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| Volume 4, Number 4, Article 4, Pages 281-287 |
doi:10.1167/4.4.4 |
http://journalofvision.org/4/4/4/ |
ISSN 1534-7362 |
Neural compensation for the eye’s optical aberrations
Pablo Artal |
Laboratorio de Optica, Departamento de Física, Universidad de Murcia, Campus de Espinardo, Murcia, Spain |
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Li Chen |
Center for Visual Science, University of Rochester, Rochester, NY, USA |
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Enrique J. Fernández |
Laboratorio de Optica, Departamento de Física, Universidad de Murcia, Campus de Espinardo, Murcia, Spain |
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Ben Singer |
Center for Visual Science, University of Rochester, Rochester, NY, USA |
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Silvestre Manzanera |
Laboratorio de Optica, Departamento de Física, Universidad de Murcia, Campus de Espinardo, Murcia, Spain |
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David R. Williams |
Center for Visual Science, University of Rochester, Rochester, NY, USA |
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Abstract
A fundamental problem facing sensory systems is to recover useful information about the external world from signals that are corrupted by the sensory process itself. Retinal images in the human eye are affected by optical aberrations that cannot be corrected with ordinary spectacles or contact lenses, and the specific pattern of these aberrations is different in every eye. Though these aberrations always blur the retinal image, our subjective impression is that the visual world is sharp and clear, suggesting that the brain might compensate for their subjective influence. The recent introduction of adaptive optics to control the eye’s aberrations now makes it possible to directly test this idea. If the brain compensates for the eye’s aberrations, vision should be clearest with the eye’s own aberrations rather than with unfamiliar ones. We asked subjects to view a stimulus through an adaptive optics system that either recreated their own aberrations or a rotated version of them. For all five subjects tested, the stimulus seen with the subject’s own aberrations was always sharper than when seen through the rotated version. This supports the hypothesis that the neural visual system is adapted to the eye's aberrations, thereby removing somehow the effects of blur generated by the sensory apparatus from visual experience. This result could have important implications for methods to correct higher order aberrations with customized refractive surgery because some benefits of optimizing the correction optically might be undone by the nervous system's compensation for the old aberrations.
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History
Received September 29, 2003; published April 16, 2004
Citation
Artal, P, Chen, L., Fernández, E. J., Singer, B., Manzanera, S., & Williams, D. R. (2004). Neural compensation for the eye’s optical aberrations.
Journal of Vision, 4(4):4, 281-287,
http://journalofvision.org/4/4/4/,
doi:10.1167/4.4.4.
Keywords
neural adaptation, optical aberrations, eye, adaptive optics
for related articles by these authors
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The human eye is affected by aberrations that degrade
the retinal image and ultimately limit spatial vision (Liang & Williams, 1997; Artal, Guirao, Berrio, &
Williams, 2001; Hofer, Artal, Singer,
Aragón, & Williams, 2001a). The
lower order aberrations, defocus and astigmatism, are corrected routinely with
spectacles, contact lenses, intraocular lenses, and refractive surgery. The
higher order aberrations, beyond defocus and astigmatism, have been known to
exist in the eye for more than 150 years (Helmholtz, 1881). However, it has only recently been
possible to correct these aberrations in the living eye. Adaptive optics (AO), a
technique developed in astronomy to remove the effect of atmospheric turbulence
from telescope images (Hubbin & Noethe, 1993), can also be used to correct the
eye’s higher order aberrations (Liang, Williams, & Miller, 1997; Vargas-Martín, Prieto, &
Artal, 1998; Fernández, Iglesias, &
Artal, 2001; Hofer et al., 2001a). One application of this technology in
the eye is to obtain high-resolution images of the retina to
resolve individual photoreceptors in
vivo (Liang et al., 1997) and to identify the photopigment in each
cell (Roorda & Williams, 1999). Another
important application of AO is to produce controlled wave-aberration patterns in
the eye, enabling new experiments to better understand the impact of the ocular
optics on vision. In particular, it is possible to address the intriguing
question of whether the visual system is adapted to the particular pattern of
optical aberrations of its own eye. To test this idea, subjects viewed visual
stimuli with aberrations controlled with adaptive optics. The AO apparatus
corrected the eye’s wave aberration and replaced it with the same wave
aberration or with a rotated copy of it.
The wavefront aberration (WA) is a function that
characterizes the image-forming properties of any optical system. It is defined
as the optical deviation of the wavefront along a certain ray from the perfect
spherical wavefront. The WA is related to the image of a point source produced
by the system, the point-spread function (PSF), through an integral equation
(Born & Wolf, 1985). AO permits the
manipulation of the eye’s WA by introducing different optical paths over
the pupil area.
An AO system consists of a wavefront sensor to measure
the WA in real time and a correcting device, typically a deformable mirror, to
modify the WA. Figure 1 shows a schematic
diagram of the AO system at the University of Rochester used in this study. A
Hartmann-Shack wavefront sensor (Liang, Grimm, Goelz, & Bille, 1994; Liang & Williams, 1997; Prieto, Vargas-Martín, Goelz,
& Artal, 2000) measures the eye's WA at 30
Hz. A narrow infrared beam (810 nm, with a spectral spread of 20 nm) produced by
a super-luminescent diode (SLD) is projected into the subject's retina acting as
a beacon source. The irradiance on the cornea was approximately 5 μW, which
is about 30 times smaller than the maximum permissible exposure for continuous
viewing according to the safety standards (ANSI Z136.1, 1993). In the second pass, after the light is
reflected from the retina and passes through the complete system, an array of
177 lenslets produces an image of spots on a charged-coupled device (CCD)
camera. The locations of the spots in this image provide the local slopes of the
ocular WA. The aberrations were measured for a 6-mm pupil up to 10th radial
order, corresponding to an expansion of 63 Zernike modes (Noll, 1976).
Figure 1. Schematic diagram of the adaptive
optics system used in the blur matching experiment. The red path represents the
infrared light used for measuring the wavefront aberration and driving the
deformable mirror, whereas the green path is the light used for the visual
experiments. From beam splitter (BS) after the eye to the cold mirror, both
lights are together, although not represented for clarity. See the text for
additional details. CCD, charged-coupled device camera; DLP, digital
light-processing; H-S, Hartmann-Shack; SLD, super-luminescent source. The
picture in the lower right corner represents the visual stimulus used in the
experiment without preferred orientation (see the text for additional details).
A 97-channel deformable mirror
(Xinetics), with an aluminized glass
faceplate and lead magnesium niobate (PMN) actuators, was used as the
wavefront-correcting device. It is placed in the system optically conjugated
both with the subject's pupil plane and the wavefront sensor, by using
appropriate lenses and two off-axis parabolic mirrors. The AO system worked in
closed-loop, with the deformable mirror driven by the measured aberration data.
Typical aberrations were nearly eliminated after 5-10 iterations, thus a
correction of the eye’s aberrations was completed automatically in
0.17-0.33 s.
In this experiment, besides removing the higher order
aberrations in the eye on each trial, the deformable mirror also acted as an
aberration generator to blur the subject’s vision either with the
subject’s own aberrations or a rotated version of the aberrations. After
the currently present aberrations were corrected, eight different aberration
patterns were produced in each case: an average normal aberration pattern and
seven similar versions rotated by 45-deg intervals. Figure 2 shows an example of the actual eight
aberration patterns and the associated PSFs for one of the subjects. The desired
aberrations were kept stable by the AO system working in closed-loop while
subjects performed the matching experiment.
Figure 2. Example of the wavefront
aberration (a) and the associated point-spread functions (PSFs) (b) for the
normal (0) and the seven orientations for one of the subjects. The numbers
represented the rotated angle.
We relied on the wavefront sensor to indicate how well
we succeeded in creating the same PSF at all orientations. The wavefront sensor
can measure the combined wave aberration of the eye and the optical system
through which the subject views the stimulus, with the exception of a
beam-splitter, a mirror, and a lens. These uncommon path elements are
diffraction-limited and have negligible impact on the wave aberration. We
computed the Strehl ratio of the PSF generated at each orientation for every
subject. These values were independent of the orientation. Specifically, there
is no tendency for the image quality, assessed with these objective measures, to
be any better in the zero-orientation condition.
Subjects viewed a binary noise stimulus, produced by a
digital light-processing (DLP) video projector (Packer et al., 2001), through
the AO system. The stimulus was viewed in 550-nm monochromatic light (shown
schematically as the green light path in Figure
1). The stimulus, also shown in Figure 1,
contains sharp edges at all orientations and subtended 1 deg of visual angle.
The binary noise stimulus was produced from a uniform distribution filtered by
taking the FFT of the noise, applying an annular filter via point-by-point
multiplication, and then inverting back into the spatial domain. To get
black-and-white spots rather than gray levels, the intensities were thresholded.
Because the bandpass annular filter is circularly symmetric, it will eliminate
all lower spatial frequencies and higher ones, which make energy at all
orientations get through. A Gaussian function smoothed the edge of the field. On
each trial, the computer randomly generated a different stimulus pattern.
The matching experiment was performed on the right eyes
of five subjects. During the measurement, the subject's head was stabilized with
a bite bar, and the subject's pupil was dilated and accommodation paralyzed with
cyclopentholate hydrochloride (2.5%). The experiment was performed for a 6-mm
diameter artificial pupil. Figure 3 shows
schematically the rationale of the matching experiment.
Figure
3. Schematic representation of the blur matching experiment. (a). The stimulus
was seen alternatively for 500 msec with the normal and the rotated wavefront
aberration. The yellow part represents the time where the desired aberration is
produced. The next green part represents the 500 ms while the stimulus is
presented to the subject with the appropriate aberrations. In each trial, the
stimulus is seen with the normal and one (randomly selected) rotated version of
the eye’s aberrations. (b). The subject’s task is to adjust the
amount of the aberrations by choosing a factor
(F)
in the rotated case to match the subjective blur of the stimulus to that seen
when the wave aberration was in the normal orientation. Additional pairs of
presentations with the normal and rotated (multiplied) aberrations are presented
until a factor
F
value is obtained for each orientation. The
subject viewed the stimulus for 500 ms immediately after the deformable mirror
generated the subject’s own aberrations or the rotated version. At other
times, the subject viewed a uniform field.
Subjects were asked to view the stimulus through the
AO system with their own aberrations or with a rotated version of their
aberrations. The stimulus was seen alternatively for 500 msec with both the
normal and the rotated PSF ( Figure 3a). The
yellow part in Figure 3 represents the time
when the desired aberration is produced. The eye’s optics remain stable
during the next 500 ms when the stimulus is presented to the subject. The
subject’s task was to adjust the magnitude (the root mean square [RMS]) of
the aberrations by multiplying it by a factor
( F) in the rotated
case to match the subjective blur of the stimulus to that seen when the wave
aberration was in the normal orientation ( Figure
3b). Subjects were unaware of when the stimulus was seen through the normal
or rotated aberrations. In the matching process, one of the seven different
rotated versions of the aberrations was randomly selected. Subjects were asked
to match the blur with all eight orientations, including the normal orientation,
in random order. Subjects could not tell which orientation was presented on
a given trial. Because the subjects matched the blur in the normal orientation
with an amplitude that was a physical match to that of normal wave aberration,
there is no possibility that increased blur for other
orientations.
If the rotated (uncommon) aberrations degraded the subjective
image quality, a factor F smaller than 1 was re-quired, as further illustrated in Figure
4 with a blurred stimulus. If the rotated wave aberration is less damaging for vision, a
factor F greater than 1 should have been required. The complete process of matching took several
minutes and was repeated up to 5 times to obtain robust estimates of the adjustment factor for each
rotated aberration pattern.
Figure
4. Additional schematic example of the blur matching experiment.
Figure 5 shows the
values of the matching (or adjustment) factor
F for the normal
aberrations (0-deg angle) and the other seven rotations in four of the subjects
that participated in the experiment. The error bars indicate the SD for each and
provide a direct indication of the statistical significance of the decline in
the matching for all
orientations. Figure 5. Blur matching values
(F) in four of the subjects as a
function of the orientation of the aberrations (in degrees). Error bars
represent SD of responses. The red line
shows value 1 that indicates no adaptation effect. Letters are subjects’
initials.
Figure 6 shows the
average values of the matching (or adjustment) factor
F (with the error
bars indicating the individual variability) for the normal aberrations (0-deg
angle) and the other seven rotations. In all subjects tested, the RMS wavefront
error of the rotated wave aberration required to match the blur with the normal
wave aberration was found to be on average 20-40% less than in the
normal-oriented aberration case. That is to say, the matching factor
F was between 0.6
and 0.8, indicating that the subjective blur for the stimulus increased
significantly when the PSF was rotated.
Figure 6. (a).
Average blur matching value (F) for the
five subjects as a function of the orientation of the aberrations (in degrees).
Error bars represent SD of responses
across subjects. The red line shows value 1 that indicates no adaptation effect.
(b). The same data in a polar representation.
Even though the matching factor was slightly higher for
the rotation of 180 deg than for the other rotations, it too was significantly
below a value of 1. A 180-deg rotation of the aberrations produces a retinal
image with an identical modulation transfer function (that is to say with the
same reduction in contrast for every sine-wave grating), although with a
different phase transfer function, as compared with the normal orientation PSF.
The fact that the subjective blur also increases in this case shows that the
adaptation process is phase sensitive. This implies that the process is not
simply a matter of adjusting the contrast of different portions of the spatial
frequency spectrum.
If the neural system is adapted to the specific shape
of the aberrations, the relative blur and then the matching factor should be
lower for those orientations that are most different from the normal
aberrations. To verify this assumption, we computed a parameter, the maximum of
the cross-correlation function, which provided information on the difference
between the original and rotated PSF.
Figure 7 shows the
comparison of the matching factor and the asymmetry parameter in four of the
subjects. This parameter resulted in a good qualitative agreement with the
values of the blur matching factor for each orientation.
Figure 7. Blur matching value
(F) (black circles and lines) and
asymmetry parameter (M) (red circles
and lines) for every orientation in four of the tested subjects.
It is also interesting to show
the effect of the matching factor as the
adjustment took place on the PSFs. As an example, Figure 8 shows the wavefront and the PSFs in one
subject (MC) for the normal case (0) and for the 45-deg rotations with matching
value 1 and 0.75. This last value actually corresponds to the matching value for
that subject and condition. The PSFs on the left (yellow label) and on the right
(blue label), although having a different extension, provide the same subjective
blur.
Figure 8. Example of the wavefront aberration
(top panels) and the associated point-spread functions (PSFs) in one of the
subjects for the normal (0) and the 45-deg rotation with two values of the
matching factors: 1 (pink label) and 0.75, corresponding to the actual matching
value for that subject and orientation (blue label). The PSF subtends 40
arcmin.
The results of this experiment support the hypothesis
that the neural visual system is adapted to the eye’s particular
aberrations, so that edges appear sharp despite the modest blur in the normal
retinal image. Although as far as we know this is the first time that strong
evidence for adaptation to higher order monochromatic aberrations has been
reported, adaptability in the visual system is indeed ubiquitous (Held, 1980). The phenomenon reported here may be the
monochromatic equivalent of chromatic fringe adaptation that renders less
visible the effects of chromatic aberration in the eye, an effect that is
closely associated with the McCollough effect (McCollough, 1965). Moreover, the neural visual system
adapts to prismatic distortions, contrast or blur (Webster, Georgeson, &
Webster, 2002). Adaptation to blurred images
can also improve letter acuity (Mon-Williams et al., 1998).
A practical example is the adaptation to the optical
distortions present in power progressive lenses widely used to correct
presbyopia. Although these lenses suffer for a large amount of aberrations
(Villegas & Artal, 2003), mainly
astigmatism, most subjects adapt and wear those lenses comfortably.
Moreover, in the clinical practice, astigmatism is
routinely under-corrected because patients usually do not tolerate a full
correction. This is probably another example of the neural visual system not
being adapted to the correction that provides the best optical quality
objectively.
We have not yet measured the rate at which the visual
system can adapt to changes in its monochromatic aberrations. If the adaptation
to chromatic aberrations is a valid guide, then the process could be expected to
take short periods of time, even a few minutes. However, adaptation processes in
the visual system occur at many different rates, and only direct measurements
will settle this issue. With the AO system, we tried to reverse or induce this
adaptation by exposing subjects to a modified aberration pattern. With exposures
of several (up to five) minutes, we were not able to see any significant change
in the blur matching results. This suggests that a long time scale is probably
involved; we do not know yet if it is in the range of days, weeks, or months.
Aberrations in the eye are dynamic by nature (Hofer et
al., 2001b). They change with pupil
diameter and accommodation during normal viewing (Artal, Fernández, &
Manzanera, 2002). This creates an apparent
paradox: If the retinal PSF is not stable over time, how can sluggish neural
adaptation maintain a clear perceptual world? A possible explanation is that
changes in pupil diameter and defocus (accommodation) preserve most of the shape
features characteristics of a particular PSF, allowing the brain a coarse
adaptation. In a recent experiment (Artal, Manzanera, & Williams, 2003), we confirmed that some shape features
in the PSFs remained stable under most normal conditions.
Another possibility is that the brain can
simultaneously accept a number of different PSFs, as long as it has sufficient
experience with each. There is some evidence in support of the latter view, and
studies have shown that the brain can maintain multiple adaptive states
simultaneously, switching rapidly between them as when spectacles are donned and
removed (Peterson & Peterson, 1938).
Another important practical aspect is the amount of
aberration that the neural system can “compensate.” All subjects who
participated in the study had normal (small) levels of aberrations. Although it
is well known that a large amount of aberrations degrades vision, it is possible
that in those eyes, the neural system also is adapted to slightly improve
vision. From the results of our blur matching experiment, it is not completely
clear what is the nature of the visual improvement produced by the neural
adaptation. While the increases of subjective sharpness would surely benefit
tasks such as letter recognition (i.e., visual acuity), identifying the effect
in other types of visual tests (e.g., contrast sensitivity) would require
additional experiments.
We demonstrated that the neural visual system adapts to
the particular eye’s monochromatic aberrations. In addition to the
fundamental nature of our finding, this adaptation phenomenon also may have
important implications for vision correction. In particular, in the area of
wavefront guided customized refractive surgery or customized contact lenses,
this effect will reduce the immediate benefit for the patient of attempts to
produce diffraction-limited eyes. If the brain is adapted to a particular
aberration pattern, when this is changed by the surgery or contact lens, the
neural compensation will remain adjusted to the first aberration pattern for
some time. The importance of this will depend on the time required to reverse
the previous adaptation.
This research was supported in part by grants from the
Spanish Ministerio de Ciencia y Tecnología (BFM-2001-0391) to PA, NIH
Grants EY0436 and EY0139, and the National Science Foundation Science and
Technology Center for Adaptive Optics, managed by the University of California
at Santa Cruz under cooperative agreement No. AST-9876783, to DRW.
Commercial relationships: none.
Corresponding author: Pablo Artal.
Address: Laboratorio de Optica, Departamento de Física, Universidad de Murcia, Campus de Espinardo, (Edificio C), Murcia, Spain.
ANSI Z136.1 American National
Standard for the Safe Use of Lasers (1993). Orlando: Laser Institute of
America.
Artal, P., Fernández,
E. J., & Manzanera, S. (2002). Are optical aberrations during accommodation
a significant problem for refractive surgery?
Journal of Refractive Surgery, 18,
S563-S566. [ PubMed]
Artal, P., Guirao, A., Berrio,
E., & Williams, D. R. (2001). Compensation of corneal aberrations by
internal optics in the human eye. Journal of
Vision, 1(1), 1-8, http://journalofvision.org/1/1/1,
doi:10.1167/1.1.1. [ PubMed]
[ Article]
Artal, P., Manzanera, S.,
& Williams, D. R. (2003). How stable is the shape of the ocular point spread
function during normal viewing [Abstract] ?
Journal of Vision,
3(12), 30a, http://journalofvision.org/3/12/30/,
doi: 10.1167/3.12.30. [ Abstract]
Born, M., & Wolf, E. (1985).
Principles of optics. New York:
Pergamon.
Fernández, E. J.,
Iglesias, I., & Artal P. (2001). Closed-loop adaptive optics in the human
eye. Optics Letters, 26, 746-748.
Held, R. (1980). The
rediscovery of adaptability in the visual system: Effects of extrinsic and
intrinsic chromatic dispersion. In C. S. Harris (Ed.),
Visual coding and adaptability (pp.
69-94). Hillsdale, NJ: Lawrence Erlbaum.
Helmholtz, H. von (1881).
Popular lectures on scientific subjects:
Second series. London: Longmans, Green.
Hofer, H.
J., Artal, P., Singer, B., Aragón, J. L., & Williams, D. R. (2001a).
Dynamics of the eye’s wave aberration.
Journal of the Optical Society of America
A, 18, 497-506. [ PubMed]
Hofer, H., Chen, L., Yoon, G.
Y., Singer, B., Yamauchi, Y., & Williams, D. R. (2001b). Improvement in
retinal image quality with dynamic correction of the eye’s aberrations.
Optics Express, 8, 631-643.
Hubbin, N., & Noethe, L.
(1993). What is adaptive optics? Science,
262, 1345-1484.
Liang,
J., Grimm, B., Goelz, S., & Bille, J. F. (1994). Objective measurement of
the wavefront aberration of the human eye with the use of a Hartmann-Shack
sensor. Journal of the Optical Society of
America A, 11, 1949-1957.
Liang, J., & Williams,
D. R. (1997). Aberrations and retinal image quality of the normal human eye.
Journal of the Optical Society of America
A, 14, 2873-2883. [ PubMed]
Liang, J., Williams, D. R.,
& Miller, D. T. (1997). Supernormal vision and high-resolution retinal
imaging through adaptive optics. Journal of
the Optical Society of America A,
14, 2884-2892. [ PubMed]
McCollough, C. (1965). Color
adaptation of edge-detectors in the human visual system.
Science, 149, 1115-1116.
Mon-Williams, M., Tresilian,
J. R., Strang, N. C., Kochhar, P., & Wann, J. P. (1998). Improving vision:
Neural compensation for optical defocus.
Proceedings of the Royal Society of London B,
265, 71-77. [ PubMed]
Noll, R. J. (1976). Zernike
polynomials and atmospheric turbulence.
Journal of the Optical Society of America,
66, 207-211.
Packer, O., Diller, L. C.,
Verweij, J., Lee, B. B., Pokorny, J., & Williams, D. R., et al. (2001).
Characterization and use of a digital light projector for vision research.
Vision Research, 41, 4, 427-439. [ PubMed]
Peterson, J., & Peterson,
J. K. (1938). Does practice with inverting lenses make vision normal?
Psychological Monograph, 50, 12-37.
Prieto, P. M.,
Vargas-Martín, F., Goelz, S., & Artal, P. (2000). Analysis of the
performance of the Hartmann-Shack sensor in the human eye.
Journal of the Optical Society of America A,
17, 1388-1398. [ PubMed]
Roorda, A., & Williams, D. R.
(1999). The arrangement of the three cone classes in the living human eye.
Nature, 397, 520-522. [ PubMed]
Vargas-Martin F., Prieto P.,
& Artal P. (1998). Correction of the aberrations in the human eye with
liquid crystal spatial light modulators: Limits to the performance.
Journal of the Optical Society of America A,
15, 2552-2562. [ PubMed]
Villegas, E. A., & Artal, P. (2003). Spatially resolved wavefront aberrations of ophthalmic progressive-power lenses in normal viewing conditions. Optometry and Vision Science, 80,
106-114. [ PubMed]
Webster, M. A., Georgeson, M.
A., & Webster, S. M (2002). Neural adjustments to image
blur. Nature Neuroscience, 5, 839-849.
[ PubMed]
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