L E C T U R E
Posterior Ciliary Artery Circulation in Health
and Disease
The Weisenfeld Lecture
Sohan Singh Hayreh
T he posterior ciliary artery (PCA) circulation is the main
source of blood supply to the optic nerve head (ONH), and
it also supplies the choroid up to the equator, the retinal
pigment epithelium (RPE), the outer 130 m of retina (and,
when a cilioretinal artery is present, the entire thickness of the
retina in that region), and the medial and lateral segments of
the ciliary body and iris. That makes the PCA circulation the
most important part of the ocular and ONH circulation. There-
fore, disturbances in the PCA circulation can result in a variety
of ocular and ONH vascular disorders, causing varying degrees
of visual loss. I have investigated various aspects of the PCA
circulation in health and disease by anatomic, experimental,
and clinical studies since 1955. The objective of this lecture is
essentially to summarize the main findings of those studies. It
is beyond its scope to review the extensive literature on the
subject that has accumulated over recent years.
ANATOMY OF THE PCAS
There is much confusion in the literature about the anatomy of
the PCAs. For a proper understanding of the subject, it is
essential to clarify their nomenclature, origin, number, and
distribution.
Nomenclature, Origin, and Number of PCAs
Most investigators use the term PCA loosely, as a generic
term, for the PCAs, short PCAs (SPCAs) and long PCAs. This is
misleading. My anatomic studies1 on the PCAs in humans
showed the following.
PCAs. There are one to five PCAs arising from the ophthal-
mic artery, one in 3%, two in 48%, three in 39%, four in 8%, and
five in 2% of eyes studied. They run forward along the optic
nerve, and each divides into multiple branches before reaching
the eyeball. The branches of a PCA pierce the sclera lateral,
medial, or, infrequently, superior to the optic nerve. Accord-
ingly, I have named them lateral, medial, and superior PCAs,
respectively.
From the Department of Ophthalmology and Visual Sciences,
College of Medicine, University of Iowa, Iowa City, Iowa.
Supported by research grants from the British Medical Research
Council; National Eye Institute Grants EY01151, EY01576, EY03330
and National Institutes of Health Grant RR-59; and in part by unre-
stricted grants from Research to Prevent Blindness, Inc. SSH is a
Research to Prevent Blindness Senior Scientific Investigator.
Disclosure: S.S. Hayreh, None
Corresponding author: Sohan Singh Hayreh, Department of Oph-
thalmology and Visual Sciences, University Hospitals and Clinics, 200
Hawkins Drive, Iowa City, IA 52242-1091; sohan-hayreh@uiowa.edu.
DOI:10.1167/iovs.03 0469
Investigative Ophthalmology & Visual Science, March 2004, Vol. 45, No. 3
Copyright Association for Research in Vision and Ophthalmology
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Lateral PCAs. They were present in 97% of the eyes: one
in 75%, two in 20%, and three in 2%.
Medial PCAs. They were present in 100% of the eyes: one
in 71% and two in 29%.
Superior PCAs. They were small and present in only 9% of
the eyes: one in 7% and two in 2%.
Branches of the PCAs
Short PCAs. They may be 10 to 20 in number, depending
on the intraorbital subdivisions of the PCA before it reaches the
sclera (Fig. 1).13 The SPCAs are of two types.25
Paraoptic SPCAs. These are only a few small SPCAs that
enter the sclera close to the optic nerve.
Distal SPCAs. These constitute most of the SPCAs. They
enter the sclera a short distance away from the optic nerve on
the medial and lateral sides and run radially toward the equa-
tor. The temporal distal SPCAs pierce the sclera to enter the
eyeball in the macular region.
Long PCAs. There are two of these: one medial and one
lateral (Fig. 1). They enter the eyeball in the horizontal plane
on the medial and lateral sides, some distance away from the
distal SPCAs, and run radially in the horizontal meridian for-
ward to the iris.1,6
VASCULAR PATTERN OF THE PCAS AND
THEIR BRANCHES
Knowledge of the vascular pattern of the PCAs and their
branches was originally drawn entirely from postmortem cast
studies, since the first description by Frederick Ruysch7 in
approximately 1700. All the postmortem cast studies appeared
to show that (1) PCAs have no segmental distribution, (2) they
anastomose freely with one another as well as with the anterior
ciliary arteries, (3) there are interarterial and arteriovenous
anastomoses in the choroid, and (4) choriocapillaris form a
freely communicating and an uninterrupted vascular bed in the
entire choroid.8,9 However, clinically, inflammatory, ischemic,
metastatic, and degenerative choroidal lesions are usually lo-
calized. This puzzling discrepancy was well summarized by
Duke-Elder10: The tendency for inflammatory and degenera-
tive diseases of the choroid to show a considerable degree of
selective localization, despite the fact that anatomically the
vessels would appear to form a continuous network, has given
rise to speculations regarding the anatomic isolation of specific
choroidal areas.
To investigate this discrepancy between the postmortem
cast studies and the clinically seen lesions, I started to research
the subject in vivo experimentally as well as clinically in 1967.
In Vivo Vascular Pattern of the PCAs
Experimentally in rhesus monkeys, I have cut one or another
or all the PCAs and evaluated the area of their distribution in
749
 750 Hayreh
the choroid and ONH and anastomoses by fluorescein fundus
angiography.1114 PCA occlusion caused by thrombosis has
been well documented in patients with giant-cell arteritis, by
various histopathologic studies.1520 That provided a model of
PCA occlusion in humans, to evaluate the in vivo distribution
and anastomoses of the PCA in the choroid and ONH by
fluorescein fundus angiography.2126 These experimental and
clinical studies showed that each PCA had a segmental distri-
bution in the choroid and ONH, and they anastomosed neither
with the adjacent PCAs nor with the anterior ciliary arter-
ies.2,3,1114,2129 Similarly, when we produced anterior ciliary
artery occlusion by recession and resection of the various recti
in rhesus monkeys as well as in patients with strabismus, the
PCAs did not fill the area of the anterior uvea supplied by the
occluded anterior ciliary artery.30,31
In Vivo Vascular Pattern of the SPCA and
Long PCA
Likewise, experimental occlusion of one or the otherSPCA32
or long PCA6in rhesus monkeys resulted in a segmental
choroidal filling defect in the area of distribution of the oc-
cluded artery. The area did not fill from adjacent normally
filling choroid.
In Vivo Vascular Pattern of the
Peripapillary Choroid
Experimental and clinical studies similarly have revealed that
the peripapillary choroid has a segmental pattern3,11,23,27 that
in turn is responsible for the segmental pattern of blood supply
in the ONH and consequently for the well-known sectorial
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IOVS, March 2004, Vol. 45, No. 3
FIGURE 1. Diagrammatic represen-
tation of branching pattern of medial
and lateral PCAs in two eyes (A, B)
and of the site of entry of the various
branches of the PCAs, as seen at the
back of the eyeball (C).
nature of ischemic lesions seen in anterior ischemic optic
neuropathy (AION) and other ischemic disorders of the ONH.
In Vivo Vascular Pattern of the
Choriocapillaris Bed
My fluorescein fundus angiographic studies revealed that the
entire choriocapillaris bed is composed of independent small
lobules.27,33,34 Each lobule is supplied by a terminal choroidal
arteriole in the center, and its venous drainage is by venous
channels situated in the periphery of the lobule (Fig. 2). These
in vivo studies further revealed that various choriocapillaris
lobules normally do not anastomose with their neighbors. The
various lobules are arranged like a mosaic. The shape and size
of the various choriocapillaris lobules vary in different regions
of the choroid (e.g., polygonal in the posterior part and elon-
gated in the peripheral part). The choriocapillaris is arranged
more compactly at the posterior pole than in the periphery, so
that it gradually becomes less dense toward the periphery.
Ernest et al.,35 Torczynski and Tso36 and many other investi-
gators since have confirmed the lobular pattern of choriocap-
illaris in humans.
Thus, my studies clearly demonstrated for the first time that
the in vivo vascular pattern of the PCAs and their branches in
the choroid and ONH vascular bed is strictly segmental, with
no anastomoses between the adjacent segments, which indi-
cates that the PCAs and their branches in the choroid and ONH
behave as end arteries in vivo. This helps to explain the local-
ized nature of choroidal and ONH lesions.
In conclusion, the findings of my in vivo studies clearly
show that postmortem cast studies had misled us for almost
FIGURE 2. Diagrammatic represen-
tation of choriocapillaris. A, choroi-
dal arterioles; V, choroidal vein. (Re-
printed, with permission, from
Hayreh SS. Segmental nature of the
choroidal vasculature. Br J Ophthal-
mol. 1975;59:631 648.)
 IOVS, March 2004, Vol. 45, No. 3 The Weisenfeld Lecture 751

three centuries into rejecting the fact that PCAs have segmental
distribution.8,9 The impressive and fascinating scanning elec-
tron micrographs of the postmortem casts published over
recent years are, unfortunately, equally misleading despite
their spectacular appearance. The explanation for this disparity
may lie in the normally rich autonomic nerve supply of the
choroidal vascular bed, which influences the in vivo pattern of
blood flow and circulation, but is totally absent in postmortem
injection studies. For example, glomus cells, controlled by
nerve fibers, at arteriovenous anastomoses in the choroid form
a mechanism to direct the bloodstream in vivo.37 Thus, in vivo
studies with fluorescein angiography reveal the actual physio-
logic circulatory pattern. In the postmortem studies, by con-
trast, when the cast material is injected under pressure, the
vessels without any neural control fill from all sources, irre-
spective of the normal blood flow pattern, and therefore they
give information about the morphologic conduits only and not
physiologic function. What matters clinically in explaining
different vascular disorders is the in vivo circulatory pattern
and not the anatomic pattern revealed by the postmortem
casts. The in vivo studies explain why inflammatory, ischemic,
metastatic, and degenerative choroidal lesions are usually lo-
calized. This reminds me of the lifelong feud between Camillo
Golgi and Ramo n y Cajal about the discrepancy between the
microscopic anatomy and functional anatomy of the neuronal FIGURE 3. Fluorescein fundus angiograms showing examples of loca-
network. Cajal finally stated: Who does not know that every tions of the watershed zone in four eyes with anterior ischemic optic
scientific accomplishment dislodges some deeply rooted error neuropathy: (A) temporal to the optic disc, (B) passing through the
and that behind it is usually concealed injured pride, if not temporal part of the disc and adjacent temporal peripapillary choroid,
enraged interest?38 (C) involving the entire optic disc and peripapillary choroid, and (D)
passing through the nasal part of the disc and adjacent nasal peripap-
illary choroid. LPCA, lateral PCA; MPCA, medial PCA; WSZ, watershed
AREAS SUPPLIED BY THE VARIOUS PCAS AND THEIR zone.
BRANCHES IN VIVO
Our in vivo clinical and experimental studies of the various Distal SPCAs. Each of these arteries supplies a sector of the
PCAs and their branches in health and disease provided essen- choroid, usually extending from the posterior pole to the
tial information on the areas supplied by each. equator (Fig. 6).32 Each sector varies markedly in shape, size,
and location and has irregular margins. The various sectors fit
Areas Supplied by the PCAs together like pieces of a jigsaw puzzle. Further subdivisions of
the SPCAs supply correspondingly smaller segments of irregu-
These arteries not only supply the choroid but also play an im- lar shape and size, so that the blood supply by the various
portant role in the blood supply of the ONH.2,3,20,23,25,29,39,40 choroidal arteries has a geographic pattern: the smaller the
When there are two PCAs one lateral and one medialthere artery, the smaller the size of the geographic area. Finally, each
is a marked interindividual variation in the area supplied by terminal choroidal arteriole supplies a lobule of the choriocap-
each PCA in humans.2,3,23,25,40 The medial PCA may supply the illaris (Fig. 2).27,3234
entire nasal choroid up to the level of the fovea, including the
entire ONH; or its supply may stop short, nasal to the nasal Areas Supplied by the Long PCAs
peripapillary choroid, so that it may take no part in the blood Each artery runs radially in the horizontal meridian: one on the
supply of the ONH; or there may be any variation between medial and the other on the lateral side (Fig. 1). On the
these two extremes (Figs. 3, 4). The lateral PCA supplies the temporal side, the long PCA supplies a sector of the choroid
area of the choroid and ONH not supplied by the medial PCA. temporal to the macular region, with its apex oriented poste-
When there is more than one medial or lateral PCA, the area riorly (Fig. 6).6 In addition to supplying a sector of the periph-
supplied by each of them may be one quadrant or only a sector eral choroid, each artery also supplies a small sector of the
(Fig. 5). When the superior PCA is present, it accordingly ciliary body and iris on the medial and lateral sides.
supplies a superior sector of varying size. Given the marked
interindividual variation in number and distribution by the
various PCAs, we can get an extremely variable pattern of WATERSHED ZONES IN PCA VASCULAR BED
distribution by them in the choroid and ONH.
A watershed zone is the border between the territories of
distribution of any two end arteries. The significance of the
Areas Supplied by the SPCAs and Their Branches
watershed zones is that in the event of a decrease in the
As has been described, the SPCAs are of two types.2,4 perfusion pressure in the vascular bed of one or more of the
Paraoptic SPCAs. Branches from these go to the corre- end arteries, the watershed zone, being an area of compara-
sponding parts of the ONH, peripapillary choroid, the circle of tively poor vascularity, is most vulnerable to ischemia. In the
Zinn and Haller (when present), and recurrent branches to the brain, for example, development of watershed zone infarcts
retrolaminar ONH pial vascular plexus. Thus, available evi- along the borders of areas of supply by the cerebral arteries is
dence indicates that all these branches of the paraoptic SPCAs a well-known phenomenon.41 45 As shown earlier, PCAs and
constitute the main source of blood supply to the ONH. The their branches, right down to the terminal arterioles, have a
circle of Zinn and Haller is discussed at length elsewhere.3 segmental distribution in vivo. Thus, I discovered that there are

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 752 Hayreh
FIGURE 4. Diagrammatic representation of some examples of loca-
tions of the watershed zone (shaded area) between the medial and
lateral PCAs in the left eye in humans.
watershed zones between the distribution of the various PCAs,
between the SPCAs, and between the anterior and posterior
ciliary arterial circulations.23,27,29 The subject is discussed at
length elsewhere29; the following is a brief summary.
Watershed Zones between the PCAs
My fluorescein fundus angiographic studies in humans have
clearly shown the watershed zones between the various PCAs
(Fig. 3).23,27,29 When there are two (medial and lateral) PCAs,
the area of the choroid and ONH supplied by the two shows
marked interindividual variation (Figs. 3, 4), and that results in
wide variation in the location of the watershed zone between
them. Figures 3 and 4 illustrate some of the locations of the
watershed zone between the medial and lateral PCAs in hu-
mans. They show that the watershed zone may (1) be located
temporal to the peripapillary choroid (Fig. 4A); (2) pass
through the temporal peripapillary choroid (Figs. 3A, 4B); (3)
pass through one or the other part of the optic disc (Figs. 3B,
3D, 4B, 4D), or the entire optic disc may lie in the watershed
zone (Figs. 3C, 4C); (4) pass through the medial peripapillary
FIGURE 5. Diagrammatic representations of some examples of loca-
tions of the watershed zones between the PCAs in the left eye in
humans, with (A) two PCAs; (BD) three PCAs in different combina-
tions; and (E) four PCAs.
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IOVS, March 2004, Vol. 45, No. 3
FIGURE 6. Diagrammatic representation of the choroidal distribution
by various temporal SPCAs and long PCA, and their watershed zones.
Dashed circle: the macular region. (Reprinted, with permission, from
Hayreh SS. Submacular choroidal vascular pattern: experimental fluo-
rescein fundus angiographic studies. Graefes Arch Clin Exp Ophthal-
mol. 1974;l92:181196.)
choroid (Fig. 4E); or (5) various combinations of these. When
there are three or more PCAs supplying an eye, the locations of
the watershed zones vary accordingly, as shown diagrammati-
cally in Figure 5. Thus, the PCA-watershed zone may involve
any part of the ONH, or may cover the entire ONH, or may pass
temporal or nasal to the ONH. The watershed zone may extend
vertically along the entire length (Figs. 3, 4), may be only in the
lower or upper vertical half, or may show other variations (Fig.
5). The watershed zones between the various PCAs play a very
important role in ONH ischemic disorders, because the part of
the ONH that is located in the watershed zone is most vulner-
able to ischemia.
Watershed Zones between the SPCAs
My experimental study has shown that each SPCA supplies a
well-defined sector of the choroid.27,29 Figure 6 is a diagram-
matic representation of the various sectors of the choroid
supplied by the temporal SPCAs and the watershed zones
between the adjacent sectors. Because all the temporal SPCAs
enter the eyeball in the macular region and spread out radially
to the periphery of the fundus to supply the temporal half of
the choroid (Fig. 7), it is natural that most of the segments of
the choroid supplied by the temporal SPCAs and their water-
shed zones meet in the macular region, and that must make the
macular region most vulnerable to ischemia in the event of
vascular insufficiency (discussed later).
Watershed Zones between SPCAs and Long PCAs
Figure 6 shows the area of the choroid supplied by the tem-
poral long PCA.27,29 My experimental and clinical studies have
revealed that there are no anastomoses between the long PCA
and the adjacent short PCAs. Thus, there is a watershed zone
between the long PCA and its adjacent SPCAs.
Watershed Zones between the PCAs and the
Anterior Ciliary Arteries
Experimental and clinical studies dealing with occlusion of a
PCA 1114,2126,40 or an anterior ciliary artery30,31 clearly show
 IOVS, March 2004, Vol. 45, No. 3
FIGURE 7. Fluorescein fundus angiogram of a normal human eye,
showing sites of entry of the SPCAs and their course in the choroid.
Arrow: the center of the macular region. (Reprinted by kind courtesy
of the late Pierre Amalric, Albi, France.)
that there are no anastomoses in vivo between the PCAs and
anterior ciliary arteries. Also, Takahashi et al.,46 on wide-angle
indocyanine green angiography in humans, found an absence
of functional anastomoses between terminal branches of the
anterior and posterior ciliary arteries. Thus, there is a water-
shed zone between the anterior and posterior ciliary arteries
that is situated in the equatorial region of the choroid.29,46
Clinically, it is well known that watershed zones play an
important role in development of ischemic lesions in the in-
volved tissue. Therefore, from the foregoing description it is
evident that the part of ONH or choroid that lies in the water-
shed zones is more susceptible to ischemic disorders than the
part that does not.
My findings on the in vivo end-arterial nature of the PCAs
and their branches, and the presence of watershed zones have
since been confirmed by several studies.35,36,46 54
VASCULAR DISORDERS OF THE PCA CIRCULATION
PCA circulatory insufficiency plays a role in the development
of several important ischemic disorders of the ONH, choroid,
and retina, including the following. My studies indicate that
occlusion of one or two vortex veins exercised a distinct
protective influence against the acute ischemic lesions pro-
duced by PCA occlusion.14
ONH Ischemic Disorders
The PCA circulation is the main source of blood supply to the
ONH.2,3,20,23,39 It is no surprise, then, that vascular insuffi-
ciency in the PCA circulation is a major factor in the develop-
ment of ischemic lesions of the ONH, including AION and
glaucomatous optic neuropathy. The subject of ONH ischemic
disorders is very much misunderstood and consequently has
become highly controversial. To have a proper understanding
of these disorders, it is absolutely essential to know some of the
outstanding features of the PCA blood supply to the ONH,
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The Weisenfeld Lecture 753
including the following: (1) The blood supply in the ONH is
segmental, so that most of its ischemic lesions result in sectoral
visual field defects.2,3,23 (2) As discussed earlier, there is wide
interindividual variation in the area of the ONH supplied by
each PCA, and in the location of the watershed zone between
the PCAs (Figs. 3, 4, 5).2,3,23
My studies in AION and glaucoma indicate that the distri-
bution pattern of the blood supply by the various PCAs and the
location of their watershed zones in relation to the ONH (Figs.
3, 4, 5) determine the extent of ONH involvement by ischemia.
For example, as described earlier, the medial PCA may supply
the entire ONH, a variable amount of it, or none at all. There-
fore, medial PCA occlusion can result in a variable amount of
visual loss or none at all. The same holds true for lateral PCA
occlusion. The end-arterial nature of the PCA circulation and its
segmental distribution also explain the development of only a
sectorial ischemia in the ONH, typically seen in AION and
other ischemic disorders of the ONH. Similarly, the watershed
zone may involve a variable amount of the ONH, the entire
ONH, or none of it (Figs. 3, 4, 5). The part of the ONH that lies
in the watershed zone is more vulnerable to ischemia than the
rest. Clearly, when the entire optic disc lies in the center of a
watershed zone, it is most vulnerable to ischemia.
Anterior Ischemic Optic Neuropathy. AION has come to
be recognized as a common, severe, visually disabling disease,
particularly in the middle-aged and elderly.20,21,24,25,40,55 In my
experimental and clinical studies, I discovered that AION is
due to interference with the PCA circulation to the ONH
(Fig. 3).13,14,20,2125,40 Arteritic AION, seen in giant-cell ar-
teritis, is due to thrombotic occlusion of any one of the
PCAs.13,14,20 26,40 Nonarteritic AION, by contrast, is essentially
due to transient hypoperfusion or nonperfusion of the PCA
circulation in the ONH (and usually not to occlusion of the
PCA), with nocturnal arterial hypotension playing an important
role.24,25,40,56 Therefore, the visual loss is usually much worse
in arteritic than in nonarteritic AION.24 26
Glaucomatous Optic Neuropathy. Glaucoma is a major
blinding disease. My experimental and clinical studies since
1964 have shown evidence of vascular insufficiency in the
ONH in glaucoma.20,39,57 66 Based on those studies up to
1970,39,57,58 and on evidence from other studies in the litera-
ture,59 62 I postulated that glaucomatous optic neuropathy is
vasogenic in origina view now widely accepted, despite the
initial skepticism. Evidence has progressively accumulated dur-
ing the past three decades suggesting that vascular insuffi-
ciency in the ONH plays an important role in its pathogenesis.
My studies in eyes with glaucoma and normal-tension glau-
coma show that 60% of the watershed zones are located as
shown in Figure 4B, 16% as in Figure 4C, and 10% as in Figure
4D. Other factors that influence the blood flow in the ONH also
play a role in development of ONH ischemic disorders63,65
for example, our studies showed a significantly (P 0.0028)
lower nighttime mean diastolic blood pressure and a signifi-
cantly (P 0.0044) greater mean percentage decrease in
diastolic blood pressure in normal-tension glaucoma than even
in AION.66
Choroidal Ischemic Disorders
These lesions have been seen in a number of systemic dis-
eases.67 They may also be due to local vascular occlusive
disorders. I have produced many of these lesions experimen-
tally in rhesus monkeys by PCA occlusion or by malignant
arterial hypertension.12,14,68 70
Acute Choroidal Ischemic Lesions. Their appearance
and types depend on (1) the stage of evolution of the lesions,
(2) the size of the artery or arteriole involved, and (3) the
severity of ischemia.12,14,68,71
 754 Hayreh
Stage of Evolution of the Lesions. Fresh lesions are white,
due to infarction of the RPE and the adjacent outer ret-
ina.12,14,68 After one week they begin to change gradually, so
that over a 2- to 3-week period they become grayish-white,
granular, depigmented areas, ultimately changing into chorio-
retinal pigmentary degenerative lesions. Histopathologically,
initially there is coagulation necrosis of the RPE and of the
outer retinal layers, and the bloodretinal barrier in the RPE is
broken, but we found that 3 months later, it re-forms, even in
eyes with severe ischemic damage.68 On fluorescein angiogra-
phy, therefore, typically during the acute stage of fresh white
lesions, the involved choroid initially shows filling defects, and
the ischemic lesions show late staining, but later on the cho-
rioretinal degenerative lesions show window defects without
any staining.
Size of the Occluded Artery or Arteriole. The size and
shape of choroidal ischemic lesions depend on the size of the
artery involved. These lesions can be divided into the following
separate clinical entities for descriptive purposes, although
they represent a continuous spectrum of the disease.
Occlusion of the PCA produces extensive regional choroi-
dal infarcts.12,14,68 I have produced them experimentally and
have seen them clinically. They are elongated or wedge-shaped
lesions of various shapes and sizes. There are often triangular
sector-shaped lesions located in the peripheral part of the
fundus, with their bases toward the equator and apices toward
the posterior pole.12,14,20,22
Occlusion of the large choroidal artery produces localized
wedge-shaped or segmental lesions.67,71 For example, I have
seen these develop in the distribution of the long PCA (Fig. 6)
as triangular lesions in the horizontal peripheral part.
Occlusion of the small choroidal artery produces lesions
that are usually geographic in shape, with the size depending
on the size of the occluded artery.12,67,71 Available evidence
indicates that clinically geographic or serpiginous choroidopa-
thy belongs to this group. King et al.72 also concluded that in
some patients serpiginous choroidopathy represents a choroi-
dal occlusive phenomenon.
Focal occlusion of small choroidal arterioles: My studies12
show that the clinical entity, acute posterior multifocal pla-
coid pigment epitheliopathy,73 actually represents an acute
ischemic lesion due to focal occlusion of small choroidal arte-
rioles.12,67,71 That conclusion has since been confirmed by
many studies.67,74 Thus, the correct name for this entity should
be acute multifocal ischemic choroidopathy.
Focal occlusion of terminal choroidal arterioles produces
small, round, localized, choroidal infarcts in the distribution of
various choriocapillaris lobules (Fig. 2). A typical example of
this is the acute focal ischemic lesion seen in hypertensive
choroidopathy (described later), which evolves into the
Elschnigs spot.70 In central serous choroidopathy, in the area
of focal leak, ischemia of one or more choriocapillaris lobules
has been shown, followed by capillary and venous hyperemia,
on angiography.75
Severity of Ischemia. Severe ischemia produces choroidal,
RPE, and outer retinal infarction.12,14,68 Mild or moderate isch-
emia, by contrast, results in ischemic dysfunction of the RPE,
with or without demonstrable frank RPE infarction, so that the
RPE loses its bloodretinal barrier property and allows leakage
of choroidal fluid under the retina, resulting in serous retinal
detachment, as seen in hypertensive choroidopathy (see be-
low) and eclampsia.70 I have also seen moderate ischemia
produce postoperative acute choroidal ischemic lesions in eyes
where, in a closed system, the intraocular pressure is kept very
high during surgery for a prolonged period (e.g., during vitrec-
tomy).76
Macular Choroidal Ischemic Lesions. As discussed ear-
lier, the multiple watershed zones between the various tempo-
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IOVS, March 2004, Vol. 45, No. 3
ral SPCAs meet in the submacular choroid (Fig. 6). Conse-
quently, the submacular choroid must be most vulnerable to
ischemic disorders. The various pieces of evidence that suggest
that the macular choroid is more vulnerable to ischemic disor-
ders than other parts of the choroid are discussed at length
elsewhere.77 Briefly, following are some examples in which my
studies have shown evidence of macular choroidal ischemia.
Example 1. In our experimental studies on malignant
arterial hypertension in rhesus monkeys, the submacular cho-
roid showed a marked, selective delayed filling, particularly of
its central part, on fluorescein angiography.70 Consequently,
hypertensive choroidopathy was almost invariably seen in the
macular region, and the choroidal ischemic lesions were most
prominent there. I have seen that clinically as well.
Example 2. In my experimental studies in rhesus mon-
keys, when I reduced the perfusion pressure in the ocular
vessels, fluorescein angiography revealed delayed filling of the
watershed zones in the macular choroid and of the central
macular choriocapillaris.34,77
Example 3. In eyes with age-related macular degeneration,
several histopathologic studies have reported degenerative
changes in the submacular choriocapillaris,78 and fundus an-
giographic51,77,78 and other blood flow studies79 84 have also
shown evidence of impaired macular choroidal circulation.
These would suggest that vascular impairment may play a role
in the pathogenesis of age-related macular degeneration in
some patients.
Thus, all the evidence collectively seems to point to the
conclusion that the submacular choroid is more vulnerable to
chronic ischemia than any other part of the posterior choroid.
Similarly, in eyes of patients with marked atherosclerosis and
arteriosclerosis, a reticular pigmentary degeneration is fre-
quently seen in the equatorial region (in the region of the
equatorial watershed zone between the anterior and posterior
ciliary circulation).34,77,85
Hypertensive Choroidopathy. The physiologic proper-
ties of the choroidal vascular bed influence its response to
malignant arterial hypertension. The choroidal vascular bed
has no blood ocular barrier, because of large fenestrations in
the walls of the choriocapillaris, and readily leaks plasma. The
choroidal vascular bed has a rich autonomic nerve supply. Bill
and Sperber86 and more recently Delaey and de Voorde87
concluded in their reviews that the choroidal circulation is not
autoregulated. Our study also showed absence of autoregula-
tion in the choroidal vascular bed in primates58 and humans. In
our experimental studies on malignant arterial hypertension in
rhesus monkeys,69,70 we found that the development of hyper-
tensive choroidopathy is a prominent feature. Following is a
brief description of the pathogenesis of development of hyper-
tensive choroidopathy: Absence of the blood ocular barrier in
the choriocapillaris 3 marked leakage of plasma (with angio-
tensin II and all other vasoconstrictors found in malignant
arterial hypertension) into choroidal fluid 3 vasoconstriction
of choroidal vessels 3 choroidal ischemia 3 RPE ischemia 3
breakdown of the bloodretinal barrier in RPE 3 serous retinal
detachment. Thus, in hypertensive choroidopathy we found
the following lesions.
Choroidal Vascular Bed Abnormalities. Initially, on fluo-
rescein angiography there was delayed choroidal filling, partic-
ularly marked in the central part of the macular region.70 Later
on, histopathology showed occlusion of the choroidal ar-
teries.69
RPE Lesions. These are focal ischemic lesions and consist
of two stages.
Acute focal ischemic lesions are punctate, pale or white,
pinhead-size lesions, situated at the level of RPE, mostly in
macular region and less often elsewhere. They are associated
 IOVS, March 2004, Vol. 45, No. 3
with overlying focal serous retinal detachment. On fluorescein
angiography the lesions stain during the late phase.70
In 2 to 3 weeks the acute lesions change into focal RPE
degenerative lesions. Later on, these RPE lesions become con-
fluent and are progressive (mostly in macular and peripheral
regions), to become polymorphous RPE atrophic areas or dif-
fuse pigmentary changes. There may be choroidal sclerosis.70
Fluorescein angiography shows window defects and no stain-
ing, because by this time the RPE bloodretinal barrier has
re-formed.68,70
Serous Retinal Detachment. This may be focal (blister-
like), flat, bullous, or total (with shifting subretinal fluid). It is
located in the macular, peripapillary and/or peripheral regions,
with subretinal fluid initially clear, later on becoming turbid,
and occasionally proteinaceous. Later on, subretinal fibrosis
may develop. The macular retina over the detachment may
show microcystic change, separation of nerve fibers, and fo-
veal cysts.70
Choroidal Vascular Changes in Glaucoma. In our ex-
perimental studies in monkeys, evaluation of choroidal circu-
lation with fluorescein angiography showed that a decrease in
perfusion pressure, caused by either an acute increase in in-
traocular pressure or a decrease in systemic arterial blood
pressure, resulted in delay in filling of the choroid, and the
transit time of the dye in the choroid was prolonged: the lower
the perfusion pressure, the more marked the changes in the
choroid.58 In this study, the peripapillary choroid was found to
be more susceptible to the changes than the rest of the cho-
roid; this was later confirmed by other experimental studies.61
Laatikainen,88 in her fluorescein angiographic studies of pa-
tients with glaucoma and normal-tension glaucoma, also found
choroidal filling defects in most glaucomatous eyes; 60% of the
eyes with moderately controlled intraocular pressure showed
delayed or deficient filling of the peripapillary choroid. The
peripapillary choroid is an important source of blood supply to
the ONH.
In our experimental chronic high pressure glaucoma study
in rhesus monkeys,89 our most striking finding was a significant
reduction of choroidal thickness and loss of choroidal ganglion
cells, especially in the central portion of the choroid. Corro-
sion casts of the choroidal vascular bed in these glaucomatous
eyes showed a slight decrease in capillary density and a de-
crease in length of the choroidal arterioles.
RETINAL ISCHEMIC LESIONS SECONDARY TO
OCCLUSION OF PCA
In eyes with PCA occlusion, in addition to AION and choroidal
ischemic lesions, the following types of retinal ischemic lesions
may also develop: (1) Ischemia occurs in the RPE and outer 130
m of the retina12,68; (2) because the cilioretinal artery is
supplied by the PCA circulation, PCA occlusion results in
occlusion of the cilioretinal artery20,22,24,26; (3) in some cases,
the PCA and central retinal artery arise by a common trunk
from the ophthalmic artery.1 The occlusion of the common
trunk results in occlusion of both arteries, which can be dem-
onstrated by fluorescein angiography.20,22,26
In my studies, the most common cause of PCA occlusion
associated with either cilioretinal or central retinal artery oc-
clusion has been giant-cell arteritis, because of the special
predilection of giant-cell arteritis to involve one or the other
PCA.20,22,24,26,40
In conclusion, my studies have shown that the PCA circu-
lation is the most important element in the ocular and ONH
circulation, because various subdivisions of the PCAs supply
the ONH, choroid, the outer retina, and medial and lateral
segments of the ciliary body and iris. The areas of the choroid
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The Weisenfeld Lecture 755
and ONH supplied by the PCAs and their branches show
marked interindividual variation. In vivo, the vascular pattern
of the PCAs and their branches down to the terminal arterioles
is strictly segmental, with no anastomoses between the adja-
cent vascular segments. The choriocapillaris bed has a lobular
pattern. Because the PCAs and their branches in the choroid
and ONH behave as end arteries in vivo, they have watershed
zones between them. That explains why various vascular le-
sions in the ONH and choroid are usually localized and why
those parts of the ONH and choroid lying in the watershed
zones are more vulnerable to ischemic disorders than the rest.
The end-arterial nature of the PCA vascular bed and location of
the watershed zones are the major determinants of the extent
and pattern of ischemic disorders of the ONH and choroid.
Disturbances in the PCA circulation can result in a variety of
ocular and ONH disorders, causing varying degrees of visual
loss. Herein, I have summarized the major disorders of the PCA
circulation involving the ONH, choroid, and retina and have
described briefly the role of PCA circulation in their pathogen-
eses, as revealed by my studies.
Acknowledgments
Modern research relies on teamwork. Over the years, I have had a
series of excellent collaborators and coworkers, too many to name. I
am happy to have this opportunity to acknowledge their invaluable
help. I am also grateful to Georgiane Perret and Patricia Duffel for their
help with the literature, and to my wife for translating the Latin
manuscript by Frederick Ruysch.7
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