(Investigative Ophthalmology and Visual Science. 1999;40:3084-3090.)
© 1999
by The Association for Research in Vision and Ophthalmology, Inc.
Optic Nerve and Peripapillary Choroidal Microvasculature of the Rat Eye
Kazuhisa Sugiyama,
Zhao-Bin Gu,
Chizuru Kawase,
Tetsuya Yamamoto and
Yoshiaki Kitazawa
From the Department of Ophthalmology, Gifu University School of Medicine, Gifu, Japan.
 |
Abstract
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PURPOSE. To investigate the three-dimensional microvascular anatomy of the optic
nerve and peripapillary choroid in the rat eye.
METHODS. Gross vascular anatomy of the posterior eye segment of Wistar rats was
studied in serial microsections with a light microscope. The optic
nerve and peripapillary choroidal vessels were sequentially
microdissected, using methylmethacrylate corrosion microvascular
castings, and were examined with a scanning electron microscope to
determine the three-dimensional relationships of the vessels.
RESULTS. The posterior ciliary artery traveled along the inferior side of the
optic nerve sheath, directly entered the optic nerve head, and divided
into three branches: the central retinal artery and medial and lateral
long posterior ciliary arteries, which provided several short branches
to the choroid. The optic nerve head vasculature was consistently
nourished by a recurrent arteriole from the central retinal artery and
an arteriole from the choroidal artery at the peripapillary choroid.
The central retinal vein flowed into a venous anastomosis along the
optic disc border of the peripapillary choroid. Capillaries within the
optic nerve drained into the central retinal vein, the marginal venous
anastomosis of the peripapillary choroid, and the pial veins, all of
which flowed into the posterior ciliary veins along the optic nerve
sheath.
CONCLUSIONS. The findings illustrate vascular anatomic differences in optic nerve
and peripapillary choroidal microcirculation between rat and human. In
rats, the peripapillary choroid plays a significant role in both blood
supply and venous drainage of the optic nerve head. The central retinal
artery also contributes to the optic nerve head
circulation.
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Introduction
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The microvascular supply and drainage of the optic nerve and
peripapillary choroid have been studied in rabbit,1
nonhuman primate,2
and human3
by
physiologically controlled microvascular corrosion
castings,4
which permanently replicate the anatomic
condition of vascular beds under the physiologic conditions at the time
of plastic injection. Such a plastic model of the ocular vasculature
appears to preserve the vascular tone and has been used to demonstrate
statistically significant differences in vascular calibers between eyes
treated with adrenergic drugs and contralateral control eyes in
rabbits.4
5
6
Our previous work has shown that the main
arterial blood supply to the anterior optic nerve is from its periphery
(branches of short posterior ciliary arteries) and that the central
retinal vein provides the sole venous drainage route of optic nerve
circulation in nonhuman primates2
and human.3
Our past results suggest that the direction of the optic nerve blood
flow is from the peripheral blood supply toward the central venous
drainage.
Recently, detailed methods to increase intraocular pressure in
laboratory rats have been published,7
8
9
10
and rats have
been extensively used as a readily available animal model of
glau-coma7
8
9
10
11
and as an optic nerve axotomy or crush
model for neuroprotection studies with relevance to
glaucoma.12
13
14
15
16
17
18
19
However, ocular hypertension or optic
nerve injury may cause ischemia or disturbance of the microcirculation
in the optic nerve head, retina, or choroid in addition to direct nerve
damage. Detailing the three-dimensional microvascular anatomy of normal
laboratory rats is crucial to establishing rat models for glaucoma or
optic nerve injury. Researchers should also know the vascular anatomic
differences between rat and human before extrapolating results from rat
models to human conditions. We first examined serial microsections of
rat optic nerve by light microscopy to determine the anatomic position
of various blood vessels with respect to the surrounding structures
because surrounding tissue had been removed from the vascular castings.
Then, we investigated the three-dimensional microvascular anatomy of
the optic nerve and peripapillary choroid using scanning electron
microscopy of microvascular castings from laboratory rats. The results
provide a basis for understanding the microcirculation of the rat optic
nerve head region and the vascular anatomic differences between rat and
human eyes.
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Materials and Methods
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All our experimental procedures conformed to the ARVO Statement
for the Use of Animals in Ophthalmic and Vision Research. We used 45
Wistar rats 9 weeks after birth, each weighing 250 to 300 g, which
had no signs of ocular inflammation by slit lamp examination.
Enucleated eyes (10 eyes of five rats) were placed in a mixture of
freshly prepared 2% paraformaldehyde, 2% glutaraldehyde, and 0.1 M
phosphate buffer (pH 7.2). After 5 minutes, a slit was made 1 to 2 mm
posterior to the limbus with a number 11 scalpel blade, and the eyes
were returned to the fixative. The eyes were processed through graded
solutions of ethanol and xylene and then embedded in paraffin. For
histologic study, 3-µm serial cross-sections (five eyes) and
longitudinal sections (five eyes) of the optic nerve were obtained and
stained with hematoxylin and eosin. These serial sections were observed
through a photomicroscope (Axioskop, Carl Zeiss, Oberkochen, Germany).
We modified luminal microvascular corrosion casting techniques
previously described for use in rabbits and rats4
20
and
examined the microvasculature of the optic nerve and posterior segment
of the eyes in 40 rats. In brief, the castings of the ocular
vasculature were obtained under controlled physiologic conditions. Rats
were anesthetized by intraperitoneal injection of ketamine (75 mg/kg
body weight) and xylazine (7.5 mg/kg body weight). Methylmethacrylate
injection media (Batson’s 17; Polyscience, Warrington, PA) was
modified to reduce the viscosity to 11 centipoise (cp), a level only
slightly higher than that of heparinized blood (8 cp). To avoid
ischemia, the respiratory system was preserved until the moment of the
plastic injection. The plastic was injected into the superior
circulation through the ascending aorta from a cannula inserted into
the abdominal aorta. Immediately before starting the injection, we
opened the thorax and cut the right atrium as a drainage route of the
superior circulation. The plastic was injected at physiologic
temperature (37°C), with a slightly higher perfusion pressure
(150–180 mm Hg) than physiologic blood pressure. The pressure was
monitored with a transducer (AP-641G; Nihon Kohden, Tokyo, Japan). The
injection pressure was maintained for 5 to 10 minutes, until the
plastic began to polymerize. Two hours after injection, the eyes were
enucleated, stored overnight in 10% buffered formalin to complete the
polymerization, and corroded in 6 M potassium hydroxide at 50°C for 2
or 3 days. The plastic vascular castings thus created were carefully
rinsed with a mild flow of distilled water using a pipette and then
dehydrated in graded solutions of ethanol. Finally, the ocular castings
were desiccated by t-butyl alcohol freeze-drying. Whole
globe vascular castings were hemisected at the equator, and the
posterior segments were mounted on stubs, sputter coated with
gold-palladium (JFC-1500, ION sputtering device; JEOL, Tokyo, Japan),
and examined with a scanning electron microscope (JSM-5410LV; JEOL).
Despite the controlled conditions that consistently produce uniform
filling of the ciliary body and choroidal vasculature, complete
methacrylate filling is more variable in the optic nerve and retinal
vasculature. Because of these difficulties, we examined only the
castings (26 eyes of 20 rats) in which the arteriolar network of the
optic nerve was completely filled.
The optic nerve castings were viewed from both the anterior and
posterior aspects of the globe. With an insect-dissection needle and
microscissors, the optic nerve and peripapillary choroidal vessels were
sequentially removed to determine specific three-dimensional
relationships of the vessels. This technique was previously described
using ocular castings of rabbit1
21
and nonhuman
primate.2
After removal of the superficial layers, the
castings were recoated with gold-palladium to obtain electron
microscopic scans of deeper, previously inaccessible layers.
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Results
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Gross Vascular Anatomy
The cross-sectional histology of the optic nerve and posterior
view of the ocular castings revealed that one artery existed in the
thick dura of the optic nerve and traveled along the inferior side of
optic nerve without giving off any branches (Figs. 1
, 2
). This artery directly entered the inferior side of the optic nerve
head and provided two long posterior ciliary arteries in the sclera
along the horizontal meridian on the medial and lateral sides of the
choroid (Figs. 2
, 3
). The choroid of the posterior segment, including peripapillary
choroid, was nourished by several short branches from long posterior
ciliary arteries (Fig. 2)
. Careful microdissection revealed that the
artery finally became a central retinal artery after branching into the
two long posterior ciliary arteries (Figs. 3
, 4
). This artery supplied the entire uveal vasculature including the
retinal vasculature; therefore, this artery should be called the
posterior ciliary artery.
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Figure 1. Cross-section of retrolaminar optic nerve showing that the posterior
ciliary artery (PCA) and the posterior ciliary veins (PCVs) exist in
the inferior side of the thick optic nerve sheath (dura). ON, optic
nerve; M, extraocular muscle.
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Figure 2. Posterior view of the ocular casting shows that the posterior ciliary
artery (PCA) travels along the inferior side of the optic nerve, enters
the optic nerve head, and branches off into two long posterior ciliary
arteries (LPCAs) along the horizontal meridian. Two posterior ciliary
veins (PCVs) run along the posterior ciliary artery. ON, optic nerve;
CH, choroid. Bar, 500 µm
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Figure 3. Cross-section of the optic nerve head in the scleral level showing the
posterior ciliary artery divides into three branches: the central
retinal artery (CRA), and the medial and lateral long posterior ciliary
arteries (LPCAs). ON, optic nerve; LC, lamina cribrosa; CRV, central
retinal vein; PCV, posterior ciliary vein; Sc, sclera.
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Figure 4. After microdissection of part of choroidal vasculature, the venous
circle, and the optic nerve capillaries, the posterior view of the
casting demonstrates that the posterior ciliary artery (PCA) becomes
the central retinal artery (CRA), and the central retinal vein (CRV)
empties into the marginal venous ring (arrow) which
flows into the posterior ciliary vein (PCV). CH, choroid, Re, retina.
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Optic Nerve Head and Peripapillary Choroidal Microvasculature
The surrounding tissue had been removed from the casting;
therefore, histologic methods were used to determine the anatomic
relationship of the various blood vessels to surrounding structures.
Figure 5 depicts the longitudinal section of the rat anterior optic nerve,
revealing a bottleneck configuration. The rat optic nerve head has
laminar beams (Fig. 3)
identical with the primate lamina cribrosa as
described in a previous study.9
In the present study, we
divided the rat anterior optic nerve into four anatomic regions in
accordance with the recognized regions of the primate optic nerve
head.22
23
The most anterior zone of the optic nerve is
the superficial nerve fiber layer region. Immediately posterior to this
is the prelaminar region, which lies adjacent to the peripapillary
choroid. More posteriorly, the laminar region is continuous with the
sclera and is composed of lamina cribrosa. Finally, the retrolaminar
region lies posterior to the lamina cribrosa.
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Figure 5. The longitudinal section of the anterior optic nerve showing the
bottleneck configuration. S, surface nerve fiber layer; P, prelaminar
region; L, laminar region; R, retrolaminar region; Re, retina; CH,
choroid; Sc, sclera.
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The anterior view of the posterior segment of the ocular casting showed
that the central retinal artery supplied the retinal vasculature and
the surface nerve fiber layer of the optic nerve head (Fig. 6)
. The lateral view of the posterior segment of the ocular casting
showed the optic nerve head and peripapillary choroid (Fig. 7A
). We carefully microdissected part of the choroidal vasculature to
observe the prelaminar and laminar regions of the optic nerve head
(Fig. 7B)
. One branch of the central retinal artery consistently
provided a recurrent arteriole to the prelaminar, laminar, and
retrolaminar regions of the optic nerve head. At the peripapillary
choroid, a short branch (choroidal artery) from the long posterior
ciliary artery also gave off an arteriole to the prelaminar, laminar,
and retrolaminar regions of the optic nerve head. The capillary network
within the optic nerve was continuous from the retrolaminar region to
the retinal vasculature.
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Figure 6. The anterior view of the casting showing the arterial supply
(arrows) of the surface nerve fiber layer of the optic
disc. CRA, central retinal artery; CRV, central retinal vein. Bar, 100
µm.
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Figure 7. (A) From the lateral view of the casting, the
arrows indicate that the capillary network of the optic
nerve head flows into the marginal venous anastomosis (MVA).
(B) Part of the peripapillary choroidal vasculature was
removed. The small arrows indicate the branch of the
central retinal artery (CRA). The large arrows denote
the branch from the choroidal artery (CA). The double
arrows show that capillaries of the prelaminar region drain
into the central retinal vein (CRV). ON, optic nerve; CH, choroid; CA,
choroidal artery; Re, retinal vasculature. Bar, 100 µm.
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The posterior view of the ocular casting and cross-sectional histology
of the laminar region of the optic nerve head demonstrated that in
addition to the vortex system, another independent venous system of the
posterior choroid formed an incomplete venous circle around the optic
nerve head in the sclera (Figs. 8A 8B
). This venous circle drained into the posterior ciliary veins
parallel to the posterior ciliary artery in the inferior side of optic
nerve dura (Fig. 8A
; see also Figs. 1
2
). After removing some
choroidal vasculature, the venous circle, and optic nerve capillaries,
we were able to observe that the central retinal vein emptied into a
marginal venous anastomosis along the optic disc border of the
peripapillary choroid (Fig. 4)
. The marginal venous anastomosis finally
flowed into the posterior ciliary veins. Capillaries in the retinal
vasculature, surface nerve fiber layer, and prelaminar region of the
optic nerve head drained into the central retinal vein (Fig. 7B)
.
Capillaries within the prelaminar and laminar regions of the optic
nerve head drained into the marginal venous anastomosis of the
peripapillary choroid (Fig. 7A)
. In the laminar and retrolaminar
regions, most of the venous drainage was to pial veins, which flowed
into the posterior ciliary veins (Fig. 9)
.
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Figure 8. (A) Posterior view of the casting, with
arrows indicating the incomplete venous circle, which
drains into the posterior ciliary vein (PCV). (B)
Cross-section of optic nerve head in the scleral level showing the
incomplete venous circle around the optic nerve head
(arrows). CH, choroid; CRA, central retinal artery, CRV,
central retinal vein; PCA, posterior ciliary artery; LPCA, long
posterior ciliary artery; CA, choroidal artery; ON, optic nerve; LC,
lamina cribrosa; Sc, sclera. Bar, (A) 500 µm;
(B) 100 µm.
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Figure 9. The lateral view of the retrolaminar region of the optic nerve casting
demonstrates that capillaries of the optic nerve flow into the pial
venous network (arrows), which drains into the posterior
ciliary vein (PCV). PCA, posterior ciliary artery. Bar, 100 µm.
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Discussion
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Although rat posterior choroidal vasculature and posterior ciliary
vein have been described,24
this is the first overall
in-depth study of the optic nerve head and peripapillary choroidal
microvasculature of the rat eye. Because the methylmethacrylate filling
of the rat optic nerve vessels is more variable than the filling of the
optic nerve vessels in larger mammals, making a complete microvascular
casting of the optic nerve in the rat eye is very difficult. The
vascular castings of a rat optic nerve are much smaller than those from
rabbit, nonhuman primate, or human, making them weak and fragile. Even
when complete microvascular filling of rat optic nerve and retinal
vasculature is obtained using previously described
methods,1
2
3
4
5
6
20
21
rinsing with water and air drying could
destroy detail at the capillary level of complicated vascular castings,
although such destruction has not occurred in larger ocular
castings.1
2
3
4
5
6
In the present study, we carefully rinsed
the ocular castings with a mild flow of distilled water, by means of a
pipette. The castings were then dehydrated in graded solutions of
ethanol and desiccated by t-butyl alcohol
freeze-drying.25
These procedures enabled us to preserve
fragile castings. Additionally, it is extremely important to reduce the
viscosity of the casting media to replicate the complete optic nerve
microvasculature without insufficient filling or extravasation of
media. A modified methylmethacrylate with a viscosity of 11 cp was
used. This plastic medium was only slightly more viscous than
heparinized venous blood (8 cp) at the time of injection.4
Maintaining a physiologic temperature of the injection media and
keeping the respiratory system functioning until the moment of plastic
injection were also crucial to preserving vascular tone.
The precise anatomic relationships of the vessels that perfuse and
drain the optic nerve and peripapillary choroidal regions are difficult
to study because of their inaccessibility and the complexity of their
angioarchitecture. When methylmethacrylate luminal corrosion castings
are viewed with a scanning electron microscope, only surface vessels
are clearly visible. However, the use of a sequential microdissection
technique1
2
21
allowed detailed inspection of the inner
three-dimensional angioarchitecture of the anterior optic nerve and
peripapillary choroid.
Rat posterior ocular vasculature has a unique and simple
angioarchitecture compared with that of rabbit or primates. In rabbit
or primates, medial and lateral posterior ciliary arteries are present
apart from the optic nerve1
2
; however, the present study
shows that in rats, the posterior ciliary artery travels in the
inferior side of the optic nerve sheath toward the optic nerve head.
The posterior ciliary artery is derived from the inferior branch of the
ophthalmic artery in the rat eye.26
This study also
confirmed that the posterior ciliary artery gives off two long
posterior ciliary arteries and a central retinal artery at the optic
nerve head region, as previously described.24
The two long
posterior ciliary arteries provide several branches to the choroidal
vasculature and finally supply the iris and ciliary body
vasculature.20
27
28
Unlike in the primate eye, in the rat
eye two long posterior ciliary arteries supply the entire uveal
vasculature, and there is no short posterior ciliary artery. These
anatomic findings suggest that the rat posterior ciliary artery is a
terminal artery to the eyeball and that optic nerve axotomy inevitably
cuts the posterior ciliary artery and produces ischemia in the overall
ocular vasculature. Crushing of the optic nerve, depending on the force
involved, must cause occlusion or stenosis of the posterior ciliary
artery. Clipping of the optic nerve is dependent on instant and limited
force to result in mechanical damage to the axons without prolonged
ischemia to the entire ocular vasculature. In the primate eye, axotomy
or crushing at proper sites on the anterior optic nerve may not cause
ischemia in retinal or choroidal vasculature, because the posterior
ciliary arteries are separated from the anterior optic nerve, and the
central retinal artery and vein enter the optic nerve 3 to 5 mm behind
the globe.2
3
29
30
31
32
33
The present study clearly demonstrates that the central retinal artery
in the rat eye contributes to the optic nerve blood supply, not only in
the surface nerve fiber layer but also in the prelaminar, laminar, and
retrolaminar regions. In contrast, the central retinal artery in human
and nonhuman primates primarily supplies blood to the surface nerve
fiber layer with a limited contribution to the retrolaminar
region.2
3
29
Moreover, in the human eye, the pial and
centripetal branches from circle of Zinn–Haller (derived from short
posterior ciliary arteries) and direct branches from posterior ciliary
arteries are the principal supply to the prelaminar, laminar, and
retrolaminar regions.3
30
31
32
33
Our results showed that the
circle of Zinn–Haller was absent in the rat eye and an arteriolar
branch from a choroidal artery at the peripapillary choroid supplied
the prelaminar, laminar, and retrolaminar regions along with an
arteriolar branch from the central retinal artery. Only two arterioles
perfused the rat optic nerve head capillaries, suggesting that the rat
optic nerve head may be more vulnerable to ischemia than that of the
human.
The present study elucidates that the venous drainage of the rat optic
nerve head is through a marginal venous anastomosis of the
peripapillary choroid in the prelaminar and laminar regions and through
pial veins in the laminar and retrolaminar regions. The central retinal
vein collected venous tributaries from the retina, surface nerve fiber
layer, and prelaminar regions of the optic nerve head, then drained
into the marginal venous anastomosis of the peripapillary choroid and
the posterior ciliary veins. These anatomic findings demonstrate that
the marginal venous anastomosis of the peripapillary choroid plays a
significant role in the venous drainage of the optic nerve head and the
retinal vasculature. The present study and a previous report indicate
that posterior ciliary veins as well as vortex veins provide venous
drainage of the posterior choroid in the rat.24
Finally, this study shows that the central retinal artery and the
choroidal artery of the peripapillary choroid present a double arterial
vascular supply to the rat optic nerve head. The venous outflow of the
optic nerve head is by means of the marginal venous anastomosis of the
peripapillary choroid and pial veins. Thus, the peripapillary choroid
plays a key role in the rat optic nerve head microcirculation. The
understanding of the vascular anatomic differences between rat and
human eyes enables the proper interpretation of results from rat
experimental models for extrapolation to humans.
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Acknowledgements
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The authors thank the Biological Department, R & D Division,
Menicon Co., Ltd., Japan for providing scanning electron microscopic
facilities and Aoi Nishizawa for her technical assistance.
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Footnotes
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Supported in part by Grant-in-Aid 08457461 from The Ministry of Education of Japan, Tokyo.
Submitted for publication May 28, 1999; accepted July 21, 1999.
Commercial relationships policy: N.
Corresponding author: Kazuhisa Sugiyama, Department of Ophthalmology,
Gifu University School of Medicine, 40 Tsukasa-machi, Gifu-shi,
500-8705, Japan. E-mail: ksugi-gif{at}umin.u-tokyo.ac.jp
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Abstract
Introduction
