Wall Cytoarchitecture of the RatCiliary Process Microvasculature

Revealed With ScanningElectron Microscopy

TAKASHI FUJIWARA,1* TATYANA I. TENKOVA,1 AND MARI KONDO2

1Laboratory Animal Center, Ehime University School of Medicine, Shigenobu,Ehime 791–0295, Japan

2Department of Pathology, Ehime University School of Medicine, Shigenobu,Ehime 791–0295, Japan

ABSTRACTCiliary process vasculature has an important role in aqueous humor

production. There have been, however, few reports describing the overallcytoarchitecture of ciliary process vasculature.

The wall cytoarchitecture of microvessels in the rat ciliary process waselucidated by scanning electron microscopy after removal of ciliary epitheliaand connective tissue components with HCl hydrolysis.

Utilizing characteristics of cellular morphology and vessel diameters,several vascular components were identified along the vascular tree: 1) ar-terial iridociliary circles (30–60 µm in outer diameter), containing a compactlayer of circularly oriented spindle-shaped smooth muscle cells; 2) theproximal part of the radial ciliary arteriole (10–25 µm), containing a lesscompact layer of circularly oriented branched-smooth muscle cells andspindle-shaped smooth muscle cells; 3) a middle part of the radial ciliaryarteriole (20–35 µm), with circularly oriented branched-smooth muscle cellsand irregularly oriented stellate cells with ramifying projections; 4) a distalpart of the radial ciliary arteriole (10–20 µm), possessing irregularlyoriented stellate cells with ramifying projections; 5) marginal venules(15–20 µm), with spidery pericytes possessing highly ramifying and over-lapped projections; 6) capillaries in the ciliary process (4–7 µm), with widelyscattered pericytes having longitudinal and several circular projections;7) venules in the posterior basal region of the ciliary process (greater than 5µm), with widely scattered pericytes having a few thin projections.

From arterial iridociliary circles to venules in the basal region of ciliaryprocess, seven parts could be recognized by wall cytoarchitecture, which wasdiscussed in relation with the function. Anat Rec 254:261–268, 1999.r 1999 Wiley-Liss, Inc.

Key words: microvessel; ciliary process; iris; pericyte, smooth muscle cell;ultrastructure; scanning electron microscopy; rat

It has been well known that the ciliary process, espe-cially its anterior and apical portions, is involved inaqueous humor production (Hara et al., 1977; Ober andRohen, 1979). The microvasculature of the ciliary processhas been studied by means of resin casting method invarious animals (Hossler and Olson, 1984; Morrison andVan Buskirk, 1984; Funk and Rohen, 1985; Toida andUehara, 1985; Morrison et al., 1987a,b). The territorial(Funk and Rohen, 1987a,b, 1990) and functional (Funkand Rohen, 1987b, 1988a, 1989) differentiations of the

Tatyana I. Tenkova is presently at Department of Psychiatry,Washington University School of Medicine, Saint Louis, Missouri63110.

Mari Kondo is presently at Otsuka GEN Research Institute,Otsuka Pharmaceutical Co., Ltd., 463–10 Kagasuno, Kawauchi-cho, Tokushima 771–01, Japan.

*Correspondence to: Takashi Fujiwara, Ph.D., Laboratory Ani-mal Center, Ehime University School of Medicine, Shigenobu,Ehime 791–0295, Japan. E-mail: tfujiwar@m.ehime-u.ac.jp

Received 15 June 1998; Accepted 18 September 1998

THE ANATOMICAL RECORD 254:261–268 (1999)

r 1999 WILEY-LISS, INC.

ciliary process vasculature have been reported. An ultra-structural study of the ciliary process vasculature of theprimate has revealed a segmental differentiation of vascu-lar smooth muscle cells and pericytes along the ciliarymicrovascular tree (Funk, 1991). Smooth muscle cells andpericytes have been well known as important in vascularfunction. Prominent special myocytes have been describedto lie on the adventitial side of afferent segment of anteriorarteriole to which nerve endings are closely associated(Funk, 1991). However, the three-dimensional morphologyof all these cells has not yet been described in the ciliaryprocess microvasculature.

The present study aimed to elucidate the three-dimen-sional structure of periendothelial cells in various parts ofthe ciliary vasculature by scanning electron microscopy tounderstand the morphological characteristics of the ciliaryprocess vasculature in relation to ciliary process circulation.

MATERIALS AND METHODSAnimals

Ten male Wistar Kyoto rats (250–300 g) were used inthis study. All animals were kept under standard houseconditions with food and water ad libitum. The condition oflighting was defined as a 12:12 hr light:dark cycle (lightperiod, 07:00–19:00). The study was approved by theEthics Committee, Ehime University School of Medicine.

Perfusion Fixation and Post-FixationThe animals were anesthetized with Pentobarbital so-

dium (25 mg/kg body weight) and perfused via the leftventricle for about 15 min with 120 ml of phosphatebuffered saline solution (PBS). Perfusion continued with150 ml of 2% glutaraldehyde fixative in 0.1 M phosphatebuffer (pH 7.4) and then with 100 ml of PBS wash atconstant pressure of about 80 mm Hg. These solutionswere warmed to 37°C before perfusion. Immediately after,the rats were transfused by infusion at the same constantpressure with 40–50 ml of heparinized whole blood toprevent the blood vessels from collapsing during subse-quent treatments. The smallest vessels in the ciliaryprocesses were completely filled with blood. The eyeballswere enucleated and cut in half along their equator.Additional 2 hr-fixation with 3% glutaraldehyde fixative atroom temperature was performed. Specimens of iris, 4–6mm in length and 2–4 mm in width, and ciliary processes,4–6 mm in length and 0.5 mm in width, were excised.During the fixation process for 2 hr, the connective tissuelayers of the iris were removed with forceps, and the ciliaryprocess epithelial surface was very gently scratched with asharp needle with the use of an operating microscope. Thespecimens were washed in 0.1 M PBS and then postfixedwith 2 % OsO4 at 4°C for 2 hr, followed by a brief rinse indistilled water.

Removal of Connective TissuesThe specimens were treated with 8 N HCl for 25–30 min

at 60°C to remove connective tissue (Fujiwara and Ue-hara, 1982) and ciliary epithelium. The specimens werewashed in distilled water, dehydrated in graded series ofethanols, immersed in isoamylacetate and critical-pointdried with CO2. They were sputter-coated with platinumand examined in a Hitachi S-500A scanning electronmicroscope.

Vessel, cell body and cell projection diameters weremeasured on photographs enlarged to a final magnifica-tion of 31500–3000.

RESULTSThe three-dimensional morphologies of the smooth

muscle cells and pericytes can be observed from theadventitial side. The morphological changes along thelongitudinal axis of the vasculature can be followed fromthe arterial iridociliary circle (AICC) to the venule in theciliary process (Fig. 1).

Iris VasculatureArterial iridociliary circles, 30–60 µm in outer diameter,

give rise to iris arterioles (IAs) and radial ciliary arterioles(RCAs). The IAs run anteriorly; the RCAs run posteriorlyand turn inward into ciliary processes. The AICCs have amedial layer one to two cells thick which consists ofcircularly oriented smooth muscle cells (Fig. 2). Thesesmooth muscle cells are closely apposed to each other,forming a compact medium around the vessel. Individualsmooth muscle cells are mostly spindle-shaped with acentral bulge 4–5 µm in diameter. They range from 35–65µm in length as measured by tilting the specimen stage tothe maximum angle around the long axis of the vessel.Similar spindle-shaped smooth muscle cells also form acompact medium one cell thick in the IA, which is 10–25µm in diameter (Fig. 3). Two of these layers usuallyencircle the IA orifice.

The RCAs in the iris markedly change in wall cytoarchi-tecture along their long axis. They are divided into threeparts: proximal, middle and distal. The proximal parts ofRCA are 10–25 µm in diameter and shorter than a quarterof the entire length of the RCA. They are surrounded by aless compact medium one to two cells thick. This compactmedium consists of branched smooth muscle cells as amajor component and spindle-shaped smooth muscle cellsas a minor component. The branched smooth muscle cellshave some circular projections, 0.8–2 µm in diameter, andthe spindle-shaped smooth muscle cells are also circular inorientation. Both types of cells progressively flatten to-ward the distal direction along the vessel. Irregularlyshaped cells are sometimes found at the branching pointfrom the AICC, where spindle-shaped or branched smooth

Fig. 1. Schematic drawing of the ciliary process vasculature in rats.Blood flows from the left (anterior) side to the right (posterior) side of theschema. AICC, arterial iridociliary circle; IA, iris arteriole; RCA, radialciliary arteriole; MV, marginal venule; CN, capillary network; V, venule.Numbers indicate the site of the following figures. Arrows show thedirections from which scanning electron micrographs of vessel wallcytoarchitecture were taken.

262 FUJIWARA ET AL.

muscle cells constrict the endothelial tube in a sphincter-like fashion (Fig. 4).

The middle parts of RCA thicken to 20–35 µm in vesseldiameter and are approximately three-fourths of the en-tire length of the RCA. The vessels are invested byirregularly shaped cells, some of which are similar tobranched smooth muscle cells, and others are quite irregu-larly shaped cells (Fig. 5). The latter cells possess severalirregularly oriented projections, which branch into manysecondary projections, exhibiting a complicated profile as awhole. The irregularly shaped cells are quite different fromtypical smooth muscle cells and are classified differentlyfrom them. We term them stellate cells. Branched smoothmuscle cells are mostly oriented circularly and stellatecells are oriented irregularly. The cellular projections ofboth types of cells are widely flattened up to 3 µm indiameter. These cells are scattered, but the cell projectionsfrequently overlap and make contact with each other,forming a cellular network around the endothelial tube.Branched smooth muscle cells gradually disappear in themore distal portion of this part of RCA (Fig. 6).

Distal parts of the RCA are 10–20 µm in vessel diameterand very short in length, running posteriorly in the iris

and turning inward to continue to the microvasculature inthe ciliary process. This portion of the RCA is providedwith a cell investment of stellate cells (Fig. 7). The stellatecells have an oval cell body, about 3 µm 3 5 µm in diameter,and several ramifying cytoplasmic projections less than2.5 µm thick. The cellular projections run circularly,obliquely or longitudinally with respect to the vessel longaxis.

Ciliary Process Vasculature

The marginal venules of the anterior apical region of theciliary process are 15–20 µm in diameter and character-ized by spidery pericytes which have highly ramifiedslender cell projections, 0.2–1.2 µm in thickness (Fig. 8).The cell projections are randomly oriented with respect tothe vessel axis, and overlap and/or attach to each other,forming a complicated and dense cellular network. Numer-ous spines extend from both sides of the projections,creating an irregular outline along the entire length. Thepericyte cell bodies are frequently located on the nonepithe-lial side of the vessel.

Fig. 2. A scanning electron micrograph of the arterial iridociliary circlewith a compact layer of spindle-shaped smooth muscle cells. The smoothmuscle cells are circularly oriented. 32,200. Scale bar: 5 µm

Fig. 3. A branching point of an iris arteriole from an arterial iridociliarycircle. The orifice of the iris arteriole is encircled by double layers ofspindle-shaped smooth muscle cells. The iris arteriole has a compactmedium. 32,400. Scale bar: 5 µm

263CILIARY PROCESS VESSEL WALL CYTOARCHITECTURE

Figures 4–7.

264 FUJIWARA ET AL.

Many capillaries branch off from the marginal venulesin the ciliary process. The capillaries, 4–7 µm in diameter,are associated with pericytes positioned along the vessel atintervals of 15–25 µm. The pericytes tend to occur atcapillary branching points (Fig. 9). The pericyte cell bodies

are oval or spindle-shaped, about 5 µm in length, fromwhich primary cell projections, less than 1 µm thick,extend longitudinally or obliquely with respect to the longvessel axis. Secondary cell projections often branch offfrom primary projections, encircling the capillary. Thecapillary pericytes of the ciliary process’s vascular networkresemble the pericytes of true capillaries in rat mammarygland (Fujiwara and Uehara, 1984).

The ends of the marginal venule, 7–10 µm in diameter,have pericytes, each with an oval cell body about 5 µm inlength with two or three long and slender cell projectionsless than 1 µm thick. The cell’s primary projections arestraight and run parallel to the long vessel axis. There area few irregularly directed secondary projections.

In the basal region of the ciliary process, capillariesdrain into venules, which are larger than 5 µm in diameterand endowed with pericytes (Fig. 10). Several thin cellprojections extend from the cell body of pericytes. Theseare less than 1 µm thick and run circularly, obliquely orlongitudinally with respect to the vessel axis.

DISCUSSIONWe elucidated for the first time the medial wall cytoarchi-

tecture of the rat ciliary process vasculature from theAICC to the venule in the ciliary process as summarized inTable 1. The method of combining scanning electronmicroscopy with connective tissue removal has been gener-ally accepted in morphological science (see Fawcett, 1994)and frequently been used for studies of the vascular wallcytoarchitecture of various tissues (Mazanet and Franzini-Armstrong, 1982; Holley and Fahim, 1983; Fujiwara andUehara, 1984; Inokuchi et al., 1989).

Iris VasculatureFrom the morphological characteristics (i.e., a compact

medium of one or two layers of circularly oriented smoothmuscle cells), the AICCs can be identified as arterioles orterminal arterioles (Rhodin, 1967), rather than as smallarteries as previously reported (Funk, 1991). The IAs canbe identified as terminal arterioles because they have acompact medium one cell thick, composed of circularlyoriented spindle-shaped smooth muscle cells (Rhodin,1967). The proximal parts of the RCA have a less compactmedium one to two cells thick and are comprised ofcircularly oriented branched smooth muscle cells as amajor component. These parts can be identified as precap-illary arterioles or as the parts transitioning betweenterminal arteriole and precapillary arteriole (Fujiwaraand Uehara, 1984). During contraction, the circular orien-tation of the smooth muscle cells in the AICCs, IAs andproximal parts of RCAs is appropriate for the function ofvasoconstriction (Fujiwara and Uehara, 1984). The AICCsand the IAs, however, appear to be more powerful inconstricting the vascular lumen than the proximal parts ofthe RCA. This is believed to be due to differences in cellcomposition, spindle-shaped smooth muscle cells vs.branched smooth muscle cells as the major component.

At the region where IAs and RCAs branch from theAICC, a ring-like impression was found by scanningelectron microscopic observation of resin casts, suggestingthe presence of a sphincter or an intimal cushion whichpossibly regulates blood circulation (Burger et al., 1983;Toida and Uehara, 1985). This is further supported by thefinding of the present study that smooth muscle cells are

Figures 4–7. Scanning electron micrographs of the radial ciliaryarteriole.

Fig. 4. A proximal part of the radial ciliary arteriole branched off froman arterial iridociliary circle. Irregularly shaped cells (asterisk) are foundon the spindle-shaped smooth muscle cells at the branching point of thevessel. N, nerve fiber; AICC, arterial iridociliary circle; A, adventitia.33,500. Scale bar: 2 µm.

Fig. 5. A middle part of the radial ciliary arteriole with circularlyoriented branched smooth muscle cells (bSM) and irregularly orientedstellate cells (S). A, adventitia. 32,700. Scale bar: 2 µm.

Fig. 6. A stellate cell with irregularly oriented ramifying and overlap-ping projections, in the middle part of the radial ciliary arteriole. Muchmore distal than Figure 5.

A, adventitia. 33,300. Scale bar: 2 µm.Fig. 7. A frontal aspect of the distal part of the radial ciliary arteriole

coming out through dense connective tissue of the basal portion of ciliaryprocess. The stellate cell (S) has several projections running irregularlywith respect to the vessel long axis. 34,700. Scale bar: 2 µm.

Fig. 8. A marginal venule with spidery pericytes in the anterior apicalregion of ciliary process. Projections of the pericyte ramify extensively andform a complicated network. Note numerous spines (arrow) along bothsides of the projections. 34,700. Scale bar: 2 µm.

265CILIARY PROCESS VESSEL WALL CYTOARCHITECTURE

sometimes stacked into two layers encircling this region ofthe IAs and RCAs.

The middle parts of the RCA can not be identified as anypreviously characterized vessels because these parts havea unique cytoarchitecture—a loose investment consistingof circularly oriented branched smooth muscle cells and

irregularly oriented stellate cells. The latter cells were forthe first time characterized in this study. Stellate cellsresemble the primitive smooth muscle cells in the collect-ing venule, which functions as a volume capacitance vessel(Rhodin, 1968; Stromberg and Wiederhielm, 1973). There-fore, the middle parts of the RCA may play a role as a

Fig. 9. A capillary with pericytes (P) in the ciliary process. Thepericytes often occur at the branching points of the capillaries and havelongitudinal and circular projections. 34,500. Scale bar: 2 µm.

Fig. 10. A venule in the basal region of the ciliary process viewed fromapical aspect. Capillaries drain into the venule. The pericytes (P) extendseveral thin cell projections running circularly or longitudinally. 33,900.Scale bar: 2 µm.

TABLE 1. Morphological features of various parts of ciliary process microvasculature in rats

Vascular parts

Vesseldiameter (µm)

min–max

Periendothelial cell

Cell shape, type and orientation Arrangement

Arterial iridociliary circle (AICC) 30–60(n 5 10)

Spindle-shaped smooth muscle cells,circularly oriented

Compact one to two layers

Radial ciliary arteriole (RCA)Proximal part 10–25

(n 5 10)Branched smooth muscle cells as a

major component and spindle-shapedsmooth muscle cells as a minor com-ponent, circularly oriented

Less compact one to twolayers

Middle part 20–35(n 5 16)

Branched smooth muscle cells, circu-larly oriented and stellate cells withramifying and overlapping projec-tions, irregularly oriented

Scattered

Distal part 10–20(n 5 5)

Stellate cells with ramifying projec-tions, irregularly oriented

Scattered

Marginal venule (MV) in the anteriorapical region of ciliary process

15–20(n 5 5)

Spidery pericytes with highly ramifyingand overlapping projections

Scattered

Capillary in the ciliary process 4–7(n 5 5)

Pericytes with longitudinal and circularprojections

Widely scattered

Venule (V) in the posterior basal regionof ciliary process

5,(n 5 5)

Pericytes with randomly oriented thinprojections

Widely scattered

266 FUJIWARA ET AL.

reservoir for blood and to maintain smooth blood flow inthe downstream ciliary process vasculature. The appar-ently weak contractile capability of the middle parts wellaccounts for the unusual finding that these parts arelarger in diameter than the upstream proximal parts inarterial vasculature.

The distal parts of the RCA can not be easily identified inrelation to already known arterial segments but appear tocorrespond to a rat ciliary process arteriole (Morrison etal., 1987b) or to a rabbit (Funk and Rohen, 1987a), monkey(Funk and Rohen, 1988b) or human (Funk and Rohen,1990) terminal arteriole considering their location in theanterior basal region of the ciliary processes. Scanningelectron microscopy and intraocular microendoscopy (Funkand Rohen, 1987b) have demonstrated that the distalparts of the RCA exhibit a prominent focal constriction ofthe vessel lumen in untreated rats and monkeys (Morrisonet al., 1987b; Funk and Rohen, 1988b) and in monkeys andhumans following administration of vasoconstrictoryagents, such as epinephrine (Funk and Rohen, 1988b,1990). Thus, these parts of the vessel play an importantrole in blood-flow regulation of the ciliary processes (Funkand Rohen, 1987b). The stellate cells, constituting themedial wall of distal part of RCA, seem to constrict thevessel lumen in response to stimulation by neurotransmit-ters, such as catecholamine and neuropeptide Y, which arereleased from the nerve fibers that densely innervate thispart of the vasculature (Ritting et al., 1993). Further studyis required to determine if the stellate cells have structuralproperties as those of smooth muscle cells, such as contrac-tile filaments, and if they are closely associated with nerveterminals as in the case of special myocytes in the monkeyciliary process (Funk, 1991).

Ciliary Process VasculatureThe marginal venules are directly supplied by the final

portions of the RCA; there are no intervening capillaries.These venules can be regarded as ‘‘thoroughfare channels’’(Funk et al., 1992) or ‘‘central channels’’ (Chambers andZweifach, 1944). The marginal venules become thinnertoward the posterior segment of the vasculature, contraryto the general feature of venules to get thicker along theircourse. This seems to be effective maintaining relativelyhigh blood pressure, as reported by microendoscopic obser-vation (Funk et al., 1992). The maintenance of high bloodpressure may be appropriate for the aqueous formation inthe marginal venules. The anterior and apical portions ofthe pars plicata through which the marginal venules drainare involved in aqueous humor production (Hara et al.,1977; Ober and Rohen, 1979).

The marginal venules may correspond to a postcapillaryvenule, since they have pericytes resembling the spiderypericytes of postcapillary venules in the rat mammarygland (Fujiwara and Uehara, 1984). Since the postcapil-lary venules are the most permeable site in the vascula-ture (McDonald, 1994), the marginal venules also may behighly permeable. This supports the suggestion that themarginal venules are a site of aqueous formation. How-ever, the pericytes of marginal venules are characterizedby cell projections, which exhibit a markedly irregularoutline with numerous spines, while the postcapillaryvenule pericytes have cell projections that are smooth inoutline. The spines of projections may regulate the perme-ability of the marginal venules.

The venules in the basal and posterior region of theciliary process are associated with pericytes that have thincell projections. From their morphology, the venule peri-cytes probably do not contract enough to constrict thevessel lumen by themselves. Both pericytes and endothe-lial cells may contract in cooperation with each other, sincea constriction of the venous segment was seen aftercarbachol administration (Funk and Rohen, 1988a). Avasoconstriction of the venous segment would also effec-tively increase the filtration pressure within the ciliaryprocess.

This study demonstrates several types of periendothe-lial cells in the rat ciliary process microvasculature anddifferentiates vascular parts based mainly on periendothe-lial cell morphology, type and juxtaposition in relationshipto physiological functions of the vascular components,suggesting different roles of periendothelial cells. Themorphological characteristics of stellate cells and thedifferences among smooth muscle cells, stellate cells andpericytes, however, must be further clarified by transmis-sion electron microscopy and immunofluorescent micros-copy for actin and myosin isoforms (Shepro and Morel,1993). There remains additional study of the ciliary pro-cess microvasculature of other species than the rat byscanning electron microscopy combined with connectivetissue removal, since the iris and ciliary process microvas-culature is different between rats and other mammalianspecies.

ACKNOWLEDGMENTSWe thank Dr. Judy Ogilvie, Central Institute for the

Deaf, Washington University School of Medicine, St. Louis,for critical reading of the manuscript, and D. Shimizu, K.Okugawa and K. Ohono, Ehime University School ofMedicine, for their technical help.

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