Vision Is Adapted to the Natural Level of Blur Present in the Retinal Image
Marcos S (2011) Vision Is Adapted to the Natural Level of Blur Present in the Retinal Image. PLoS
ONE 6(11): e27031. doi:10.1371/journal.pone.0027031
Vision Is Adapted to the Natural Level of Blur Present in the Retinal Image
Lucie Sawides 0
Pablo de Gracia 0
Carlos Dorronsoro 0
Michael A. Webster 0
Susana Marcos 0
Michele Giugliano, University of Antwerp, Belgium
0 1 Instituto de O ptica, Consejo Superior de Investigaciones Cient ficas (CSIC) , Madrid , Spain , 2 Department of Psychology, University of Nevada , Reno, Nevada , United States of America
Background: The image formed by the eye's optics is inherently blurred by aberrations specific to an individual's eyes. We examined how visual coding is adapted to the optical quality of the eye. Methods and Findings: We assessed the relationship between perceived blur and the retinal image blur resulting from high order aberrations in an individual's optics. Observers judged perceptual blur in a psychophysical two-alternative forced choice paradigm, on stimuli viewed through perfectly corrected optics (using a deformable mirror to compensate for the individual's aberrations). Realistic blur of different amounts and forms was computer simulated using real aberrations from a population. The blur levels perceived as best focused were close to the levels predicted by an individual's high order aberrations over a wide range of blur magnitudes, and were systematically biased when observers were instead adapted to the blur reproduced from a different observer's eye. Conclusions: Our results provide strong evidence that spatial vision is calibrated for the specific blur levels present in each individual's retinal image and that this adaptation at least partly reflects how spatial sensitivity is normalized in the neural coding of blur.
Funding: This work was supported by the following: Ministerio de Ciencia e Innovacio n (MICINN), Formacio n de Personal Investigador (FPI) Predoctoral
Fellowship to LS; Consejo Superior de Investigaciones Cientficas (CSIC) I3P Predoctoral Fellowship to PdG; EY-10834 to MW; MICINN FIS2008-02065 and
EURYI-05102-ES (European Heads of Research Councils-European Science Foundation EUROHORCs-ESF) to SM. The funders had no role in study design, data collection and
analysis, decision to publish, or preparation of the manuscript.
Competing Interests: The authors have declared that no competing interests exist.
Optical aberrations degrade the quality of the images projected onto
the retina and vary widely in magnitude and distribution across the
population . Unlike spherical or cylindrical errors, High Order
Aberrations (HOAs) are not typically corrected, and thus individuals
are each chronically exposed to different patterns of retinal blur. We
asked whether spatial coding in the visual system is matched to the
native blur level specific to an individuals HOAs. Recent studies have
demonstrated short-term aftereffects in both perceived blur and visual
acuity following exposure to blur introduced optically or by filtering
images [2,3]. Several studies show evidence that eyes are adapted to
HOA induced by corneal pathology , by corneal surgery  or by
aging . We have shown that observers can adapt to the blur induced
by HOA from scaled versions of their own aberrations, or those from
other subjects . However, the extent to which observers are adapted
to their own optical aberrations remains unresolved. On the one hand,
both short- and long-term adaptation can selectively adjust to the axis
of astigmatic blur [8,9], and visual performance is better in observers
with optics strongly degraded by corneal pathology compared to
normal subjects induced with similar amounts of HOAs . Moreover,
Artal et al.  found that stimuli seen through an individuals natural
aberrations appear sharper than when seen through a rotated version
of the same aberrations, and adaptation to surgically induced HOAs
has been suggested to occur in patients after LASIK surgery . These
studies thus point to neural compensations for the wave aberrations
characterizing the individuals eye. Yet on the other hand, studies of
visual acuity and subjective image quality have found immediate
improvements after correcting HOAs, with only a small residual bias
toward the observers native HOAs and little further improvement
with training [11,12]. These results have therefore suggested that there
may instead be relatively little adaptation to HOAs. To directly test for
this adaptation, we used a custom-developed Adaptive-Optics (AO)
system to measure and correct the observers aberrations (with best
spherical refraction error correction and a 5-mm pupil). By removing
the natural aberrations of the eye, all observers were exposed to
identical aberration patterns and therefore any difference in the visual
response must be due to neural factors. We then manipulated retinal
blur by projecting degraded images with known HOAs. Subjective
focus was measured with a 2-Alternative-Forced-Choice (2AFC)
procedure in which the observer had to report whether the image
displayed on the monitor appeared too blurred or too sharp.
Testing scaled HOA patterns
In the first experiment, sequences of images were blurred by
convolution with the corresponding point spread functions (PSFs)
estimated from scaled versions of each observers HOA patterns,
ranging from diffraction limited (scale factor F = 0) to double the
amount of natural blur (F = 2) in 0.05 steps. When F = 1, the
simulated image thus represents the natural degradation imposed
by the subjects HOAs (Fig 1). The blur level selected as best
focused was very close to the natural blur level for 3 of 4 observers,
and for all observers remained very similar whether observers first
adapted to a neutral gray field or to the image filtered by their own
natural blur. The settings under neutral adaptation (gray field)
were roughly 77% of their HOA (89.3% excluding Subject S3 who
has a low tolerance to blur) and similar to the settings when they
were adapted to their own HOA (82%, and 94.3% excluding S3)
(Fig 2A). The neutral focus therefore was not perceived for fully
corrected optics, and in general, occurred at a blur level near the
subjects own aberrations. The low difference in the perceived
neutral focus between neutral adaptation (gray field) and natural
adaptation suggested that the subjects were pre-adapted to their
own aberration level. The average difference in the perceived
focus between the neutral and the natural adaptation conditions
was 0.012 (in terms of strehl ratio, SR, defined as the normalized
peak of the PSF). However, the perceived focus was biased from
the blur level predicted by their HOAs (by 0.044 in terms of SR,
on average) when each observer was instead adapted to images
blurred by others HOA patterns, corresponding to the native blur
of the other 3 participants (Fig 2B). The pattern of after-effects was
consistent with the adaptation predicted by the overall blur
magnitude. Specifically, in individuals with lower SRs (more native
blur), adaptation to the blur from the less aberrated eyes caused
their native focus level to appear too blurred (as expected if they
were now adapted to images that were previously for them too
sharp Fig 3, observer S1). Conversely, observers with low levels of
natural blur perceived their natural focus level as too sharp when
adapted to the blur from more aberrated eyes (Fig 3; observer S4).
Testing 128 real complex HOA patterns
In a further experiment, we examined whether the internal
norm for blur is set to a specific aberration pattern or to the overall
blur, regardless of its form. Observers again judged whether
images appeared too blurred or too sharp, but this time for an
image sequence generated from a set of 128 different HOA
patterns from real eyes. These ranged from very pronounced
HOAs (from surgically corrected eyes) to almost diffraction-limited
(achieved with AO-correction measurements), with blur levels (SR)
ranging from 0.049 to 0.757 (5-mm pupils). A subset of PSFs and
the corresponding simulated images generated by convolution are
shown in Fig. 4 (A, B). Fifteen subjects were tested, with SR
ranging from 0.103 to 0.356 (5-mm pupils). There was a close
correspondence between the image quality perceived as neutral
and the retinal image quality produced by the aberrations of the
subject, with an average deviation of 0.014 (in terms of SR), and a
strong correlation between the blur of the image perceived as
neutral and the subjects own blur (Slope = 0.95; R = 0.94;
p,0.0001; Fig. 4C). For the majority of the subjects, the blur
level perceived as best focused was well predicted from the
magnitude of the native blur present in their eyes.
Adaptive Optics (AO) is a useful technique to compensate the
aberrations of the subjects, as had been shown in numerous
previous studies . AO, allowing to appropriately control
the blur level of the retinal image, provided a powerful technique
to directly test neural adaptation to the subjects own blur level.
The innovative finding of the paper is that subjects appear to be
adapted to the blur level imposed by their own optical aberrations.
Adaptive Optics has allowed us to cancel the natural aberrations of
all subjects, exposing observers to identical aberration patterns and
ensuring that any difference across subjects will arise from their
own neural processing and their prior neural adaptation. Under
these conditions, we found that an observers focus settings remain
largely unaffected when adapting to their own aberrations, but
were significantly biased toward higher or lower blur levels when
adapted to the aberrations from observers with more or less optical
blur respectively. This demonstrates that the visual mechanisms
mediating the perception of focus can differentially adapt to
changes in image blur level resulting from HOAs. Moreover, the
finding that aftereffects were weakest near the level of the
observers natural blur (Fig 4, S1 and S4) further suggests that
the individuals subjective neutral point corresponded to the
longterm adapted state induced by their optics. This in turn suggests
that the blur level that appears correctly focused to an observer is
not merely a learned criterion (e.g. so that all observers encode
blur similarly but choose the blur level they are accustomed to
seeing). Specifically, if observers differed only in how they labeled
the blur (and thus did not differ in the neural encoding) then they
should all show the same aftereffects for a given adapting level,
regardless of whether they described that level as too blurred or
Figure 1. Testing scaled high order aberrations patterns. a) Adapting images in testing scaled high order aberrations patterns: Gray field and
simulated adapting images generated by convolution with the PSFs (shown, with corresponding SR) obtained from 4 different subjects HOA
patterns. Tilt and astigmatism were set to zero whereas defocus was adjusted to maximize optical quality. Data are for 5-mm pupils.
Figure 2. Testing scaled high order aberrations patterns. a) Relative Strehl Ratio of the perceived best focus image (with respect to the
subjects native level) for gray field adaptation or adaptation to each subjects own HOAs. b) Difference in Strehl Ratio between gray and natural
adaptation when subjects were adapted to their own HOAs (blue) and other subjects HOAs (red), averaged across the other 3 HOA patterns.
too sharp (since the adaptation would induce the same shifts in
their neural sensitivity). Instead, direction of the blur aftereffect
was specific to each observers intrinsic blur level, revealing that
the individual differences in perceived focus at least in part reflect
differences in how their sensitivities are normalized to their
ambient blur level .
Our results also show that the close association between the
coded norm for blur and the observers aberrations holds over a
very wide range of native blur levels (Fig 3). For the majority of
subjects, the blur level that is perceived as best focused is very
closely predicted from the magnitude of the native blur present in
their eyes. Together with the observed adaptation effects, this
finding strongly suggests that the perception of focus is calibrated
for the specific blur levels present in each individuals retinal
image. On the other hand, this normalization may depend largely
on the overall level of the blur and not on the specific pattern of
HOAs generating this level, for this close association held even
though the stimuli were not matched to the observers in terms of
the actual form of the HOAs. This raises the possibility that the
processes of blur adaptation may be unable to resolve subtle
Figure 4. Testing 128 real complex high order aberration patterns. a) Subset of 16 PSFs estimated from HOA in real eyes (from a total of 128
used in the blur judgment experiment), with their corresponding SR. Tilt and astigmatism were set to zero whereas defocus was adjusted to
maximize optical quality. Optical quality ranges from highly degraded from surgical eyes to almost diffraction-limited (from AO-correction). Data are
for 5-mm pupil diameters. b) Test sequence images blurred by convolution with the corresponding PSFs in a). The experiment used the complete
sequence of 128 images. c) Strehl Ratio of the image perceived as best focused versus the natural Strehl Ratio for each of the 15 subjects.
differences in the patterns of blur specific to different HOAs, so
that the adaptation state is instead largely controlled only by the
blur magnitude. The fact that the overall amount of blur proved
more critical than orientation is a further novel finding of the
study. However, this does not preclude the possibility that the
adaptation can also selectively adjust for some differences in the
HOA pattern when blur magnitudes are equated  analogous
to the selectivity found for low order aberrations .
How can these results be reconciled with evidence for only weak
adaptation to HOAs? A likely answer is that different studies have
measured different perceptual judgments. Correcting HOAs leads
to improvements in visual acuity and an increased subjective
impression of sharpness [12,15,17]. Previous studies testing for
adaptation after correction selected the sharpest image for best
image quality, while our observers were instead required to choose
the point of subjective focus at which the image appeared neither
blurred nor sharp. Consistent with this difference, we scaled the
PSF by factors ranging from 0 to 2, which ranged from sharper to
blurrier than their natural HOA, whereas previous studies
(e.g.) instead used stimuli ranging from -1 to 1, and thus
never increased the blur relative to the natural level. It is thus
plausible that the much stronger implied adaptation we observed is
because this adaptation is more conspicuous in how it affects
judgments of perceived focus, which may correspond to the neural
norm for blur perception . This norm is set by the observers
natural level of blur, yet as we have shown can be rapidly
recalibrated when adapted to a different level of HOAs.
Consequently spatial vision may be normalized to compensate
for the optical imperfections of the eye in the same way that color
vision is normalized to discount the spectral filtering of the lens
Materials and Methods
All participants, who were acquainted with the nature of the
study, provided written informed consent. All protocols met the
tenets of the Declaration of Helsinki and had been previously
approved by the Consejo Superior de Investigaciones Cientficas
(CSIC) Ethical Committee.
Four experienced observers participated in the first experiment
and 15 observers (3 of the authors and 12 naive observers)
participated in experiment 2. All had normal vision, their natural
Strehl Ratio at best focus varied from 0.097 to 0.356 (0.097 to
0.1932 in experiment 1 and 0.103 to 0.356 in experiment 2).
Apparatus and Stimuli
The primary components of our custom Adaptive Optics system
are a Hartmann-Shack wavefront sensor (HASO 32 OEM,
Imagine Eyes, France) and an electromagnetic deformable mirror
(MIRAO, Imagine Eyes, France). A motorized Badal system
compensated for the subjects spherical error and two
psychophysical channels were used for stimulus presentation. The first
channel, composed of a 12 mm69 mm SVGA OLED minidisplay
(LiteEye 400) ,was used to fix the sight during the measurement
and correct the subjects aberration; The second, composed of a
12616 inches CRT Monitor and controlled by the ViSaGe
psychophysical platform (Cambridge Research System, UK), was
used to project the adapt and test images. The system was
controlled using custom routines written in Visual C++ (to control
the AO-loop and the Badal system) and Matlab to control the
ViSaGe psychophysical platform. More details of the AO-system
are reported in recent studies [15,17].
Psychophysical measurements were performed under static
correction of aberrations. We performed a close loop correction at
13 Hz in 15 iterations and saved the state of the deformable
mirror with the voltage applied to each actuator for future use.
The residual wavefront error was continuously monitored (before
and after each measurement) and deemed satisfactory if less than
0.15 mm RMS (excluding tilts and defocus). On average, RMS
(excluding tilts and defocus) decreased from 0.52360.33 mm to
0.08060.038 mm, with an average HOAs correction of
Generation of the optical blur
The original image (a face) in both experiments was acquired
using a photographic digital camera with an original resolution of
4 M pixels and converted to grayscale. In the first experiment,
testing scaled HOA patterns, the optical blur was generated by
convolution of the image with the PSF estimated from the subjects
HOAs. Aberrations of the subject were measured using the
AOset-up, and fitted by 7th order Zernike polynomials. Tilts and
astigmatism were set to zero whereas defocus was set to optimize
SR and achieve best optical quality. Standard Fourier Optics
techniques , were used to calculate the corresponding Point
Spread Function PSF. The PSF was scaled to match the pixel-size
of the face image in 1.98u window. All computations were
performed for 5-mm pupils. The Stiles-Crawford effect was not
considered, as for a typical values (,0.1 mm21)  its effect was
negligible for the purposes of our study. A double diffraction when
viewing the convolved image through a diffraction-limited 5-mm
pupil (convolution + artificial pupil-aperture) was not corrected by
means of inverse filtering as also considered negligible. Simulations
conducted to assess the impact of these two effects revealed that
the effect on the final contrast of convolved E targets with similar
levels of blur to those used on the experiment was less than 10%
with respect to the contrast obtained without including these two
factors. Simulations and experiments using a CCD camera as an
artificial retina confirmed that the convolved images were optically
corrected both in scale and contrast, within the experimental error
of the CCD image acquisition. Sequences of images were
generated for each subjects HOAs, by multiplying each Zernike
coefficient by a factor F between 0 and 2 in 0.05 steps. Multiplying
the Zernike coefficients by these factors modifies the amount of
blur while preserving the relative shape of the PSF. Each set of
testing images contained 41 different test images ranging from
diffraction-limited to double the amount of natural blur. When the
factor F was equal to 1, the simulated image represented the
natural degradation imposed by the subjects HOAs and these
images were used in the conditions testing adaptation to natural
In the second experiment, testing 128 real complex HOA
patterns, the optical blurred was generated by convolution, using
the same method as in first experiment, with the PSF estimated
from 128 different complex aberration patterns from real eyes.
Tilts and astigmatism were set to zero, whereas defocus was set to
optimize Strehl Ratio and achieve best optical quality. The optical
quality ranged from high amounts of HOAs (from surgically
altered eyes) to almost diffraction-limited (achieved with
AOcorrection measurements). The sequence of test images thus
contains 128 images with Strehl Ratio ranging from 0.049 to 0.757
Observers viewed the images in a darkened room. An artificial
pupil in a pupil conjugate plane guaranteed that the measurements
were performed under constant pupil size of 5-mm pupil diameter.
The subjects pupil was aligned to the system using a bite bar and
the pupil was centered and focused. The subject was then asked to
adjust the best subjective focus, by controlling the Badal system
with a keyboard while he/she looked at a high contrast Maltese
cross on the minidisplay.
Natural aberrations were measured and corrected (all
aberrations except tilts and defocus) in a closed loop adaptive optics
operation. Then, the subject was asked again to adjust the Badal
system position that provided the sharpest subjective focus for this
AO-corrected condition. The state of the mirror that achieved this
correction was saved and applied during the measurements.
During testing, the natural pupil was continuously monitored to
ensure centration, and the wave aberration was measured before
and after each test (i.e. every 5 minutes) to ensure appropriate
AOcorrection (with a new closed-loop correction applied if necessary).
The images in the tests were presented on the CRT monitor
and subtended 1.98 degrees. The psychophysical paradigm
consisted of a 2AFC procedure, where the subject responded
whether the image was sharp or blurred. Stimulus levels were
varied with a quest algorithm in order to find the level of best
perceived focus point for a given adaptation condition (neutral
adaptation with a gray-field or adaptation to natural aberrations).
In all cases, the sequence of the psychophysical experiment
consisted of 1 min exposure to the adapting image after which a
test image was presented to the subject who had to respond if the
image was sharp or blurred. The subject re-adapted for 3 seconds
between each test image. Adapting images were spatially jittered in
time to prevent local light adaptation.
In the first experiment, blur judgments were measured on 4
subjects (Strehl Ratio ranging from 0.094 to 0.1932 (5-mm pupils),
after neutral adaptation (gray-field) and after adaptation to images
blurred with the natural degradation imposed by each of the 4
subjects HOAs (including their own). The results were analyzed in
terms of the SR of the perceived focus point. In a second
experiment, judgments of perceived blur were measured in 15
subjects to determine for each individual the physical blur level
that appeared best focused under neutral adaptation (gray field).
Typically 3 repeated settings were made for each observer.
Conceived and designed the experiments: LS SM. Performed the
experiments: LS. Analyzed the data: LS. Wrote the paper: LS PdG CD
MAW SM. Gave technical support and conceptual advice: CD PdG.
Supervised the project: SM MAW.
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