International Ophthalmology 6, 85-93 (1983) 0165-5701830062-008501.80 [625432]

International Ophthalmology 6, 85-93 (1983) 0165-5701/83/0062-0085/$01.80
9 Dr W. Junk Publishers, The Hague. Printed in The Netherlands
Physiological anatomy of the choroidal vascular bed
Sohan Singh Hayreh
Iowa City, U.S.A.
Keywords: choroid, posterior ciliary artery, choriocapillaris, vortex vein, macula, circulation.
Abstract
Physiological anatomy of the choroidal vascular bed, based on the in vivo clinical and experimental fluorescein
fundus angiographic studies, is reviewed. These studies have demonstrated that the posterior ciliary arteries
(PCAs) and their branches right down to the terminal choroidal arterioles, the choriocapillaris, and the vortex
veins have a segmental distribution in the choroid.
Introduction
Extensive anatomical studies of the choroidal vas-
cular bed have been conducted, mostly by studying
casts prepared by the postmortem injection of a
variety of materials (2, 26, 27, 33-36) and recently
by studying casts by scanning electron microscopy
(24, 28, 29, 32). These studies have formed the basis
of the classical anatomical textbook description of
the choroidal vasculature. According to most of
these descriptions: 1. extensive anastomoses exist
between the various branches of all the short
posterior ciliary arteries (PCAs), so that occlusion
of one vessel ordinarily does not produce infarction
of the choroid; 2. the short PCAs anastomose with
the anterior ciliary arteries at the equator of the eye;
3. the choriocapillaris is arranged in one plane as a
single continuous layer of wide lumen capillaries
and they form a continuous anastomotic network
over the entire choroid; and 4. the uveal veins
communicate freely and the vortex veins (VVs) have
no segmental distribution. However, it is well-
known that inflammatory, metastatic, ischemic and
degenerative lesions in the choroid are usually
localized (5). Moreover, a numer of clinical and experimental observations reported in the literature
(18) suggest that the PCAs have a segmental supply
to the choroid. Wybar (35, 36), Ring & Fujino (26),
and Uyama et al. (32) even from their cast studies,
also concluded that these arteries were segmentally
arranged and that each branch supplied a localized
zone of the choroid. In view of these conflicting
observations and with the advent of fluorescein
angiography, which has enabled us to study not
only the blood flow but also the physiological
anatomy in vivo, we and a number of other workers
have investigated the choroidal vascular bed in vivo;
these studies have almost revolutionized our con-
cept of the choroidal vascular bed and helped to
explain the pathogeneses of some obscure fundus
lesions. The following account represents the state
of our present knowledge on the subject, based
mostly on our studies (12).
Anatomy of the posterior ciliary arteries (PCAs)
There is a good deal of confusion as to the nom-
enclature, number, origin and distribution of the
PCAs in man. I have described the subject in detail

86 S.S. Hayreh
elsewhere (6).
Number: The ophthalmic artery in man gives out
one (in 3%), two (in 48%), three (in 39%), four (in
8%), or five (in 2%) PCAs. When there are more
than three PCAs, the additional arteries are usually
small in size.
Nomenclature: I have designated the PCAs accor-
ding to their relation to the optic nerve near their
site of entry into the eyeball. They are called:
(a) Medial PCA: This lies medial to the optic
nerve and may be one (in about 70%) or two (in
about 30%) in number.
(b) Lateral PCA: This lies lateral to the optic
nerve, and there may be one (in about 75%)~ two (in
about 20%), or none (in about 3%).
(c) Superior PCA: This is seen in only 9% and
may be one (in 7%) or two (in 2%); these are usually
small in size.
The various PCAs run forward, divide into a large
number of small branches and pierce the sclera near
the optic nerve. Out of these branches of the PCAs,
one on the medial and another one on the lateral
side form the long PCAs, while the rest are called
the short PCAs. The number of short PCAs piercing
the sclera varies from about 10 to 20, depending
upon the number of times the PCAs have sub-
divided before reaching the sclera. From this ac-
count it is evident that there are three types of
PCAs:
1. Main PCAs: These arise from the ophthalmic
artery and are usually 2 to 3 (medial and lateral
PCAs).
2. Long PCAs: These are two in number – one
medial and the other lateral.
3. Short PCAs: These may be 10 to 20.
I want to stress very strongly that unless this
terminology is clearly understood and adhered to,
there may be tremendous confusion.
Distribution: The short PCAs supply the following:
(a) Choroid: as far as the equator.
(b) Retina: The choroid supplies the overlying
retina to a depth of about 130# including the retinal
pigment epithelium (RPE) and adjacent outer
layers of the retina up to the outer part of the inner
nuclear layer. If a cilio-retinal artery is present, then
the entire thickness of the retina is supplied in the
distribution of the cilio-retinal artery. (c) Anterior part of the optic nerve: The PCA
circulation is the main source of blood supply to the
optic nerve head and the adjacent retrolaminar part
of the optic nerve (7, 13, 14).
2. The long PCAs supply a sector of the choroid,
starting almost immediately from the point where it
joins the choroid temporal to the macular region
after having pierced the sclera, and extending for-
ward (11, 34). It also supplies the corresponding
segment of the anterior urea.
Physiological anatomy of the choroidal vascular bed
In vivo clinical and experimental fluorescein fundus
angiographic studies have clearly demonstrated
that the choroidal blood flow is segmental, almost
like that seen in the retinal vasculature. The findings
are described in detail elsewhere (12). The following
is a brief summary:
(a) The medial and lateral PCAs supply the
corresponding half of the choroid (Fig. 1) (12, 18).
In man the watershed zone between the medial and
lateral PCAs may be located anywhere between the
fovea and nasal border of the optic disc (Fig. 2), (15,
)
Fig. 1. Diagrammatic representation of distribution by various
temporal short posterior ciliary arteries (SPCAs) and their
watershed zone in posterior part of fundus. Dotted circle in
region of distribution of temporal SPCAs represents macular
region. Areas of supply by medial PCA and temporal long PCA
are also shown. [Reproduced from Hayreh (10)].

Fig. 2. Watershed zone between medial and lateral PCAs in
man. (a) Right eye, showing filling of medial PCA and lateral
PCA but watershed zone still not filled. (b) Left eye with lateral
PCA occlusion, showing no filling of temporal choroid and
temporal half of optic disc. (c) Left eye with medial PCA
occlusion, showing no filling of the optic disc and ehoroid nasal
to fovea with cilioretinaI artery occlusion. (d) Right eye with
medial PCA occlusion, showing no filling of nasal choroid and
nasal 3/4 of optic disc. (c) Diagrammatic representation of the
location of the watershed zone (shaded area). (Reproduced from
Hayreh, S.S.: (a) Brit, J~ Ophthal. 59: 631-648, 1975; (b) Brit. J.
Ophthal. 58: 955~63, 1974; (e, d) Inter. Ophthal. 1:9 18, 1978;
(e) Glaucoma, Thieme, Stuttgart, p. 129, 1978). L

88 S.S. Hayreh
A B C
Fig. 3. Fluorescein fundus angiograms of a rhesus monkey eye at the posterior pole.
A. The early arterial filling phase of the choriocapillaris, showing each lobule of the choriocapillaris (supplied by the terminal choroidal
arteriole) forming a big fluorescent spot. Each spot is surrounded by a polygonal unfilled zone, producing a mosaic pattern in the
choriocapillaris.
B. Peak arterial filling phase. Note the extraordinarily well-defined mosaic pattern, with each unit of the mosaic an independent entity,
and the isolated non-filling or slow filling of some of the lobules is clearly visible. It suggests that there is no communication between
adjacent lobules.
C. Venous phase of the choriocapillaris filling, showing a honeycomb pattern; the fluorescent pattern is reverse of that seen in A., ie., the
fluorescent areas are nonfluorescent and vice versa. [Reproduced from Hayreh (8)].
17) and this has been reported by others as well
(37). The position of the watershed zone is of great
clinical significance since it determines the extent of
involvement of the optic nerve head in acute ische-
mia through occlusion of one of the two main PCAs
(Fig. 2) (15, 17).
(b) The short PCAs: These supply segments of
the choroid extending radially from the posterior
pole to the equator (Fig. 1), and each segment
varies greatly in shape, size and location and has
irregular borders (10, 12). Smaller subdivisions of
the short PCAs supply still smaller segments of
irregular shape and size, having a geographic pat-
tern. Ultimately, each terminal choroidal arteriole
supplies a lobule of choriocapillaris. There may be a
marked spatial variation in the filling of the various
choroidal segments so that on fluorescein angio-
graphy well-defined geographical filling defects are commonly seen in the normal choroid (8); physiol-
ogical choroidal filling defects should not be con-
fused with pathological choroidal filling defects.
My criterion to differentiate normal from abnormal
filling defects in the choroid is to correlate the filling
Fig. 4. A three-dimensional schematic representation of the
choriocapillaris pattern. A = choroidal arteriole. V = choroidal
veins. [Reproduced from Hayreh (9)].

defects with the normal retinal vascular filling, i.e.,
if the choroidal filling defect disappears when the
major retinal veins start to fill, it is normal, but if it
is delayed then it is usually abnormal.
(c) The long PCAs: A detailed account of these
arteries is given elsewhere (11). These supply a
sector of the choroid extending radially and tem-
porally from the temporal border of the macular
region (Fig. 1).
(d) Choriocapillaris: I have given a detailed ac-
count of the choriocapillaris elsewhere (9). My fluor-
escein angiographic studies revealed that each ter-
minal choroidal arteriole supplies an independent
segment of choriocapillaris, with the arteriole join-
ing the segment in its center and the draining
venules lying around the periphery of this segment
(Fig. 3, 4) (9). This supports observations by other
authors on the vascular pattern in the choriocapil-
laris (4, 25, 31, 34) but contradicts those of Krey
(23) and Shimizu (28). Each lobule of the chorio-
capillaris is an independent unit (of a polygonal
shape in the posterior fundus), with no anastomosis
with the adjacent segments in vivo (Fig. 3). The
various segments are arranged like a mosaic, the
borders of the mosaic being formed by the venous
channels. The size of each lobule of the choriocapil-
laris varies, and in my studies has been found to be
usually about one-quarter of the disc diameter or
VORTEX VENOUS WATER-SHEDS
0.55 (0.:53-0.66) ram
m
m
I
\ N %~
w
I
Fig. 5. Diagrammatic representation of watershed zones of
vortex veins. F&X = fovea. M = macular region. OD = optic
disc. [Reproduced from Hayreh (10)]. Choroidal vascular anatomy 89
Fig. 6. A fundus photograph of an albino patient showing the
chorio-vaginal vein (arrow).
less. The choriocapillaris are most densely packed
at the posterior pole and progressively become less
densely arranged towards the periphery. Unlike the
retinal capillaries, the choriocapillaris exercise no
blood-barrier because their endothelial fenestra-
tions make them highly permeable.
(e) Vortex veins (VVs): Each VV drains the
corresponding segment of the iris, ciliary body, and
choroid. The four VVs could be compared to the
four main retinal branch veins. There are poor
communications between the adjacent VVs (19).
The watershed zones between the various VVs
therefore extend antero-posteriorly through the en-
tire length of the uveal tract (19) – a horizontal
watershed between the upper and lower VVs passes
through the optic disc and macular region, while a
vertical watershed between the temporal and nasal
VVs passes between the optic disc and macular
region (Fig. 5).
(f) Chorio-vaginal vein: In addition to the VV, in
some eyes a vein may be seen which passes from the
choroid through the sclera closely adjacent to the
optic nerve-head (Fig. 6), and drains into the
venous plexus of the pial sheath of the optic nerve
(3). The chorio-vaginal vein occurs more frequently
in highly myopic eyes than others (5).
(g) Choroidal anastomoses: The presence of in-

90 S.S. Hayreh
terarterial and arteriovenous anastomoses in the
choroid has been well-documented in all the post-
mortem injection studies; similarly, interarterial
anastomoses between the branches of the PCAs and
the anterior ciliarly arteries have been well demon-
strated in these studies. However, in eyes with
experimental or clinical acute occlusion of the
PCAs or their smaller divisions, there is no evidence
at all of the presence of such anastomoses (12). It is
possible that the intact nervous supply to the
potential anastomotic channels in the living eye
may prevent them from working as such, but in the
dead eye the neural control is absent and the
anastomoses readily fill with the injection material.
We have no convincing explanation yet for this
disparity between in vivo and in vitro observations.
The in vivo studies thus have indicated that the
PCAs and their branches, right down to the ter-
minal choroidal arterioles, the choriocapillaris, and
the VVs have a segmental distribution in the chor-
oid and that the PCAs and choroidal arteries are
end-arteries (12). The reason for the significant
disparity between the morbid anatomy (based on
study of the choroidal casts) and physiological
anatomy (based on fluorescein angiographic studies)
is that the former gives information about the
morphological channels only, while the latter shows
the pattern of actual blood flow in those channels.
It is the physiological anatomy which is of real
clinical significance.
Watershed or boundary zones in the choroidal
vascular bed
Since the arteries and the VVs in the choroid do not
anastomose with one another in vivo, the border
between the areas of supply of any two adjacent
vessels, from the main PCAs to the terminal ehor-
oidal arterioles, and the VVs, forms a watershed
zone. The watershed zones between the various
choroidal vessels are arranged as follows:
1. Main PCAs: The arrangement of watershed
zones between medial and lateral PCAs is described
above (Fig. 2).
2. Temporal short PCAs. The watershed zones
between them are arranged somewhat radially, radiating from the macular region, so that most of
these watershed zones meet in the macular region
(Fig. 1).
3. Between the PCAs and anterior ciliary arteries:
This is situated in the equatorial region.
4. ChoriocapiItaris. The watershed zones between
the various lobules of the choriocapillaris are usu-
ally arranged like a honeycomb (Fig. 3C).
5. Vortex veins: The arrangement of the watershed
zones between the VVs is described above (Fig. 5).
Submaeular choroid
Because of the well-known localized involvement of
the macular region in a large number of conditions,
a good deal of interest has centered on the sub-
macular choroid. I have discussed the subject at
length elsewhere (10, 12, 16). In spite of some claims
about the discovery of a special macular artery (22,
34), all the available evidence is against the exis-
tence of such an artery (24, 26, 28, 36). All the
temporal short PCAs enter the eyeball in the
macular region and each artery then radiates to-
wards the periphery, like the spokes of a wheel; each
one of the short PCAs in the macular region gives
branches to the submacular choriocapillaris, as was
also seen in the casts by Shimizu and Ujiie (29). In
the human eye, the sites of entry of the various short
PCAs are usually situated some distance away from
the center of the macular region, and each artery,
near its site of entry, gives recurrent centripetal
macular branches which together supply the macu-
lar region (Fig. 7). Each short PCA supplies a
segment of the choroid, with no anastomoses be-
tween adjacent segments. Most of the segments of
the choroid supplied by the temporal short PCAs
and their watershed zones meet in the macular
region (Fig. 1). Similarly, the four quadrants of the
uveal tract drained by the four VVs and their
watershed zones meet in the macular region (Fig. 5).
It has been consistently stated that the submacular
choroid has a more abundant arterial supply than
other parts of the choroid. This impression is based
essentially on the fact that the submacular choroid
is much thicker than elsewhere. This is because all
the temporal short PCAs pierce the sclera in the

Choroidal vascular anatomy 91
Fig. 7. Fluorescein fundus angiogram of a normal human eye, showing the sites of entry of the short PCAs and their course in the
choroid. Arrow marks the center of the macular region. Note that no artery lies in the center of the macular region. (Reproduced by the
kind courtesy of Dr. P. Amalric: Int. Ophthal. 6:149-153 (1983).)
macular region to join the choroid in the sub-
macular choroidal region, and are thus aggregated
together in this region. A mere increase in the
number of arteries in the submacular choroid does
not increase the blood supply and nutrition to that
area (t0, 36). Wybar (63) Ring & Fujino (26), and
Matsuo (24) found no difference in the structure
and density of the choriocapillaris in the macular
region and other areas equidistant from the optic
disc. Increased blood flow in the submacular chor-
oid (1, 30) simply seems to represent increased
blood flow in the large number of arteries aggre-
gated in the submacular choroid, and not neces-
sarily through the choriocapillaris. Terminal arte-
rioles supplying the macular choriocapillaris arise directly from all the temporal short PCAs and other
large choroidal arteries lying in the submacular
choroid, and are usually short, vertical and enter
the choriocapillaris perpendicularly and abruptly as
compared to those going to the choriocapillaris in
the peripheral choroid (24, 26, 28, 29). This ana-
tomical peculiarity of the submacular terminal
choroidal arterioles would make the macular
choriocapillaris much more vulnerable to embolism
than the peripheral choriocapillaris.
Peripapillary choroid
This part of the choroid is supplied by branches

92 S.S. Hayreh
from the short PCAs. Like the rest of the choroid,
postmortem cast studies have consistantly shown
free anastomoses in the peripapillary choroidal
arteries so as to form a continuous vascular net-
work. Shimizu & Ujiie (29), in their choroidal casts,
found that branches of the short PCAs run centri-
petally while undergoing a series of bifurcations;
an incomplete arterial ring was found along the
margins of the optic nerve head, formed by the
numerous arteries entering the arterial ring, and the
latter was regarded by the authors as an inter-
arterial anastomosis. Shimizu & Ujiie (29) con-
cluded that the peripapillary choroidal arterioles
therefore cannot be regarded as end arteries.
The peripapillary choroid is a very important
part of the choroid since it is the main source of
blood supply to the prelaminar and retrolaminar
parts of the optic nerve (7, 13, 14, 29). There are
some serious misunderstandings prevailing on the
subject. It is not uncommon to find authors stating
that if the peripapillary choroid is so very important
in the blood supply of the anterior part of the optic
nerve, then why does the optic disc remain normal
in eyes with peripapillary choroidal atrophy. The
branches supplying the optic nerve arise essentially
from the main arteries in the peripapillary choroid
and not from the small branches and the chorio-
capillaris stop abruptly at the disc margin. In
almost all of the ophthalmoscopically visible peri-
papillary choroidal atrophy the loss is limited to the
choriocapillaris and fine vessels only, with the large
vessels still intact.
My in vivo fluorescein fundus angiographic
studies have clearly demonstrated the segmental
nature of the peripapillary choroid in experimental
occlusion of the PCAs (12, 18, 20) and their
subdivisions (10), by the segmental occurrence of
anterior ischemic optic neuropathy in more than
90 95% of cases, and associated segmental filling
defects in the peripapillary choroid on angiography
(13, 21) and localized sectoral filling defects in the
peripapillary choroid in other conditions. In the
living eye, therefore, the peripapillary choroid has a
definite segmental distribution, and this is another
example of the discrepancy between the post-
mortem anatomical findings and the in vivo circu-
lation. ThUs, meticulously conducted studies, based on
excellent postmortem injection cast preparations,
no doubt give us useful information on the mor-
phology of the choroidal vascular bed, but these
studies misled us greatly. This is because fluorescein
angiographic studies in the living eye have clearly
revealed that the postmortem studies did not give us
correct information about the physiological ana-
tomy and the pattern of blood flow in the choroidal
vascular bed. Fluorescein angiography can truth-
fully be said to have been the major contributor so
far in the study of the choroidal circulation in
health and disease. The choroidal vascular pattern
described above is based mainly on the fluorescein
angiographic studies and should form a basis for a
better understanding of the choroidal vascular bed
in health and disease.
Acknowledgements
I am grateful to my wife Shelagh for her help in
the preparation of this manuscript and to Ms.
Georgiane Parkes-Perret for her secretarial assist-
ance and to the photographic department for the
illustrations. This study was supported in part by
the U.S. Public Health Service Grant No. EY-1576
and EY-1151.
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Author's address:
Department of Ophthalmology
University of Iowa
Iowa City, IA 52242
U.S.A.