Glaucoma

Correlation Between the Ganglion Cell-Inner Plexiform

Layer Thickness Measured With Cirrus HD-OCT and
Macular Visual Field Sensitivity Measured With
Microperimetry
Shino Sato, Kazuyuki Hirooka, Tetsuya Baba, Kaori Tenkumo, Eri Nitta, and Fumio Shiraga
Department of Ophthalmology, Kagawa University Faculty of Medicine, Miki, Kagawa, Japan

Correspondence: Kazuyuki Hirooka,

Department of Ophthalmology, Kagawa University Faculty of Medicine,
1750-1 Ikenobe, Miki, Kagawa 7610793, Japan;
kazuyk@med.kagawa-u.ac.jp.
Submitted: October 19, 2012
Accepted: March 30, 2013
Citation: Sato S, Hirooka K, Baba T,
Tenkumo K, Nitta E, Shiraga F. Correlation between the ganglion cell-inner
plexiform layer thickness measured
with Cirrus HD-OCT and macular field
visual sensitivity measured with microperimetry. Invest Ophthalmol Vis
Sci. 2013;54:30463051. DOI: 10.
1167/iovs.12-11173

PURPOSE. To evaluate relationships between the macular visual field (VF) mean sensitivity and
the ganglion cell and inner plexiform layer (GCA) thicknesses.
METHODS. Seventy-one glaucoma patients and 29 healthy subjects were included in this crosssectional study. At each visit, GCA thicknesses were measured by Cirrus HD-OCT and static
threshold perimetry was performed using Macular Integrity Assessment (MAIA). The
relationship between the VF sensitivity and GCA thickness was examined globally, and in
the superior hemiretina, inferior hemiretina, and six VF sectors with both VF and optical
coherence tomography (OCT) in retinal view. Regression analysis was used to investigate the
relationship between the GCA thickness and macular sensitivity.
RESULTS. Macular VF sensitivity (dB) and GCA thickness relationships were statistically
significant in each sector (R 0.3650.706, all P < 0.001). The highest correlation observed
was between the inferotemporal average mean sensitivity and the inferotemporal average
GCA thickness (R 0.706) with both VF and OCT in retinal view. Strength of the structure
function relationship for each of the corresponding inferior sectors was higher than those for
the corresponding superior sectors. The strength of the structurefunction relationship of the
temporal sector was higher than that of the nasal sector.
CONCLUSIONS. GCA thickness measured by Cirrus HD-OCT showed statistically significant
structurefunction associations with central VF. Inferotemporal central VF had the strongest
association.
Keywords: optical coherence tomography, visual field, microperimetry

dvances of optical coherence tomography (OCT) have

enabled assessment of retinal ganglion cell (RGC) axons by
measuring the thickness of the peripapillary retinal nerve fiber
layer (RNFL) and the macular area. More recent advances in
segmentation algorithms have it made possible to use OCT to
visualize and measure individual retinal layers in the macular
region.13 RTVue-100 OCT (Optovue, Inc., Fremont, CA)
incorporates a ganglion cell complex (GCC) scan mode that
measures the inner macular retinal layer thickness from the
internal limiting membrane to the inner plexiform layer (IPL),
which is composed of ganglion cell axons, cell bodies, and
dendrites. Previous studies have shown that the macular GCC
thickness measurements derived from GCC scan data are
significantly lower in glaucomatous eyes with visual field (VF)
defects than in healthy eyes, and have a good glaucoma
discriminating power that is comparable to that of the RNFL.47
The thickness of the RGC or RGC IPL (GCA: ganglion cell
analysis) in the macula has also been measured by OCT.2,8
Mwanza et al.9,10 recently showed that the Cirrus HD-OCT GCA
algorithm (Carl Zeiss Meditec, Dublin, CA) can successfully
detect and measure the inner macular layers (the GCA; an area
that contains the ganglion cell layer and the IPL) with excellent
intervisit reproducibility.

Microperimetry, which is known as fundus controlled

perimetry or fundus perimetry, assesses retinal sensitivity
during the direct examination of the ocular fundus. Microperimetry data are independent of eye movements and exactly
related to the stimulated area. In addition, VF sensitivity can
also be measured by microperimetry with improved spatial
localization.
A number of studies have used spectral-domain OCT to
focus on the relationship between structural and functional
damage as a way to improve our ability to detect the presence
and progression of glaucomatous damage. Results of these
studies have demonstrated there are high correlations between
the global VF sensitivity and the peripapillary RNFL/GCC
thickness.5,11,12 The macular VF, including the central vision, is
very important if a glaucoma patient is to enjoy normal daily
life. Therefore, preservation of the macular VF is the key
concern in glaucoma management. Wang et al.2 found that local
thickness of the RGC IPL (GCA) could be obtained from
frequency-domain OCT scans, with these measurements
showing qualitative agreement with local VF sensitivity. Raza
et al.8 recently showed a strong relationship between losses in
standard automated perimetry (SAP) sensitivity and decreases
in local RGC IPL thicknesses (GCA).

Copyright 2013 The Association for Research in Vision and Ophthalmology, Inc.
www.iovs.org j ISSN: 1552-5783

3046

IOVS j April 2013 j Vol. 54 j No. 4 j 3047

Relationship Between Macular VF and GCA

The purpose of the current study was to evaluate the
correlation between the GCA thickness and the local VF
sensitivity obtained when using microperimetry, Macular
Integrity Assessment (MAIA; CenterVue, Padova, Italy), in each
sector of the macula.

MATERIALS

AND

METHODS

All patients were examined at Kagawa University Hospital from

November 2011 through May 2012. At each visit, the GCA
algorithm was used to detect the macular inner structure
thickness, while MAIA was used to determine the static
threshold perimetry. All eligible subjects received a detailed
explanation of the study and signed an informed consent form
in accordance with the principles embodied in the Declaration
of Helsinki. The study protocol was approved by the
institutional review board of the Kagawa University Faculty
of Medicine. Healthy control subjects were either subjects
attending the outpatients clinics, spouses and friends of the
recruited patients, or volunteers from the hospital staff.
All subjects underwent a complete ophthalmic examination
that included visual acuity testing with refraction, IOP,
gonioscopy examinations, and dilated fundus examination
with stereoscopic biomicroscopy of the optic nerve head
using slit lamp and indirect ophthalmoscopy. To be included in
the study, all subjects had to have a best-corrected visual acuity
of 20/40 or better, a spherical error within a range between
4.0 and 6.0 diopters (D), a cylinder within 6 2.0 D, and
open angles (grade 3 and 4 according to the Shaffer grading
system). Exclusion criteria included a history of any kind of
retinal pathology or neurologic disease, retinal laser procedure,
or either retinal or intraocular surgery. One eye in each subject
was randomly chosen for inclusion in the study. To be enrolled
as a control in the study, subjects had to have an IOP less than
or equal to 21 mm Hg, no history of retinal pathology, and a
normal visual field. Glaucomatous eyes were defined as eyes
exhibiting structural glaucomatous changes (vertical cup-disc
asymmetry between fellow eyes of 0.2, a cup-to-disc ratio of
0.6, and neuroretinal rim narrowing, notches, localized
pallor, or RNFL defects with glaucomatous VF loss in the
corresponding hemifield). A glaucomatous VF was defined as a
glaucoma hemifield test (GHT) outside normal limits on at least
two consecutive baseline tests and the presence of at least
three contiguous test points within the same hemifield on the
pattern deviation plot at P less than 1%, with at least one at P
less than 0.5% excluding points on the edge of the field or
those directly above and below the blind spot.

Cirrus HD-OCT Imaging

All eyes were scanned by the Cirrus HD-OCT system. Only
good-quality scans were used for the analyses. To be included,
scans had to have a signal strength less than or equal to 6, be
without RNFL discontinuity or misalignment, involuntary
saccade or blinking artifacts, and show an absence of algorithm
segmentation failure during a careful visual inspection. The GC
analysis algorithm was used to automatically measure the
macular GCA thickness. Software version 6.0 of the GCA
algorithm was used to process the data in this study, as it was
able to detect and measure the thickness of the macular
ganglion cell-inner plexiform layer within a 14.13 mm2
elliptical annulus area centered on the fovea. The protocol
carries out 200 horizontal B-scans, which are comprised of 200
A-scans per B-scan that are performed 1024 times within a
cube measuring 6 3 6 3 2 mm. These scans were designed to
allow analysis of the retinal topography.8,9 The GCA algorithm
is able to process data from either of the three-dimensional

(3D) volume scans performed by the Cirrus HD-OCT. Both of

these scan patterns cover the same physical field of view,
namely an area that is 6 3 6 3 2 mm. However, the
dimensionality of the image data is either 512 3 128 3 1024
or 200 3 200 3 1024. The input image data are initially
segmented using the existing Cirrus inner limiting membrane
(ILM) and RPE segmentation algorithms in order to create a
region of interest that lies within the intraretinal layers.9,10 The
algorithm identifies the RNFL layer, the GCA layer (an area that
ranges from the outer boundary of the RNFL to the outer
boundary of the IPL, and that includes both the RGC layer and
the IPL), and the outer retinal layer. The segmentation
procedure operates in three dimensions and uses a graphbased algorithm to identify each layer. A detailed description of
how the algorithm operates has been previously presented in
detail.9,10 There are nine thicknesses measured within the
annular area that is centered on the fovea. These include the
average, superior average, inferior average, and six sectoral
(superotemporal, superior, superonasal, inferotemporal, inferior, inferonasal) values of the respective layers.

Microperimetry Examinations
In all subjects, MAIA was used to measure the retinal
sensitivity. MAIA was performed in a dim room without any
dilation of the pupil. The following parameters were used in
the current study: a 68-stimuli grid covering the central 108 of
the retina, a 4 to 2 threshold strategy, a fixation target that
consisted of a red circle with a 18 diameter, stimulus size
Goldmann III, background luminance set at 4 apostilb (asb),
maximum luminance of 1000 asb, and a stimulus dynamic
range of 36 dB. Use of the MAIA device made it possible to
determine which of the fixation stabilities were stable. Only
stable fixation tests were included in the analysis.

Mapping Structure to Function

For analysis of functional measurements, VF sensitivity was
obtained for each subject. According to the criteria described
earlier, 8 of 108 eyes that qualified for initial inclusion were
excluded. Seven of these eyes had a signal strength less than 6,
while one eye showed unstable fixation. Therefore, a total of
100 eyes were included in the final analysis. When comparing
the GCA thickness to the local loss in VF sensitivity, it is
important that the displacement of the RGCs in the macula be
taken into consideration.13 The average location of the RGCs
associated with each MAIA test point was approximated using
equations that were derived from the histologic analysis-based
work of Drasdo et al.14 Figure 1 shows the location of the
visual field MAIA test points, while Figure 2A shows the
location after adjusting for the RGC displacement. Structurefunction relationships were determined from each of the six
sectors with both VF and OCT in retinal view (Fig. 2B). Since
fundus perimetry data are exactly related to the stimulated
area, functional measurements of MAIA were correlated with
the structural measurements of the OCT in the same hemifield.

Statistical Analysis
To determine the association between the local VF mean
sensitivity and the relative GCA thickness, we based this study
on previous work that related the SAP sensitivity to peripapillary RNFL thickness1517 or RGC IPL thickness (GCA) in the
macula.8 Briefly, the assumptions for this model were as
follows: the measured GCA thickness R consists of two
components, the thickness S, which is due to portions of the
IPL and RGC layer (GCA) that is affected by glaucoma, and the
residual B, which includes portions of the IPL and RGC layer

Relationship Between Macular VF and GCA

IOVS j April 2013 j Vol. 54 j No. 4 j 3048

FIGURE 1. Detection of macular sensitivity. Right eye fundus image of a 50-year-old patient with primary open-angle glaucoma (POAG). Figure
shows microperimetry results with differential light threshold values color-coded from 0 to 36 dB.

(GCA) not affected by glaucoma. These areas may include glial

cells, blood vessels, bipolar cell axons, and amacrine cell
projections. Thus, overall R S B. As the MAIA field
sensitivity changes, the value of S will decrease, while B will
remain constant. As the VF sensitivity decreases, the signal
portion S of the local GCA thickness R will decrease linearly
when the VF sensitivity is expressed in linear units. Thus, R
(S0  B) T B for T less than or equal to 1.0, where S0 is the
median of the control GCA thickness at a particular eccentricity, T is the relative sensitivity (defined as 100.1D), and D is the
VF sensitivity minus the mean value of healthy subjects. T
equals 1.0 when there is no loss (0 dB difference from normal)

and approaches 0 when there are large losses in the sensitivity.

The variable B was calculated for each zone as the median of
the GCA data when the local VF sensitivities were less than 20
dB.
Correlations of the GCA thickness with the corresponding
VF mean sensitivity were examined by using Spearman rank
order correlations. Differences between the control and
glaucoma groups were assessed by an independent Students
t-test and the v2 test for categorical parameters. All statistical
values are presented as the mean 6 SD, with P values less than
0.05 considered to be statistically significant. Statistical
analyses were performed using SPSS version 19.0 (IBM, New

FIGURE 2. Representative example showing the six sectors of the ganglion cell analyzer thickness and the adjustment for retinal ganglion cell
displacement. (A) The 10 to 2 VF displaced points corresponding to the RGC locations based on a model derived from histologic analysis.5 (B) GCA
thickness areas were divided into six sectors, with the corresponding VF regions then obtained using MAIA.

IOVS j April 2013 j Vol. 54 j No. 4 j 3049

Relationship Between Macular VF and GCA

TABLE 1. Clinical Characteristics of the Study Population

TABLE 3. Macular Sensitivity for the Average, Superior Average,

Inferior Average, and in Each of the Six Sectors

Glaucoma

Normal

Age, y
Sex (M/F)
Diagnosis

62.5 6 11.0
40/31

64.3 6 12.2
17/12

0.71
0.83

POAG
NTG
EG

32
37
2

Mean Sensitivity, dB

Refraction (D)

1.6 6 2.3

0.7 6 1.9

0.10

NTG, normal-tension glaucoma; EG, exfoliation glaucoma; M, male;

F, female; D, diopter.

York, NY). Comparisons of the strength structurefunction

association were evaluated by tests of equality of dependent
correlation coefficients.

RESULTS
A total of 71 glaucoma patients (32 POAG, 37 normal-tension,
and 2 exfoliative) and 29 healthy subjects were enrolled in the
study. The demographic characteristics are presented in Table
1. Since the healthy control participants were selected based
on age- and refractive error-matching, there was no significant
difference noted in the mean age between the healthy subjects
and glaucoma patients. Based on the standard VF severity
grading scale,18 the grade of the disease in the glaucomatous
eyes of the 71 patients ranged from early to moderate, with 29
(41%) classified as early, 24 (34%) classified as moderate, and
18 (25%) classified as severe.
Table 2 lists the GCA thickness, while Table 3 presents the
macular sensitivity. GCA thickness and macular sensitivity were
significantly different between the glaucoma and healthy
subject groups.
Figure 3 shows the structurefunction relationship between the GCA thickness and the corresponding VF mean
sensitivity with both OCT and VF in retinal view. To check the
goodness of fit, we calculated the number of points falling
outside the 95% confidence boundary. For the global GCA
thicknessVF mean sensitivity, seven eyes fell outside of the
95% confidence boundary. Although the difference in the
structurefunction relationship was not significant among six
sectors, the highest Spearman correlation coefficient was
0.706 in the inferotemporal sector. Strength of the structure
function relationship of each of the corresponding inferior
sectors (R 0.5460.706) were higher than those of the

TABLE 2. GCA Thickness for the Average, Superior Average, Inferior

Average, and in Each of the Six Sectors
GCA Thickness, lm
Glaucoma
Average
Superior hemifield
Inferior hemifield
Superotemporal
Superior
Superonasal
Inferotemporal
Inferior
Inferonasal

65.1
67.1
63.1
63.9
67.5
70.9
59.6
62.0
67.7

6
6
6
6
6
6
6
6
6

7.7
9.2
8.0
9.8
9.6
10.0
9.0
8.4
9.2

Normal

6
6
6
6
6
6
6
6
6

<0.01
<0.01
<0.01
<0.01
<0.01
<0.01
<0.01
<0.01
<0.01

79.8
80.8
78.8
79.6
81.0
81.7
80.4
76.6
79.4

5.2
5.5
5.5
5.1
6.5
6.3
6.1
5.9
5.7

Glaucoma
Average
Superior hemifield
Inferior hemifield
Superotemporal
Superior
Superonasal
Inferotemporal
Inferior
Inferonasal

21.4
23.4
19.4
21.4
23.6
25.1
17.5
16.8
24.2

6
6
6
6
6
6
6
6
6

6.3
6.0
8.4
8.3
6.8
5.6
10.3
11.1
6.5

Normal

6
6
6
6
6
6
6
6
6

<0.01
<0.01
<0.01
<0.01
0.02
0.07
<0.01
<0.01
0.02

26.9
26.9
26.9
26.9
26.8
27.1
27.0
26.4
27.1

1.5
1.6
1.5
1.7
2.0
1.7
1.7
1.6
1.8

corresponding superior sectors (R 0.3650.601). In

addition, the strength of the structurefunction relationship
of the temporal sector was higher than that of the nasal sector
(inferonasal [R 0.546] versus inferotemporal [R 0.706] [P
0.02], superonasal [R 0.365] versus superotemporal [R
0.601] [P 0.002]).

DISCUSSION
The pathology of glaucoma is characterized by the death of
RGCs and their axons. Although there is substantial individual
variability, the average retina contains 1.07 million RGCs, with
approximately 50% of the RGCs located within 4.5 mm of the
fovea.19,20 It has been demonstrated in humans that the RGC
loss is evident around the fovea during the early stages of the
disease.21 Therefore, we selected the central macular VF as the
local functional target in the current study and then assessed its
structurefunction relationship by using the GCA thickness.
Although SAP is able to show the functioning of individual
retinal locations in the macula, reliable test results can be
difficult to obtain because of unstable fixation in some cases.
When using an autotracking system, MAIA is able to
automatically record the fixation behavior during the test
while the autotracking system makes it possible to adjust the
stimulus points to predefined retinal positions and perform
reliable field testing, even in eyes with unstable fixation.
Because of these advantages, this study used MAIA to measure
the macular VF sensitivity.
The current study examined structurefunction relationships in smaller regions, which to the best of our knowledge,
has not been previously investigated. The determination of
which region has a stronger structurefunction association has
clinical implications, as use of the stronger region could
provide better detection and follow up in glaucoma patients
who may present with an early stage of macular VF defects.
Thus, our current results indicate the importance of studying
the relationship patterns in smaller regions. The strength of the
structurefunction relationship is related to the individual
anatomy and its variation in the subject, the stage of glaucoma
present in the study sample, the VF scale, and the regression
model used. During the previous examinations of the
correlations between the VF sensitivity and the early glaucomatous stages, healthy individuals, and the glaucoma suspect
eyes, the correlations were shown to be weaker than those
observed in moderate-to-severe glaucoma.22,23 The reason for
this is because the range of VF is narrow in healthy and
glaucoma suspect eyes. Thus, the strength of a structure
function relationship may be dependent upon both the actual
retinal and VF areas in which the association is assessed and

Relationship Between Macular VF and GCA

IOVS j April 2013 j Vol. 54 j No. 4 j 3050

FIGURE 3. Scatters plots showing the association between the Cirrus HD-OCT thickness parameters and the corresponding retinal sensitivity. (A)
Average thickness of the GCA versus the macular mean sensitivity. (B) Superior average thickness of the GCA versus the superior macular mean
sensitivity. (C) Inferior average thickness of the GCA versus the inferior macular mean sensitivity. (D) Superotemporal thickness of the GCA versus
the superotemporal mean sensitivity. (E) Superior thickness of the GCA versus the superior mean sensitivity. (F) Superonasal thickness of the GCA
versus the superonasal mean sensitivity. (G) Inferotemporal thickness of the GCA versus the inferotemporal mean sensitivity. (H) Inferior thickness
of the GCA versus the inferior mean sensitivity. (I) Inferonasal thickness of the GCA versus the inferonasal mean sensitivity. Spearman correlation
coefficients, *P < 0.001.

the specific imaging device that is used in the study. In

addition, histologic studies in human24,25 and monkey eyes26
have shown that in the central retina, there are more ganglion
cells in the nasal and superior sectors than in the temporal and
inferior sectors, respectively. These differences in the distribution of the ganglion cells might affect the strength of the
structurefunction relationship.
Raza et al.8 recently reported finding that the local RGC
IPL thickness (GCA) correlated well with the local sensitivity
loss obtained with the 10 to 2 SAP setting in the central 7.28 of
the 14 patients with glaucoma and in the 19 healthy subjects.
The differences between the current and previous study were
as follows: our study showed that the strength of the
correlation between the VF mean sensitivity and the GCA
thickness varied within the macular region. In addition, our
study measured the VF sensitivity with microperimetry in an
attempt to improve the spatial localization. We also examined a
total of 100 eyes, as it was hoped this larger sample size would
result in a greater statistical power.
In the past, relationships between RNFL losses and VF
defects have been studied using different theoretical curves to
fit the data.1517,27,28 Results have shown that a complete loss

in sensitivity does not result in a RNFL thickness of zero, but

instead, is actually associated with a finite RNFL thickness. In
the early stage of glaucoma, the decline in RNFL thickness is
rapid, and there is a lag in the visual sensitivity loss. However,
as the glaucoma becomes severe, RNFL thicknesses reach a
base level beyond which only the visual sensitivity declines.
For these reasons, we decided to evaluate the structure
function relationship using the model proposed by Hood et
al.15,16 Our results showed that their linear model fit the
structurefunction data quite well.
With regard to potential limitations, we were not able to
observe any overall age effect, the number of subjects in this
study was relatively small; however, a further study with a
larger number of subjects should be able to address this issue.
We also did not notice any obvious difference in the structurefunction agreement for patients with POAG, normal-tension
glaucoma, or exfoliation glaucoma. Additional studies that
more closely examine the different types of glaucoma will need
to be undertaken.
In conclusion, although the GCA thickness measured by
Cirrus HD-OCT was significantly correlated with the macular
retinal sensitivity assessed by MAIA, the strength of the

IOVS j April 2013 j Vol. 54 j No. 4 j 3051

Relationship Between Macular VF and GCA

correlation varied from region to region. Combining GCA
thickness with macular VF sensitivity may provide a better
understanding of the amount of glaucomatous damage that
occurs in the macula region.

Acknowledgments
Disclosure: S. Sato, None; K. Hirooka, None; T. Baba, None; K.
Tenkumo, None; E. Nitta, None; F. Shiraga, None

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