fine structure of the human ciliary muscle

8/3/2019 Fine Structure of the Human Ciliary Muscle

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October, 1962 Volume 1, Number 5I N V E S T I G A T I V E O P H T H A L M O L O G Y

Fine structure of the humanciliary muscle

Toyoko Ishikawa*

The ciliary muscle in human eyes consists of bundles of muscle cells surrounded by flattenedconnective tissue cells. Each b undle g enerally contains unmyelinated nerve fibers accom-panied by Schwann cells and a few connective tissue components. Some of the nerve fiberscontain many vesicles characteristic of nerve endings. The nerve fibers are, in a few cases, invery close apposition to the muscle cell mem brane, but in most instances they ar e separatedby basement membrane material. Single muscle cells are, in general, cylindrical and entirelywrapped in a basement m embrane except at small areas of contact with o ther muscle cellswhere it is absent. The central region of these cells contains a slender nucleus, centrosomes,Golgi apparatus, endoplasmic reticulum, and abundant mitochondria. Many myofilamentsoriented parallel to the length of the cell axis are found in the cytoplasm. Elongatedpatches of dense material are observed between the myofilaments, particularly in contactwith cell membranes. Numerous pinocytic vesicles occur along the muscle cell membrane.In the spaces between the bundles, collagen, very thin collagen-like (reticular) and elasticfibers, myelinated and unmyelinated nerve fibers, and capillaries are seen. The capillarywalls are thicker than those of the ciliary processes, and lack pores.

I n recent years, great numbers of investi-gators have payed attention to the finestructure of striated muscle, and manynew findings and confirmations of classicalideas concerning its fine structure havebeen brought to our knowledge. However,the smooth muscle cell, having less strikingfeatures in comparison with striatedFrom the Department of Ophthalmology, Collegeof Physicians and Surgeons, Columbia Uni-versity, New York, N. Y.This investigation was supported by ResearchGrants B]202(C5) and B492(C7) from theNational Institute of Neurological Diseases andBlindness of the National Institutes of Health,United States Public Health Service.^Fellow, Fight for Sight Research Fellowship,financed by the Bob Hope Fight for Sight Fundof the National Council to Combat Blindness,Inc., New York Citv.

muscle, has been the subject of only afew, some very brief, studies of the musclein the uterus,1"3 urinary bladder,4 andartery.5"7The ciliary muscle in the eye plays animportant role in accommodation, is veryactive and, therefore, probably differs instructure from smooth muscle found else-where. It also varies in structure in dif-ferent species. The present study dealswith electron microscopic observations ofhuman ciliary muscle which extend thoseof Shiose,8 and reports further structuraldetails, especially of the cytologic charac-teristics of the muscle cell, its morphologicconstruction, and the innervation of theciliary muscle.Materials and methods

Normal human ciliary muscles of 5 eyes ob-tained at operation were used in this study. Two587


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588 Ishikawa Investigative O phthalmologyOctober 1962

eyes were from persons 66 and 42 years old, wereremoved for small malignant melanomas of theposterior choroid, and the other eyes were 2, 4,and 7 years old; the first was removed because ofa retinoblastoma and the other 2 for orbitalrhabdomyosarcoma.After enucleation, the eyeballs were immediately(within 2 to 3 minutes) cut into anterior andposterior parts near the ora serrata. The anteriorhalf of the eye was immersed in cold fixative(2 per cent OsO 4 in veronal-acetate buffer, pH7.4, with 0.045 Gm. sucrose per 1 ml. fixative),and the ciliary body was carefully stripped fromthe sclera. The ciliary body was dissected andfixed in fresh cold fixative for 2 hours.After dehydration through an ethanol series, thematerials were embedded in either Araldite orEpon 812 according to Luft's9 procedure.Sections for electron microscopy were madewith a glass knife on a Porter-Blum microtomeand were stained with uranyl acetate or a solu-tion of lead.10 ' a i Counterstaining with a solutionof lead, after very brief staining with uranylacetate, was employed for a few sections. Electronmicrographs were taken with Siemens Elmiskop Iat original magnification of 2,500 to 12,000.

ObservationsThe smooth muscle cells of the humanciliary body are grouped in bundles. Ineach bundle, the muscle cells are closelypacked and many peripheral nerve fibersare found between them. Each bundle isclosely surrounded by a sheath of flattenedfibroblasts (Figs. 1-6). Connective tissue,consisting mainly of collagen fibrils andfibroblasts, occupies the space betweenbundles. A small amount of connectivetissue found inside the bundles consistschiefly of fine fibrils which may correspondto reticular fibers. In some instances, these

fine fibrils are attached to the fibroblast.Occasionally pigment cells are seen in-side the bundles. Corresponding to thedescription based on the light microscopicobservations12 some morphologic differ-ences can be observed between the so-called meridional (the meridional fibersrun anteroposteriorly and cross the equatorof the globe at right angles) and the radialportion which is internal to the meridionalfibers and fans out posteriorly to make awide attachment to the connective tissueof the choroid.13

In the meridional part, clearly separatedbundles of muscle cells run parallel to eachother, and the intermediary connectivetissue spaces are small (Figs. 1, 2, and 5).Therefore, in the meridional sections, asshown in Fig. 2, the muscle appears toconsist of longitudinally disposed cylin-drical bundles. In contrast in the radialpart, the contour of the bundles is ratherirregular and obscure and a dense con-nective tissue fills the spaces between thebundles (Fig. 3).Moreover, the size and the shape ofmuscle cells differ in these two regions, i.e.,the cells in meridional muscle have a rela-tively smooth outline and are about 3 jx inwidth at the widest part, usually the cen-tral area where the nucleus is located.Their length is too great to be estimatedin these sections. In some cases one canfollow a cell for over 20 n even in a singlesection, whereas the cells in the radial parthave an irregular outline which is approxi-mately one and a half times as great in thenuclear region (Figs. 3 and 4).The fine structure of smooth muscle cellin the human ciliary body is described be-low.Cell membrane and basement mem-brane. Similar to the smooth muscle of theuterus,1 '3 urinary bladder,4 and arteries,5'Ga single smooth muscle cell in the ciliarybody is clearly bounded by a distinct cellmembrane and by a basement membranewhich has a thickness of about 250 A andwhich covers almost the entire cell closely,leaving only a few small areas uncovered.

The interspace between the cell and base-ment membranes is constant, and approxi-mately 150 A in width. In some regions,two basement membranes of contiguouscells fuse into a single membrane, or twocell membranes of contiguous cells sharea single basement membrane (Fig. 5).Frequently, the small areas where twoadjacent cell membranes appear to beattached directly, without any interposingbasement membrane, are observed as indi-cated by arrows in Fig. 6. The width ofthese areas is always less than 0.25 ^ in


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Volume 1Number 5 Fine structure of human ciliary muscle 589

the plane of section. The cell membranesat such areas are thickened and show asomewhat desmosome-like structure. Thebasement membrane in these areas is con-tinuous from one cell to the other. The con-tour of some muscle cell membranes isuneven, as shown in Figs. 2, 4, and 11. Nomyofilaments could be recognized in theconvex portion of the cytoplasm of thesecells.A great number of vesicles, or caveolae,about 640 A in diameter are found alongthe cell membrane (Figs. 5 and 8). Theymay be a type of pinocytotic vesicle whichsuggests active transport in one or bothdirections.14Nucleus and its vicinity. The nuclei ofsmooth muscle cells are, in general, elon-gated in meridional and oval in the radialportions, respectively (Figs. 2 and 3). Thenucleus is located in the central part withits axis parallel to the longitudinal axis ofthe cell. Occasionally indentations of thenuclear envelope can be seen (Fig. 8).The fine structure of the nucleus in ciliarymuscle cells is very similar to that ofsmooth muscle cells described by otherauthors. The nuclear envelopes consist ofdouble membranes separated by about 100A in which pores occur only rarely. Theinterior of the nucleus is filled with agranular material scattered rather evenlyand with an occasional slight aggregationof material observed along the innernuclear membrane. Prominent nucleoli canbe encountered (Fig. 8).A small or indistinct Golgi complex hasbeen reported in smooth muscle of severaltissues.The ciliary muscle cells, on the contrary,contain a well-developed Golgi apparatuswhich appears to be separated into severalunits, one in the vicinity of the elongatednucleus, generally at one side (Fig. 8).Single fragments are composed of 4 to 5parallel Golgi membranes associated withnumerous Golgi vesicles.A pair of centrioles occurs frequently inthe region enclosed by the nucleus andthe Golgi apparatus (Fig. 8).

Mitochondria and endoplasmic reticu-him. The mitochondria of ciliary musclecells are rod shaped and occasionally bifur-cated as shown in Fig. 8. Their diameter,approximately 0.2 [x , is relatively constantbut their length varies considerably. Themitochondria are bounded by a doublelimiting membrane. The inner limitingmembrane extends inward to form theclosely packed cristae mitochondriales. Themitochondrial matrix is filled with a densematerial.The mitochondria tend to be concen-trated on both sides of the elongatednucleus and in the central region of thecell, decreasing in number toward the endof the cell. The number of mitochondria isgreater in the radial muscle cells than inthose of the meridional cells. Fig. 7 showsthe large number of mitochondria in a cellin the radial portion. It is remarkablydifferent from that found in smooth musclecells in other parts of the body.The systematic arrangement of endo-plasmic reticulum found in striated mus-cles15 is not seen in ciliary muscle cells.This material generally appears in tubularor vesicular shapes. Most of it belongs tothe so-called smooth-surfaced endoplasmicreticulum. Fig. 9 shows part of a musclecell found in the radial portion. In thisillustration, considerable amounts of endo-plasmic reticulum can be recognized. Inmost cases it consists of tubular or vesicularprofiles which anastomose at some points.The content of reticulum or intracisternalmaterial is amorphous and shows a higher

electron density than that of the cyto-plasmic matrix. The vacuolizations ordilatations of the reticular system foundin some sections are probably artifacts pro-duced during the preparation of the sec-tions.Most of the endoplasmic reticulum liesparallel to the m itochondria. In some placesa connection between endoplasmic reticu-lum and cell membrane can be seen (Fig.10). Over almost the entire cytoplasm,except where it is occupied by a mass ofmyofilaments, dense particles are observed.


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They are 100 to 250 A in diameter andheavily stained with the solution of lead.Most of these seem to be RNP-particles, thelarger ones may be glycogen. Occasionallylipid droplets are seen in the cytoplasm ofthe muscle cells.Myofilaments. In striated muscle, themyofilaments are regularly grouped intobundles, called myofibrils, and show clearcross-banding. Neither regular groupingnor cross-banding can be observed in themyofilaments of ciliary muscle cells. Myo-

filaments are, however, distributed through-out the entire cell and are arranged longi-tudinally (Figs. 9 and 10). In the trans-verse sections they appear as tiny dots andshow relatively regular arrangement, i.e.,hexagonal distribution at a distance ofabout 600 A from each other (Fig. 5).On examination of uranyl-stained sec-tions at higher magnification, a single myo-filament may be seen to be composed oftwo elements, a dense core about 80 A indiameter surrounded by a faint filamentousmaterial. These elements, however, areindistinguishable in longitudinal section.Between the myofilaments, particularlyalong the cell membrane, dense elongatedbodies are found in every cell (Figs. 1 and5). Both in transverse and longitudinal sec-tions a fine filamentous structure can beobserved around these dense bodies (Fig.5) .Nerve fibers and endings in ciliary mus-cle. Many nerve fibers are very frequentlyobserved in sections of ciliary muscle. Theconnective tissue spaces contain both

myelinated and unm yelinated nerve fibers,which are always enfolded by cytoplasmicextensions of Schwann cells (Figs. 3, 5,and 15). Numerous unmyelinated nervefibers with their Schwann cells penetratebetween the muscle cells.The diameter of nerve fibers in thebundles varies from 0.1 to 1.2 /x . Somenerve fibers are entirely wrapped bySchwann cells and contain fibrillar ele-ments and a few mitochondria. The major-ity of the nerve fibers are rich in mito-chondria and vesicles of 400 A in diameter.

These vesicles are similar to the synapticvesicle found in synaptic endings else-where; therefore, it is reasonable that thesealso are synaptic endings. Furthermore,these nerve endings are not covered bySchwann cells, at least adjacent to themuscle. In very rare instances, tubularstructures may be found in these synapticendings (Fig. 10). In the ciliary musclecells, three different types of neuromuscularjunctions may be recognized with differentfrequencies. Fig. 12 shows the first type ofjunction. This type is the most frequentlyfound so that it is seen very easily in everypreparation. The main difference betweenthis junction and the others is the inter-vention of the basement membrane be-tween the membranes of the muscle andthe nerve ending. The interspace betweentwo synaptic membranes averages 800 Ain width, including the thickness of thebasement membrane.The second type may be found occa-sionally and is shown in Fig. 11. The maincharacteristics are the very close apposi-tion of synaptic membranes and the smallarea of apposition. The intermembranousspace is approximately 100 A in width. Inthis type, a few muscle cells may be re-lated to a single nerve ending.The third type is found very rarely. Init, a large nerve ending, approximately 2 fxin diameter contacts the muscle cell overa relatively large area.Capillaries and connective tissue. Th espace between the muscle bundles in theciliary body is occupied by connective

tissue, nerve tissue, and blood vessels.Generally capillaries are situated outsidethe bundles, but occasionally they comeclose to the muscle cells (Figs. 1 and 14).The capillary walls are thicker than thoseof the ciliary processes16 and usually lackpores. The connective tissue spaces areoccupied mainly by the collagen fibrils,which show the characteristic periodicity of640 A. The flattened fibroblast, pigmentcell, very thin collagen-like fibers, and theelastic fibers which often appear in olderciliary bodies are also seen.


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Volume INumber 5 Fine structure of human ciliary muscle 591

n

Fig. 1. Slightly oblique, transverse section of a meridional portion of human ciliary muscle.The muscle cells (M ) are grouped in flattened bundles which are surrounded by thin, flattenedfibroblasts (F). Between the bundles, nerves (n) and a capillary (Cap) are seen. P, Pigmentcell. Specimen age, 2 years. (xl0,000.)


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592 Ishikawa Investigative OphthalmologyOctober 1962

2. .Fig. 2. Longitudinal section of a meridional portion of human ciliary muscle. Slender musclecells (M ) are packed closely to and parallel with each other. The connective tissue components(con) are sparse and pigment cells (P ) are seen within the bundles. Specimen age, 7 years.(x7,200.)


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f i r

t.ca t*

to

Fig. 3. Cross section of the radial portion of ciliary muscle. Bundles cannot be clearly dis-tinguished from each other. Many collagen fibrils (cf) are seen in the connective tissue space.M, Muscle cells, n, Nerve fibers, F, Fibroblasts. Sepecimen age, 42 years. (x9,300.)


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594 Ishikawa Inoestigative OphthalmologyOctober 1962

* IU

In*.Fig. 4. For legend see opposite page.


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Yfthrme 1Ntimber 5 Fine structure of human ciliary muscle 595

nBm

ERmyo

Bin %>\1

kSch

Fig. 5. Cross-section of meridional muscle cells. Muscle cells contain mitochondria (m),endoplasmic reticulum (ER) and myofilaments (myo) distributed throughout the cytoplasm.Dense bodies (arrow) are seen between the myofilaments and along the cell membrane. Asingle muscle cell is almost entirely covered by basement membrane (Bm). Fine collagen-likefibrils (f) are seen in the bundle and in the connective tissue space, n, Nerve fibers. Sch,Schwann cell. F, Fibroblasts. (xl7,400.)

Fig. 4. Longitudinal section of the radial portion of the ciliary muscle. Muscle cells (M ) showmore irregular profiles and have a larger cell body than have the meridional fibers shown inFig. 2. Nerve fibers (n ) are accompanied by Schwann cells (Sch). F, Fibroblasts. Specimenage, 4 years. (x8,600.)


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\

\l*nFig. 6. Cross-section of meridional muscle cells. The small areas indicated by arrows showthe direct attachment of adjacent cells with no basement membrane (Bin) between two cells.Basement membrane in the area covering is continuous from one to the next. F, Fibroblast.m, Mitochondria, n, Nerve fibers. (x28,000.)

Fig. 7. Slightly oblique, longitudinal section of radial muscle cells (M). Large numbers ofmitochondria (m ) are present in the cytoplasm, especially near the nucleus (N). cf: Collagenfibrils. F, Fibrobkst. (xl7,000.)

Fig. 8. General survey of a part of the nuclear region of a ciliary muscle cell. Nucleus (N )shows an indentation and has a prominent nucleolus (Nl). A well-developed Golgi apparatus(C ) and a pair of centrioles (C) are seen at this region. Along the cell membrane, manypinocytotic vesicles (v) are observed, m, Mitochondria. Bra, Basement membrane. (x34,800.)

Fig. 9. Higher magnification of a part of a ciliary muscle cell from the radial portion, showingmitochondria (m), endoplasmic reticulum (ER), and myofilaments (myo). {Note that themitochondria and endoplasmic reticulum are located near each other.) Numerous free RNPparticles (p) are seen in the cytoplasm except between myofilaments. (x29,00 0.)


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M

Fig. 7. For legend see opposite page.


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598 Ishikawa Investigative OphthalmologyOctober 1962

Bm

J0

m

N

Nl

Fig. 8. For legend see page 596.


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jr J -

ER

myo

"ER-8Y)-

X I

Jt*Fig. 9. For legend see page 596-


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ww


Fig. 10. Longitudinal section of muscle cells (M ) and nerve endings showing Type 1 neuro-muscular junction. In the synaptic ending, tubular structures (ts) are seen in the nerve aswell as synaptic vesicles (sv) and mitochondria (m). Endoplasmic reticulum in a muscle cellis shown crossing myofilaments (myo) and attaching to the muscle cell membrane (arrow).(x20,800.)


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1M

Fig. 11. Neuromuscular junction Type 2. The nerve ending containing synaptic vesicles (so)and mitochondria (m ) is directly attached to muscle cell (M ) membranes in a small area. Nobasement membrane is seen between the nerve ending and the muscle cell membranes. Threejunctions (arrows) are seen on a .single nerve ending. Note folds in muscle cell membrane,left side of figure. (x20 ;800.)


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Fig. 12. Neuromuscular junction Type 1. A nerve ending containing many synaptic vesicles(so) and mitochondria (m ) is in apposition to the muscle cell (M ) membrane, with an inter-vening basement membrane (Bin). The nerve ending is not covered by a Schwann cell (Sch),at least on the side adjacent to the muscle. (x26,000.)


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tf N

M

13.Fig. 13. A large nerve ending containing synaptic vesicles (so) and mitochondria (mj is seenin a depression in the muscle cell (M ) with a large attachment area without basement mem-brane (Bin). N, Nucleus. (x28,O0O.)

Fig. 14. Muscle cells (M ) and blood capillary (Cap) containing erythrocytes (E). A capillaryis located close to the muscle cell with no intervening flbroblast. Endothelial cells (En) of thecapillary are thin but lack pores. Many pinocytotic vesicles (v) are seen along the cell mem-branes of muscle cells and the endothelial cell. (xl5,600.)


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Fig. 15. A part of the connective tissue in the ciliary body showing a capillary (Cap) an dmyelinated (mn) and unmyelinated nerve fibers (n). Small peripheral nerve fibers also areenfolded by Schwann cells (Sch). Collagen fibrils (cf) and a fibroblast (F) are seen in theconnective tissue space. (xl5,600.)

16Fig. 16. A part of an arteriole found in the ciliary body. The smooth muscle cells (M ) aroundthe vessel contain only a small number of cytoplasmic organelles. Collagen fibrils (cf) an delastic fibers (ef) are seen around the vessel. En , Endothelial cell. (xl8,200.)


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Fig. 17. Three-dimensional schema of a portion of a muscle bundle of a human ciliary body.F, Fibroblast enveloping the bundle. Nm I and Nm II. Type I and II neuromuscular junc-tions, n, Nerve. Sch, Schwann cell. Dl , Desmosome-like contact points between muscle cells.Bm , Basement membrane. Bm. s, Surface view of continuous basement membrane coveringtwo separate muscle cells. N, Nucleus. M, Muscle cell, myo, Myofilaments. m, Mitochondria.ER , Endoplasmic reticulum. G, Golgi apparatus. Db, Dense bodies. No collagen fibers areshown.

DiscussionAccording to the descriptions of theuterus'13 and arteries5*r> their smoothmuscle cells are more or less enclosed bythe intercellular collagen fibers. Thecellular sheath found in ciliary muscle wasnot reported in the description of othersmooth muscles. The fibroblast sheath inthe ciliary muscle may correspond morpho-logically to the endomysial cell in themuscle spindle17 or to the Henle sheath in

nerve tissue. Functionally, on the other

hand, it might be possible to assume thatthe sheath acts as a diffusion barrier, as dothe capsular sheath cells in muscle spindlesor in epineurium. isAccording to the explanation by Shiose smuscle spindle-like tissue was distinct fromthat of "ordinary" muscle bundle. However,every muscle bundle in ciliary musclepossesses a more or less muscle spindle-like structure as shown in the present ob-servation. Nevertheless, no distinct cap-sular-sheet cells can be recognized in the


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case of ciliary muscle, as in the case of themuscle spindle.There is a morphologic basis for sug-gesting that the ciliary muscle is composedof physiologic units, i.e., the bundles ofseveral smooth muscle cells. These aggre-gates, separated from the others by fibro-blast cytoplasm, contain nonmyelinatednerves and nerve endings which may berelated to more than one cell, but onlythose of one bundle.The muscle cell in the ciliary body has a

distinct cell membrane and it seems to becertain, based on this material, that in-dividual cells are entirely separated fromeach other. At the area of most direct con-tact between adjacent cells in the ciliarymuscle, the cell membranes are notseparated by a basement membrane, andthere is a cell membrane to membraneapposition. This structure is similar to thatof the intercalated disc in cardiac muscle 10and therefore probably may be assumed tobe the site of a firm attachment device andof a pathway of conduction from cell tocell.The irregular contour of the muscle cellmembrane shown in Figs. 4 and 11 maybe interpreted as indicating contraction.Although there is no direct support of this,the absence of myofilaments from thefolded portion strongly suggests this inter-pretation.Electron microscopic studies of uterusand artery smooth muscle cells showedthem to contain relatively small numbersof organelles, mainly near both ends ofthe elongated nucleus. The smooth muscleof the arteries in the human ciliary bodyand the sphincter muscle of the iris, whichwere obtained from the same eyes used inthe present study, also have many charac-teristics similar to those of the uterus men-tioned above. In contrast, the maincharacteristic of the fine structure ofhuman ciliary muscle is the abundance ofmitochondria and endoplasmic reticulumcompared with ordinary smooth muscle.This characteristic is more conspicuous inthe radial portion. Generally, the smooth

muscle fibers of the ciliary body are re-ported to be aggregated in three groupsaccording to the direction of their longaxes, meridional, radial, and circular por-tions. In general, the muscle cells of thefirst two portions differ from each other insize, shape, and fine structures as well asin localization. For convenience's sake,these two types of cells were describedrespectively in previous observations. How-ever, such characteristics are not distinctin each part, but change rather gradually;therefore, in some parts of the ciliarymuscle, especially in the middle portionof the meridional and radial portions, themuscle cells have intermediate character-istics in all respects. In the circular portionof the ciliary muscle, the muscle cells maynot be distinguishable from those of theprevious two portions in their structuralcharacteristics except by their location. Inother words, muscle cells in the circularportion have also "intermediate character-istics" in shape, size, and fine structure.The relatively large number of cyto-plasmic organelles, especially the largenumbers of mitochondria, might suggestthat ciliary muscle cells possess higherenzymatic and functional activity thanthose of other regions. The rich endo-plasmic reticulum in ciliary smooth muscleis not arranged in a systematic pattern, asin striated muscle, but is distributed toform a framework in cells which possessgrouping of the myofilaments. In suchcases, it can be presumed that it has afunction similar to that of sarcoplasmic

reticulum.A single type of myofilament varyingfrom 30 to 80 A in diameter has beendescribed in smooth muscle cells of varioustissues by several authors. In uranyl-stainedpreparations of ciliary muscle, myofila-ments can be observed as a complex ofdense and faint filaments. Further studyof the myofilaments of smooth muscle isindicated.A dense elongated body found by almostall observers in smooth muscle generallyis also distinct in the ciliary muscle. Based


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on the present study, it seems reasonablethat this structure is an attachment deviceof the myofilaments, as suggested by Peaseand Molinari.5Boeke20 in 1932 described innervation ofciliary muscle as follows: "As far as can bemade out, here every single muscle cellseems to have its own nerve termination."In this electron microscopic study, numer-ous nerve fibers are observed, most ofwhich appear to be nerve endings. It isimpossible to estimate the number of in-nervations in the ultrathin sections. Thefrequency of occurrence of nerve endingsin single sections is very much higher inciliary muscle than in smooth muscle else-where. Three types of neuromuscular junc-tion could be recognized in the ciliarymuscle in this study. The first is an in-direct type of contact of synaptic mem-branes with an intervening basement mem-brane. The majority of nerve endings be-longing to this type were also found inthe smooth muscle of arterial walls,21 inuterus,4 and ciliary muscle.8 The secondtype is a more intimate contact of nerveand muscle without an intervening base-ment membrane. This type of contact isnot too frequent and was not reportedin smooth muscle previously. In the third,the nerve ending may be seen to lie in adepression in the muscle cell and to attachclosely to the muscle membrane over arelatively large area. This type was re-ported in uterine muscle by Caesar andassociates4 and in muscle coat of rat vasdeferens by Richardson22 and occurs rarelyin ciliary muscle. Some nerve fibers, inciliary muscle, studied in longitudinal sec-tions contained more than two synapticareas in a single nerve fiber. In such cases,most of the myoneural junctions belongedto the first type.Most blood vessels in the ciliary body arecapillaries. A few small arterioles and smallvenules are found. The endothelium of thecapillaries in the ciliary body is thin,although thicker than that of the ciliaryprocesses or of the subepithelial spaces,and has no pores. The structural difference

between capillaries in the ciliary processesand the ciliary muscle might represent afunctional difference.An attempt has been made to summarizemuch of the information obtained fromthe study of these electron micrographs ina schematic drawing, Fig. 17.I wish to thank Professor George K. Smelserfor his encouragement during the course of thiswork, his valuable suggestions and helpful con-tribution in discussions throughout this study.I am also indebted to Drs. G. Clark, R. M.Ellsworth, C. A. Perera, and A. B. Reese for their

cooperation in obtaining the surgical material.REFERENCES

1. Shoenberg, C. F.: An electron microscopestudy of smooth muscle in pregnant uteaisof the rab bit, J. Biophys. & Biochem. Cytol.4: 609, 1958.2. Mark, J. S. T.: An electron microscope studyof uterine smooth muscle, Anat. Rec. 125:473, 1956.3. Yamamoto, I.: An electron microscope studyon development of uterine smooth muscle,J. Electronmicroscopy 10: 145, 1961.4. Caesar, R., Edwards, G. A., and Ruska, H.:Architecture and nerve supply of mammaliansmooth m uscle tissue, J. Biophys. & Biochem.Cytol. 3: 867, 1957.5. Pease, D. C , and Molinari, S.: Electronmicroscopy of muscular arteries, J. Ultrastruc-ture Res. 3: 447, 1960.6. Parker, F.: An electron microscope study ofcoronary arteries, Am. J. Anat. 103: 247,1958.7. Moore, D. H., and Ruska, H.: The finestructure of capillaries and small arteries, J.Biophys. & Biochem. Cy tol. 3: 457 , 1957.8. Shiose, Y.: Electron microscopic studies onthe ciliary muscle, Acta Soc. Ophth. Jap. 65:375, 1961. (In Japanese.)9. Luff, J. H.: Improvements in epoxy resinembedding methods, J. Biophys. & Biochem.Cytol. 9: 409, 1961.10. Millonig, G.: A modified procedure for leadstaining of thin sections, J. Biophys. &Biochem. Cytol. 11: 736, 1961.11. Karnovsky, M. J.: Simple methods for "stain-ing with lead" at high pH in electron micros-copy, J. B iophys. & Biochem. C ytol. 11 : 729,1961.12. Salzmann, M.: The anatomy and histologyof the human eyeball in the normal state,translated by Brown, E. V. L., Chicago, 1912,The University of Chicago Press.13. Horn, A. W.: Histology, ed. 3, Philadelphia,

1957, J. B. Lippincott Company.


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fine structure of the human ciliary muscle

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