Fundamentals of Presbyopia: visual processing and binocularity in its transformation
Rozanova et al. Eye and Vision
Fundamentals of Presbyopia: visual processing and binocularity in its transformation
Olga I. Rozanova 1
Andrey G. Shchuko 0 1
Tatyana S. Mischenko 1
0 Irkutsk State Medical University , Irkutsk, Russian Federation
1 Irkutsk branch of S. Fyodorov Eye Microsurgery Federal State Institution , Irkutsk, Russian Federation
Background: The accommodation has considerable interactions with the pupil response, vergence response and binocularity. The transformation of visual reception processing and the changes of the binocular cooperation during the presbyopia development are still poorly studied. So, the regularities of visual system violation in the presbyopia formation need to be characterized. This study aims to reveal the transformation of visual reception processing and to determine the role of disturbances in binocular interactions in presbyopia formation. Methods: This study included 60 people with emmetropic refraction, uncorrected distance visual acuity 1.0 or higher (decimal scale), normal color perception, without concomitant ophthalmopathology. The first group consisted of 30 people (from 18 to 27 years old) without presbyopia, the second cohort comprised 30 patients (from 45 to 55 years old) with presbyopia. The eyeball anatomy and optics were evaluated using ultrasound biomicroscopy, aberrometry, and pupillometry. The functional state of the visual system was investigated under monocular and binocular conditions. The registration of the disparate fusional reflex limits was performed by the original technic using a diploptic device which facilitated investigation of the binocular interaction under natural conditions without the accommodation response, but with the different vergence load. The disparate fusional reflex was analyzed using the proximal and distal fusion borders, and the convergence and divergence fusion borders. The calculation of the area of binocularity field was 2 performed in cm . Results: The presbyopia formation is characterized by a change in an intraocular anatomy, optics, visual processing, and binocularity. The processes of binocular interaction inhibition make a significant contribution to the misalignment of the visual perception. The modification of the proximal, distal and convergence fusion borders was determined. It was revealed that 87% of the presbyopic patients had binocularity shortage, whereas the reduction of binocularity field area in extreme grade was seen in 6% of cases. Conclusions: The presbyopia formation is accompanied by a significant reorganization of the visual system activity and by the creation of the new visual processing interactions. These data may be useful in presbyopia surgery.
Presbyopia; Binocularity; Visual processing; Visual reception
According to the International Classification of Diseases
(ICD-10, version: 2010) presbyopia belongs to the class
of refraction and accommodation disturbance and is
slow, age-related and irreversible accommodation
decline. Currently, over 1.7 billion people in the world are
afflicted with presbyopia [
]. The problem appears in
people at the age of 40 – 45 years, which is the period of
maximal professional and creative activity involving
analyses of a significant volume of visual information [
The problem of presbyopia correction is an actual task,
but in spite of the active introduction of advanced methods,
the question about adequate presbyopia correction remains
open and unsettled [
]. For the compensation of
accommodation deficit, different variants of a multifocal optical
system creation have been described [
But the creation of a multifocal monocular optical
system or anisometropic binocular optical system is closely
associated with the adaptation processes, which are very
complicated in some patients. The multifocal monocular
optical system does not have any physiological analogs
]. Regardless of the multifocal IOL model, there
is always a proportion of patients who complain of the
visual dysphotopsia as blurring, misting, “holographic”
view, 3D - view. In 5% of cases, this dysphotopsia
syndrome becomes rigid and is an indication for IOL
]. The reasons for the visual
dysphotopsia are not clear enough. The explantation of multifocal
intraocular lens is debated as an “army method of
refractive surgery” [
] and is about 3 to 10% according to
the data by different authors [
Most of the presbyopia theories consider the
intraocular changes purely. The presbyopia is mainly viewed as
an accommodation decrease determined by the
reduction of lenticular elasticity and changing lens suspension
]. At the same time, the
accommodative response is a part of the near synkinetic reflex. The
accommodation has significant interactions with the
pupil response, vergence response, and binocularity.
However, based on the theory of functional systems, the
loss of useful component in the body’s activity is
accompanied by the measures to compensate or to adapt for it
]. Therefore, the reduction of the accommodative
response that underlies the presbyopia development must
be inevitably accompanied by the imbalance among the
components of the near synkinetic reflex. How does the
accommodation decrease influence the ocular motor
forces which are responsible for the stable constant visual
image? This problem has not been solved yet.
The changes of the binocular cooperation during the
presbyopia development are still poorly studied.
According to our previous studies, there is some deficit of
binocular cooperation in age-related accommodation
]. Besides, the aging-induced accommodation
decrease is strongly linked with other physiological aging
processes and the degradational changes of sensory
neurons. The normal aging is accompanied by the visual
acuity decrease, contrast sensibility decrease, color
perception changing, stereoacuity decrease [
age-related reduction of stereovision is marginally
correlated with fusional ability decrease . But what
remains unclear is the role of binocular disorders among
mechanisms underlying presbyopia pathogenesis.
Therefore, comprehending the binocular interaction changes
in people with presbyopia is a critical issue, and the
regularities of visual system violation in the presbyopia
formation need to be characterized.
The purpose of this study is to examine the transformation
of visual reception processing and to determine the role of
binocular interactions disturbance in presbyopia formation.
The study adhered to the tenets of Helsinki Declaration
and was approved by the Institution Research and Ethics
Committee (protocol number 8/13 from 25/11/2013).
All patients were adequately informed and signed a
consent form. Of the 60 people examined, the first group
consisted of 30 people (from 18 to 27 years old) without
presbyopia, and the second group comprised 30 patients
(from 45 to 55 years old) with presbyopia.
The criteria for inclusion in this study comprise the
presence of emmetropic refraction (i.e., the spherical
equivalent of cycloplegic measurements from +0.25 D to
−0.25 D), uncorrected distance visual acuity of each eye
1.0 (decimal scale) or higher, normal color perception,
ophthalmopathology absence. All patients of the second
group complained of the insufficient near vision, and
they made use of the glasses.
Considering that binocularity correlates the
heterophoria value and interpupillary distance [
exclusion criteria comprised a heterophoria degree greater
than five prism diopter, the pupillary distance less than
62 mm and greater than 64 mm.
All patients had a full ophthalmological examination
including the evaluation of 80 parameters of eye anatomy,
visual processing, and binocularity.
Assessment of the eye anatomy and the physiological optics
The refractive error was the average spherical equivalent of
five cycloplegic measurements taken with an autorefractor/
keratometer (KR8800, Topcon, Japan). All cycloplegic
measurements were made 25 min after the administration of
1% tropicamide (2 drops during 5 min interval twice).
The other investigations were performed 7-10 days later.
The amplitude of accommodation (AA) was measured
using a minus lens method. The subjects were asked to
fixate N8 target at a distance of 40 cm. Then minus lenses
were introduced in 0.25 D steps until the patient reported
the first sustained blur that could not be cleared by the
further conscious effort. This procedure was done for each
eye first monocularly and then binocularly. The total AA
was estimated as the endpoint minus lens which was
possible to see the target at 40 cm under binocular
conditions. The AA measurement in people with presbyopia
was done using the near addition lens.
The axial length, lens thickness, anterior chamber
(AC) measurements were made with the help of an
ultrasound biometer (AL-3000, Tomey, Japan). An
average of three measurements for each parameter was used.
Ultrasound biomicroscopy (UBM) measurements were
made using HiScan 2000 (Optikon, Italy), and UBM was
done in the supine position as described by C. Pavlin
and F. Foster [
]. Images from the iris root to the pars
plicata zone were obtained in 12 o’clock direction. The
ciliary body thickness in cross section and the length of
anterior portion Zinn’s ligament were examined. The
ocular wavefront aberration across a 3 mm zone in the
pupil and the pupil diameter (under photopic and
mesopic conditions) were obtained using the principle of
automated retinoscopy (OPD-Scan, NIDEK, Japan). The
anterior chamber volume, iris and lens configuration,
corneal aberrations, lens light transmission, were fixed
using Pentacam (Oculus Optikgeräte GmbH, Germany).
Assessment of visual processing under monocular conditions
The distance visual acuity and the near visual acuity
were measured with logical geometric scale Bailey-Lovie
(logMAR). Other examinations included evaluation of
the contrast sensitivity at spatial frequencies 3, 6, 12,
18 cycles per degree (CSV-10000E, VectorVision, USA),
the threshold of light sensitivity (EP3000, Tomey, Japan),
the flicker fusion threshold, the amplitude and implicit
time of maximal electric retinal response, and the
amplitude and implicit time of visual evoked potentials
(EP1000, Tomey, Japan).
For this purpose, the data reflecting the different levels
of binocular interaction were systematized. These
include the near physiological diplopia, the stereovision
test Lang I&II, and the binocularity field (spatial limits
of disparate fusional reflex).
To induce the physiological diplopia, each patient was
asked to look into the far distance (5 m). Then a
nearlying target (in the distance 10 cm, i.e., not in the
horopter curve) was presented. The presence (yes/no) of
double virtual objects was fixed.
In the case of physiological diplopia, the registration
of the disparate fusional reflex limits was performed.
For this, a diploptic device (AVIS 01, Krasnogvardeec,
Russia) was used, which facilitated investigation of the
binocular interaction under natural conditions without
the accommodation response, but with the different
vergence load [
]. The first point of the
measurement is 40 cm. Then the double targets were
moved inwards until the virtual stereo image was
observed (Fig. 1). It was a point of binocularity without
The change in the distance between the centers of the
double near lying tests (p) and the distance from the
eyes to the targets (n) while maintaining of the virtual
binocular image perception makes it possible to define
the fusional reflex limits in space. Then the targets were
moved increasingly inward and outward to force the
vergence response (Fig. 2). There were some points of
maximum convergence and divergence. The patient reported
all the visual images which were recorded.
The disparate fusional reflex was analyzed using the
1. The proximal fusion border (PF) and distal fusion
border (DF) were determined while the double
targets were approaching and moving away (Fig. 2).
The difference between these parameters
corresponds to the length of the binocularity field.
2. The convergence fusion border (CF) and the
divergence fusion border (DivF) were determined
with the help of the decrease and the increase of the
distance between the double targets (the point of the
measurement is 40 cm from the eyes). The
Fig. 1 The perception of virtual binocular visual image
difference between these parameters corresponds to
the width of the binocularity field.
3. Finally, we performed the calculation of the
binocularity field area (A) in cm2 (Fig. 3).
All data were analyzed with a spreadsheet application
(Statistica ver. 8.0; StatSoft Inc., USA). The data were
represented as the mean value ± standard deviation
(Mean ± SD). The Shapiro-Wilk test was used for
assessing of normality distribution. The statistical differences
in measured values were analyzed using a t-test. The
critical level of significance (p) upon the examination of
statistical hypotheses was 0.05. The comparison analysis,
the Pearson correlation analysis, and the logistic
regression models were done. The Pearson correlation
coefficient with absolute values equal to or greater than 0.7
with p < 0.001 was accepted as the close relation. The
discriminant function analysis (DFA) was used for the
selection of the analytes that maximally discriminated
the studied groups. The DFA was built in a step-wise
manner after direct standardization. The final
discriminatory power of each analyte was characterized by a
partial Wilk’s Lambda coefficient; 1.0 (no discriminatory
power) to 0.0 (perfect discriminatory power). The
Mahalanobis distance D2 between centroid values for each
group was measured.
The baseline features of the study population were
summarized in Table 1. The mean patient age was 22.3 ±
3.2 years in the first group, and 52.4 ± 2.2 years in the
second group. The groups did not differ in gender,
spherical refraction equivalent, eye globe axial length,
oculomotor status. In the first (control) group, the mean
accommodation amplitude was 6.93 ± 1.12 D (minimum
5.75 D, maximum 10.0 D). All patients with presbyopia
had a decreased accommodation: the mean
accommodation amplitude was 1.99 ± 0.89 D (minimum 0.5 D,
maximum 4.0 D).
Intraocular anatomy and optics
The presbyopia formation is characterized by a change in
an intraocular anatomy. Significant differences were
detected in the anterior-posterior size of the lens – from
3.73 ± 0.23 to 4.41 ± 0.21 (p = 0.0001). The optical density
(light transmission coefficient) of the lens increased in the
nuclear area from 15.5 ± 1.2 to 26.6 ± 3.4% (p = 0.0001),
and in the cortical layers – from 9.1 ± 0.9 to 10.8 ± 1.3%
(p = 0.03). The change of the intraocular anatomy was
expressed as: the decrease of the ciliary body thickness (in
the inner top projection) from 0.82 ± 0.10 to 0.63 ±
0.11 mm (p = 0.001), the increase of the distance between
the trabecula and the ciliary processes from 0.79 ± 0.10 to
1.02 ± 0.11 mm (p = 0.001), and the shortage of the front
portion Zinn ligament length from 1.23 ± 0.31 to 1.04 ±
0.26 mm (p = 0.002).
The variation of both static and dynamic components
of the optical physiological system was established in the
eyes of presbyopic patients. This was evidenced by a
significant increase of the total root mean square wavefront
errors (from 0.13 ± 0.04 to 0.17 ± 0.05 μm in pupil
diameter 3 mm, p = 0.0001) and the corneal root mean square
wavefront aberrations. In patients with presbyopia, an
increase in the Zernike coefficients of the corneal
spherical aberration Z40 from 0.17 ± 0.05 to 0.23 ± 0.06 μm
(p = 0.0001) was observed. Also, a significant decrease of
the pupil excursion was found. The photopic pupil
diameter decreased from 3.81 ± 0.76 to 3.35 ± 0.78 mm
(p = 0.0001) whereas the mesopic pupil diameter
decreased from 6.47 ± 0.56 to 5.50 ± 0.94 mm (p = 0.0001).
Monocular visual characteristics
In the next step, a comprehensive study of the sensory
activity of the visual system was carried out. The patients
with presbyopia had a decrease not only in
accommodation amplitude and uncorrected near visual acuity but also
in the most of the visual reception parameters (Table 2).
A significant decrease of the contrast sensitivity in low
and high spatial frequency ranges, the average values of
the b-wave ERG maximum amplitude, the flicker fusion
threshold and an increase in the a-wave and b-wave ERG
maximum latency were found in patients with presbyopia.
The change in the perception Lang stereo tests was not
A study of binocular cooperation showed an inhibition
of the near physiological diplopia in 20% of the patients
There were multiple changes. These include a
significant distortion of the binocular interaction zone with
the reduction of total binocularity area, shift in the space
towards the near focal point, and the fusion
neutralization in the convergence zone. The changes in
the proximal, distal and convergence fusion borders
were determined (Table 3).
The regressions between disparate fusion reflex limits
and accommodation amplitude are shown in Fig. 4. In the
first (control) group, the mean area of binocularity field
was 365.6 ± 45.1 cm2 (minimum 280 cm2, maximum
Table 3 Comparisons of Fusion Reflex Characteristics in Study
Groups (M ± SD)
Proximal fusion border, cm
Distal fusion border, cm
Convergence fusion border,
Divergence fusion border,
Length of binocularity
Width of binocularity field,
5.23 ± 1.58
90.05 ± 7.35
24.83 ± 6.14
18.90 ± 6.85
69.20 ± 12.21
30.31 ± 6.91
Area of binocularity field, cm2 365.60 ± 45.10 174.40 ± 87.70 0.0001
456 cm2). All patients with presbyopia had a decreased
fusion ability with the mean area of binocularity field at
174.4 ± 87.7 cm2 (minimum 48 cm2, maximum 385 cm2).
The regression between binocularity field area and
accommodation amplitude is shown in Fig. 5.
It is interesting to note that 77% patients with
presbyopia had binocular suppression in some grade, while 6%
of patients had extreme decrease in the binocularity field
area (Fig. 6).
The multivariate kinds of statistical analyses were used
for the understanding of the vision reception
transformation in presbyopia formation.
A Pearson correlation analysis of visual system
parameters was made. The comparison of the
correlation Pleiades (correlations with P-value equal or less
than 0.001) within Control and Presbyopia Groups
revealed a reduction in the strength of most
relationships. The correlation Pleiades are represented in
Fig. 7, where the positive correlations were shown as
red arrows and the negative correlations as blue ones.
It is evident that young people without presbyopia have
a much larger number of interdependencies between
structural and functional indicators of the visual system
than in patients with presbyopia. In young people, 25 close
relationships were established, but in patients with
presbyopia, there were only 6 such relationships. Instead of
destroyed relationships, there was a new correlation
between the width of the binocularity field and the implicit
time of visual evoked potentials (r = −0,7; p = 0.001).
In the forward stepwise discriminant analysis, eight
indices were selected for 100% discrimination of studied
groups. The matrix of most informative variables for
discrimination is represented in Table 4.
The separation between groups is not only due to the
accommodation state but also to some other significant
changes in the structural and functional parameters. The
indicators of the tolerance show that all features are orthogonal
and their contributions to the separation do not overlap.
The results of the discriminant analysis showed that
the fusional ability made the high contribution in the
separation of two groups. At the same time, the
contribution of other sensory parameters in the division was
This research aimed to describe the transformation of
the visual system functional organization during the
presbyopia formation. The results of the study broaden
our understanding of the presbyopia mechanisms. It was
found that the structural and functional state of the
visual system in middle-aged patients with presbyopia is
significantly different from young people.
The reduction of the accommodation is significant, but
not the only sign of visual transformation in patients with
presbyopia. The increase in the number of optical errors
despite the pupil tour decrease worsens the conditions for
the formation of the retinal image. The formation of
presbyopia is accompanied by the misalignment of visual
sensory processing with varying degrees of functional defect
severity (Fig. 8).
The decrease of the contrast sensitivity at frequencies
below four cpd reflects the amplification of the visual
system internal noise (at the level of receptive fields).
Whereas the contrast sensitivity at high spatial
frequencies is limited with optical parameters (aberrations,
diffraction phenomenon or “sampling noise” of the visual
image). The patients with presbyopia had the signs both
internal noise and sampling noise (noise of signal
processing). The change of temporal parameters of the
visual system at middle age patients indicates the initial
deficiency of interactions between neurons and the signs
of the central nervous system fatigue. These changes can
be viewed as signs of aging.
The new data about binocular visual system activity
was established. The processes of binocular interaction
inhibition make a significant contribution to the
misalignment of the visual perception. The area of
binocularity field, where the disparate fusion is possible, was
reduced twice. The variation of proximal fusion limit
and a decrease of the binocularity field area are more
serious than the variation in other sensor parameters.
On the one hand, this phenomenon may be a result of
age-related changes in the neurons. On the other hand,
the inhibition process can be motivated by the desire to
liberate the body from the excessive flow of the visual
information under the shortage of accommodation. The
process of efferent synthesis is an active selection of
information aimed to release biologically significant flows
and is formed in such integral efferent excitations that
are required by the body in a given situation.
Our results correspond to the relevant studies.
GrangerDonetti revealed that majority of presbyopes had disorders
of binocular cooperation in some degree due to a decrease
in the slow convergence [
]. The accommodation
amplitude decrease is accompanied by the increase of vergence
movement latency, the reduction of the vergence fusion
and the speed of the fast vergence [
In this study, we analyzed data in people with the
visual system that mostly meets the ideal. Even in this
situation, 77% of presbyopia patients had binocularity
shortage. In 6% of cases, there were profound signs of
the deep inhibition processes. These data are likely
useful in presbyopia surgery. The analysis of the surgery
results using monovision or multifocal optical strategies in
patients with an extreme deficit of binocularity is the
next step of research.
The presbyopia formation is accompanied by a significant
reorganization of the visual system activity and the
creation of the new visual processing interactions. It was
revealed that 77% of the presbyopia patients had
binocularity shortage. The overall reduction of binocularity field
area in extreme grade was seen in 6% of cases. These data
may have implications for presbyopia surgery.
The authors are grateful to Isay M. Mikhalevich and Vladimir V. Malyshev for
their help and advice.
The authors have no financial support and sponsorship.
OIR made substantial contributions to conception and design, analysis, and
interpretation of data, total statistical analysis, AGS revised it critically for
important intellectual content and supervision, TSM participated in data
acquisition, drafted the manuscript. All authors read and approved the final
The authors have no proprietary or commercial interests in the medical
devices that are involved in this manuscript.
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