration time). This was spread into several
sessions spanning two months. Each block took approximately 25 min to
complete. Subjects performed the task in a dimly lit room while they were
seated in a comfortable position with chin and forehead supports. Each
block started with the calibration and/or validation sequence described
earlier (w5 min) followed by drift correction. The trial started with an auditory
beep immediately after drift correction. For each trial, subjects had to com-
plete four task phases: object following, gaze centering, visual search, and a
second object following (Figure 1A).
Object Following
During object following, subjects followed a target object as it was randomly
repositioned four times against a gray background (Figure 1A, i). The center
of the object was uniformly distributed within the central 31 3 22 region of
the display. Each move was initiated only when the onscreen position of the
subjects’ scotoma did not occlude the target object for at least 1.5 s. This
was done to encourage eccentric fixation. Subjects were told to examine
the target object as accurately as possible, given that it was the search
target for the upcoming visual search phase. Otherwise, subjects did not
receive any explicit instructions on how to use their gaze.
Gaze Centering
During gaze centering, subjects centered their gaze in the middle of the
screen so that their scotoma was placed inside a black rectangular box
for 1.5 s (Figure 1A, ii). This was performed right before the onset of visual
search in order to minimize any positional bias.
Visual Search
During visual search, subjects searched for the target object (the same
object as in phase 1) amidst a cluttered background with an array of
nontarget distracters (Figure 1A, iii). Both the target and nontarget dis-
tracters were superimposed on the scene rather than being part of the
scene. This was done in order to minimize any contextual effects on search
performance. Subjects were given an unlimited amount of time to perform
the search, after which they indicated the presence or absence of the search
target by a key press (‘‘p’’ for presence and ‘‘a’’ for absence). The probability
Current Biology Vol 23 No 17
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A Search accuracy B Search time C Number of saccades

100 5 30
Average

Number of Saccades
Invisible

Search Time (sec)

4 Scotoma 25 Controls
Accuracy (%)

90
20 Invisible
3 Scotoma
80 15
Invisible
Scotoma
10
70 2
5
Free Free Free
Explicit Training Retention Explicit Training Retention Explicit Training Retention
Exploration Exploration Exploration
60 0
0 10 20 30 40 50 60 70 80 90 0 10 20 30 40 50 60 70 80 90 0 10 20 30 40 50 60 70 80 90
Block Number Block Number Block Number

Figure 5. Changes in Visual Search Performance

(A) Visual search accuracy (percent correct) as a function of block number (same format as in Figure 2B). The mean accuracy level (89% 6 2.1% SD) was
similar to that of the control group and was constant through the course of the experiment.
(B) Time taken to complete a search trial (either target present or target absent) as a function of block number.
(C) Number of saccades required for the completion of a search trial. Only correct trials were included for (B) and (C). Error bars represent 61 SD.

of the target being present was 0.5. Subjects were instructed to perform the
search task as quickly and as accurately as possible. An auditory feedback
was provided for a correct response.
Second Object Following
A second object following phase was conducted similarly to the first object
following phase, except that the target was a randomly drawn object that
appeared on a cluttered background (Figure 1A, iv). Oculomotor perfor-
mance (fixational PRL and saccadic rereference) was assessed during the
two object following phases (phases 1 and 4) under the assumption that
the target object was the intended target of gaze.
Subjects performed at least two or three blocks per day and completed
9 to 30 blocks of the task during free exploration. Subjects then received
explicit training (42 to 72 blocks) for refining the emerged PRL. This was
accomplished by having the subjects perform the same task as in the free
exploration period except that their PRLs were marked with a small 0.7
white cross (Figure 1B), and subjects were instructed to use the cross as
the point of gaze. This effectively encouraged the subjects to rely on the
emerged PRLs for the task and possibly improve fixation accuracy with
the peripheral locus. For normal foveal vision, a significant decrease in the
accuracy of eye positions has been reported in the absence of a fixation
marker [37]. Upon the completion of explicit training, subjects took a break
for at least 1 week before being recalled for another round of the task for five
to seven blocks (retention assessment). After the retention assessment,
subjects performed five additional blocks of the object following and visual
search tasks against a gray background, a process that was identical to the
first object following phase and the third visual search phase of the free
exploration period of the experiment but with one exception: the luminance
of the simulated scotoma was matched to that of the background (Figure 1C).
As a result, the simulated central scotoma was not visible to the subjects
(invisible scotoma). Thus, the invisible scotoma experiment consisted of
two phases: object following (Figure 1C, i) and visual search (Figure 1C, ii).
A separate group of six subjects participated in a control experiment (a total
of five blocks) identical to free exploration but without the simulated sco-
toma (control experiment). The specific numbers of blocks each subject per-
formed in the different stages of the experiment are listed in Table S1.
Data Analysis
Gaze position data were first preprocessed by an edge-preserving median
filter with a 200 ms window in order to remove transient noise. Then, a modi-
fied version of a standard parsing algorithm [38, 39] was applied to the pre-
processed data in order to robustly classify saccades and fixations while
excluding microsaccades [40]. We defined a period of eye movement as a
saccade if the following conditions were met: (1) the eye velocity exceeded
20 per s during the entire period, (2) the peak velocity during this period was
in the top 25th percentile of the recording phase, (3) the beginning and end of
this period had a velocity of at least 15% of the peak velocity, and (4) the
amplitude of the eye movement during this period exceeded 0.9 . Periods
that were not saccades were candidates for fixations. A candidate period
was classified as a fixation if it started with at least 50 ms of stable gaze
(SD in gaze position did not exceed 0.5 in any direction) and ended with
one of the following conditions: (1) a period of missing data (a blink)
exceeding 500 ms, (2) the start of a saccade, or (3) the start of a reliable drift
that exceeded 1 .
Fixation density maps were derived from the retinal positions of the target
objects during periods of fixation via kernel density estimation with a bivar-
iate Gaussian kernel [41]. The PRL was defined as the peak of the density.
Fixation stability has traditionally been quantified by calculating the area
of the ellipse that encompasses a given proportion of eye positions during
fixation [42]. This area is termed the BCEA [43]. A more stable fixation cor-
responds to a smaller BCEA. In the current study, the variance of fixation
was defined as the BCEA that encompassed 68% of fixations around the
mean [42] and was used as an indicator of fixation stability. BCEAs were
calculated from the density maps. (The fixational BECAs measured from
the current experiment are most likely to be overestimations because we in-
structed our subjects to simply ‘‘follow and examine’’ an object, 2 to 2.7 in
size without specifying where on the object a subject must fixate.) The den-
sity maps for the first saccade landing site were obtained in a similar manner
from the retinal positions of the target objects at the end point of the first
saccade after object movement.
Supplemental Information
Supplemental Information contains two figures and one table and can be
found with this article online at http://dx.doi.org/10.1016/j.cub.2013.06.056.
Acknowledgments
This work was supported by National Institutes of Health grants
R01EY017707 and R01EY016093. The authors would like to thank A. Disney,
G. Legge, G. Timberlake, and two anonymous reviewers for their helpful
comments and discussion of the manuscript and J.L. Gonzales and E. Trinh
for their help with subject recruitment and data collection.
Received: May 25, 2013
Revised: June 14, 2013
Accepted: June 24, 2013
Published: August 15, 2013
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