The Egyptian Journal of Hospital Medicine Vol., 17 :167 – 186 Dec.2004 I.S.S.N: 12084 1687 -2002

Retinal Photoreceptor Fine Structure in some

Fairoze Khattab; Fahmy I. Khattab; Nagui Fares and Aman Zaki (Department of Zoology, Faculty of Science, Ain Shams University, Abbassia, Cairo, Egypt.)

Abstract

The structure of the photoreceptors of four different reptiles: the homed viper Cerastes cerastes (diurnal and nocturnal), the European Chameleo (diurnal), the gold skink Eumeces schneidrii (diurnal) and the Egyptian gecko, Tarentola annularis (nocturnal) has been investigated by light and electron microscopy. The photoreceptors of diurnal reptiles were mainly of the cone type and those of nocturnal were mainly rods. The ellipsoid region of both double rods in the nocturnals and large single cones in the species having both nocturnals and diurnal activity, consist of several mitochondria arranged in a remarkable radially gradient architecture which accommodates with the specific function of this region as a focusing device helping to condense light onto the outer segments. Moreover the principle cone of and single cone of diurnal reptiles possessed a large oil droplet in the region between the inner segment and outer segment. This droplet is thought to play a role in filtering light and so doing enhanced contrast reduce glare and lessen chromatic aberration. It is worth to mention that the outer segment of rods in nocturnal reptiles approaches a length of approximately four folds the length of the inner segments of the same photoreceptors cells. This character is of a particular interest, since the outer segment is the site of photopigments and the increase in its length magnifies its ability of light and consequently accommodate with the night vision.

Introduction The structure of retinal photoreceptors found in most scleral parts of the inner has been investigated in a variety of segment, mainly in cones, in amphibians, vertebrate species (Cohen, 1963 a & b, reptiles and ( Hailman, 1976 & Mac Braekevelt, 1972, 1975, 1989, 1992, 1994). Nichol et .al 1978).Synapses of rods and While some variation is noted between cones were first described by Dickson & species, the typical photoreceptor consists Hollenberg,1971,Borwein & Hollenberg, of an outer segment, connecting cilium, 1973). inner segment nuclear region with synaptic Rods and cones are two distinct types process and paired or double cones occur of photoreceptors of the retina were first widely in all groups below the placental described by Schultze (1867 & 1873) , he mammals, including the mammalian studied both nocturnal and diurnal marsupials (Braekevelt,1972). vertebrate species and formulated his The outer segment of the photore- duplicity theory. ceptor lies close to and intimately asso- Vertebrate retinae are duplex, ciated with the pigment epithelium ( Hogan, containing both rods operating maximally et. al , 1974). at low light intensities and cones ,operating The outer and inner segments were maximally at high insensitive and in colour connected by an eccentrically positioned vision (Borwein,1981). Some retinae had stalk (cilium) ( Fawcett, 1966 ; Borwein & been reported to contain rods only, e.g. in Hollenberg, 1973). rats, but a few cones have been shown to be Coloured or colourless oil droplets are present by Hughes (1977). permanent inclusions of the adult visual cell Rods and cones appear together in in some non mammlian species ,They are primates. The cone inner segment is much

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bulky than the rod inner segment(Miller & four studied reptiles were shown in first Snyder,1973) The difference in diameter paper in figs. (1 a, b, c & d) between the cone and rod outer segments, however is smaller in cones(Young,1971 I.Cerastes cerastes and Borwein et.al,1980). The retina of Cerastes cerastes is As part of a comparative morphol- formed of two types of cones ,large single ogical study of vertebrate photoreceptors, cones and small single cones ,The later are this report describes the fine structure of in association with the rod type segments these rods and cones in the retinae of some (Figs. 1a & 1 ).The large and small single reptiles and new observations are added to cones are composed of an outer and inner existing studies. segments. The outer segments are closely associated with the pigment epithelial cells Materials And Methods and their processes (Fig.1).The inner For this study the of four healthy segments have densly packed mitochondria adult Egyptian reptiles, the homed viper in their ellipsoid region (Figs.2 & 5).The (Cerastes cerastes),European Chameleon outer segments of large single cones are (Chameleo chameleon), gold skink short and wide (Figs.2&3).They are (Eumeces schneiderii) and Egyptian gecko occupied by double membrane disks, or (Tarentola annularis) were used. flat tened sacs (Figs.3&4). The myoid All animals under investigation were region of the large single cones displays a collected from Abou-Rawash district, Giza barrel shape and is approximately close to Governorate in Egypt. Animals were the outer limiting membrane (Figs.2&6) sacrificed and the whole of each animal and also contains numerous Golgi cisternae was quickly removed, opened at the equator with vacoules (Fig.6).Fine microvillar and fixed for 5 hours in 5% gluteraldehyde processes extend from the inner segment of buffered at pH 7.3 with 0.1 micron the large single cones which are specifically Sorensen's phosphate buffer at 4oC. The found in this species (Fig.6).The second posterior half of the eye ball was then type of cones are the small single cones removed washed in 5% sucrose in 0.1 m which appear smaller than the large single phosphate buffer (ph 7.3) (Hayat, 1970) and cones (Figs 1a,1&2).The small single cones cut into pieces less than 1mm2. The tissue have short outer segment ,which is not as was then post-fixed for 2 hours in 1% wide as the corresponding segment of the osmium tetroxide in the same phosphate large cone (Figs.1& 2).This region is filled buffer they were washed twice for 15 with flattened double membrane disks minutes in a phosphate buffer pH 7.3.then (Fig.7). dehydrated through graded ethanols to There is an accumulation of propylene oxide and embedded in aralldite. condensed mitochondria(ellipsoid) at the Semithin sections of 0.7 m thickness were apex of the inner segment of small single cut with glass knives on the 6000 MT RMC cones (Figs. 8 & 9) The ellipsoid region of ultratome. then stained with 0.25% the small single cones differ from the toluidine blue (Davis,1971) and examined ellipsoid region of the large single cones in by light microscopy. Thin sections (600- the lack of association of mitochondria and 700A0)were then cut and collected on microdroplet (Figs.7&9).The myoid region copper grids. These sections were stained in of the small single cones contains numerous aqueous uranyl acetate and lead citrate and Golgi cisternae, with numerous vacuoles examined and photographed in a JEOL (Fig.8).Each small single cone has a 1200 EXIL transmission electron cytoplasmic process that extends from its microscope. inner segment and is called the claycal process (Fig.7). Results The rods have long cylindrical outer Light microscopic examination of the segments that reach to the pigments the semi-thin sections of the retinae of all the epithelial cells. The lamellar sacs or disks are more closely packed than the

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corresponding compartment of the other The membrane surrounding the oil photoreceptor (Figs.1,5 & 7). A prominent droplets has an irregular outline with ellipsoid region is located at the apex of the several reinforcements, or dense foci at inner segment of the rod, but no oil droplets definitive points of adhesion with the or microdroplets are present (Figs.1 & external membranes of the mitochondria 7).Unlike the cones ellipsoid the that surround the oil droplet (Fig.13).These mitochondria of the rods ellipsoid are less mitochondria encircle the entire perimeter packed and are mostly elongated to oval in of the oil droplet. In the internal portion of shape (Figs.1& 7). the cone inner segments, the mitochondria A structure similar to ellipsoid are spherical, while in the external region of containing closely packed mitochondria is the inner segments they are oval, or infrequently located underneath the outer elongated in shape (Fig.12).As the limiting membrane(Fig.6). mitochondria approach the scleral portions The connecting cilium is the only of the ellipsoid, they acquire a transverse connection between the outer segment and disposition, with the cristae parallel to the the inner segment of both large cone and major axis of the mitochondria (Figs 12 & small cone (Figs.3&10).This cilium is an 15).At this level ,adhesions between the eccentrically positioned stalk containing mitochondrial membranes are frequently nine pairs of microtubules arranged observed. A greater electron density of the circumferentially. mitochondrial matrix is also noticeable in the scleral portions of the inner segments II.Chameleo chameleon (Figs.12&13) The photoreceptor layer of Chameleo The outer and inner segments are chameleon contains only the cone-type of connected by a well developed connecting photoreceptors. It comprises single and cilium (Fig.14). double cone (Figs.1b & 11). In the inner segments, glycogen The double cone consists of a granules are usually accumulated in a principal cone and an accessory cone. Both compact area,(the parabloid).In this region, the single and double cones are composed the glycogen granules are associated with of an outer and an inner segments. The several profiles of both types of inner segment posses a large oil droplet ,an endoplasmic reticulum (Fig.16). The ellipsoid, parabloid and myoid . principal cone does not have a parabloid However, the accessory cone lacks the region(Fig.11).The parabloid of the oil droplet, ellipsoid , parabloid and myoid. accessory cone is different from that of the (Figs. 1b & 11) single cone by its remarkable circumfe- The double cone consist of a principal rential limiting membrane(Fig.11).The cone, which posses an oil droplet in the myoid region of single cones contains scleral portion of its inner segment and an cytoplasmic vacuoles and Golgi apparatus accessory cone which never has an oil (Fig.17).The myoid region of the double droplet (Figs.11& 12).The outer segment of cones displayed a similar fine structural both types of cones, is filled with double features of the corresponding area of the membrane disks, or flattened disks and single cone. slightly tapers (Fig.13). The claycal processes are thin III. Eumeces schendrii: cytoplasmic extensions from the distal end The retina of the Eumeces schendrii is of the inner segment and they form a extremely of cone dominant with very few palisade around the proximal outer segment rod. All cones are single cones and multiple of both single and double cones photoreceptors are not present(Figs.1c & (Figs.12&13). Regardless of the type of 18).The cones are large cells with project cone to which they belong ,the oil droplets through out the outer limiting membrane are oval shape and the lipid matrix is of a (Fig.19).All cones outer segments display a very homogenous electron density single membrane-bound oil droplet (Figs.11&12). (Figs.19&21).Below the oil droplet a very

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large accumulation of mitochondria (the vacuoles, accumulation of rough ellipsoid),with an aggregation of glycogen endoplasmic reticulum and the Golgi (parabloid) (Figs.19,21&22). apparatus (Figs.24 & 27).The outer segment The parabloid is followed by the inner of both types of rods composed of segment (myoid) which is rich in Golgi bimembranous disks (Figs. 24,26 & 29). complexes and cytoplasmic vacuoles (Figs.22&23). List of Figures The cone outer segments are Fig.1:Electron micrograph of the Cerastes relatively short and taper distally cerastes retina photoreceptor layer (Figs.19&20).Rod photoreceptors are much showing the interdigitation of the mela- narrower than cones and their inner nosomes (Me) containing cytoplasmic segments are smaller than cone inner process of retinal pigment of epithelial segments(Fig.20). layer (RPE) are closely associated with A prominent ellipsoid is located at the the outer segment (os) of photorec- tip of the inner segment, but no oil droplet eptors layer. The photoreceptors are are recognized(Fig.20).Rods outer segment formed of large single cones (Lsc), are longer than those of cones outer small single cones (ssc) and rods (R). segment and are not taper distally(Fig.20). X 4500 Fig.2:Electron micrograph showing photo- IV-Tarentola annularis receptors layer of Cerastes cerastes The photoreceptor layer of Tarentola retina layer, with small single cones annularis contain only the rod-type of (ssc) and large single cones (Lsc) photoreceptors.It comprises single and consists of a lamellated outer segment double rods (Figs,1d & 24).The double rod (os) and a large dense inner segment consist of a principal rod and an accessory which contains dense ellipsoid region rod(Figs.1d & 24).Both rods are composed (e) and a myoid region (my).The outer of long outer segment, ellipsoid and a limiting membrane is also indicated myoid. However, the principal rod has (olm). X 6000 characteristic parabloid body (Figs.24 & Fig.3:Electron micrograph of a large single 26).In addition, it posses a long outer cone in Cerastes cerastes photore- segment. The inner segment of the principal ceptor showing connecting cilium (cc) rod contains in its upper region, condensed joining the outer segment (os) and inner aggregation of mitochondria (ellipsoid). segment (Is). X 30000 The mitochondria occupying the Fig.4:Electron micrograph of Cerastes peripheral region of the ellipsoid are cerastes photoreceptor the outer elongated and contain well defined cristae. segment (os) of a large single cone The central mitochondria are highly elec- showing numerous double membr-anes tron dense. Below this area is an aggreg- parallel disks. X 90000 ation of glycogen particles, the parabloid Fig.5:Electron micrograph of Cerastes region (Figs.24&27).After the parabloid, cerastes photoreceptor a large single the myoid region contains numerous Golgi cone and the outer segment of a rod zones(Fig.24), the accessory rod consists of (Ros).The ellipsoid region (e) of a large a long outer segment (Fig.1d).The ellipsoid single cone showing mitochondria (mi) region of the accessory rod contains few packed with moderate electron dense aggregation of rounded mitochondria micro droplets (Md).The outer segment (Fig.25). Below the ellipsoid ,the long (os) of the short cone consisting of myoid region contains Golgi zones parallel disks. X15000 (Fig.29). Fig.6:Electron micrograph of photoreceptor The single rod contains a large outer layer in Cerastes cerastes retina segments (Figs.1d & 24), the ellipsoid showing a large single cone (Lsc.) with region with an aggregated rounded their round nucleus (N) and small mitochondria (Figs.25 & 26),and the myoid single cones (ssc) with their ellipsoid which contains several cytoplasmic region (e) lying above the outer limiting

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membrane (olm) However, unusually showing the presence of oil droplet (od) existing small ellipsoid region (e) lying only in the single cone (SC) and in the underneath the outer limiting membr- principal cone (pc) of the double cone ane is also shown. X 16000 (DC) ,and its absence from the Fig.7:Electron micrograph of photoreceptor accessory cone (AC). Clayal process layer in Cerastes cerastes retina show- (CP) surrounds the outer segment (os). ing a large single cone (Lsc.) with X 12.000 densely packed mitochondria (mi) in Fig.13:High magnification in Chameleo this cisternae ellipsoid (e) region. The chameleon photoreceptor layer showing myoid region contains Golgi apparatus a part of the principal cone, several (Ga),many cytopla-smic vacuoles (V) mitochondria (mi), enclose a position to and lateral microvillar processes a large oil droplet (od), lamellated outer (MV).The ellipsoid region of rod (Re) segment (os) and a clayal process (Cp). conta-ins a few elongated mitochondria X 60.000 (mi).The outer segment (Ros) of rod is Fig.14:High magnification in Chameleo long and has a very narrow lamellated chameleon photoreceptor layer of an structure. X 16000 accessory cone showing a connecting Fig.8:Electron micrograph of Cerastes cilium (cc) between its inner segment cerastes photorceptors showing a small (IS) and outer segment(os). X 75.000 single cone, the ellipsoid (e) region Fig.15:High magnification in Chameleo with densely stained mitochondria (mi), chameleon photoreceptor layer electron clayal process (CP) and outer segment micrograph of the ellipsoid(e) region (os). X 30000 and parabloid area (p) of double cone. Fig.9:Electron micrograph in the Cerastes The ellipsoid region contains several cerastes photoreceptor of a group of mitochondria (mi) ,smooth endoplasmic small single cones. Each cone consists reticulum (SER) and several small of an ellipsoid (e) with densely packed granular structure (arrow heads) mitochondria (mi) and a myoid (MYL) X 30.000 region with Golgi zone (Ga) and Fig.16: Electron micrograph in Chameleo cytoplasmic vacuoles (V).The nuclei of chameleon photoreceptor layer of photoreceptors(N) lie underneath the parabloid region showing dispersed outer limiting membrane (olm). X 4500 glycogen granules (gl) and several Fig.10:Electron micrograph in Cerastes profiles of both types of endoplasmic cerastes photoreceptor showing a small reticulum (ER). X 30.000 single ,connecting cilium (cc) joining Fig.17:Electron micrograph in Chameleo the outer segment (os) and the inner chameleon photoreceptor layer show- segment cone (Is). X 16000 ing the outer limiting membrane (olm) Fig.11:Electron micrograph of photore- and myoid (my) region of photore- ceptor layer in Chameleo chameleon ceptor which contains prominent Golgi showing single cones (SC) and double apparatus (Ga) and cytoplasmic vacu- cones (DC).The double cone comprises oles (V). Numerous cytoplasmic proce- a principle cone (PC) and an accessory sses of Muller cells (Mu) are also cone (AC). Each cone consists of an shown. These cells possess several fine outer segment(os), oil droplet (od), microvillar processes (F) and contain ellipsoid (e), parabloid (p) and myoid several mitochondria. Muller cells (my).This layer of photorec-eptors is processes surround the inner most interiorly boarded by the outer limiting region of the photoreceptor cells which membrane (olm). Apical processes contain prominent nucleoli (nu). (Ap) from the retinal pigment X 12000 epithelium extend between the Fig.18:Electron micrograph in Chameleo photoreceptors. X 4500 chameleon photoreceptor layer Fig.12:Electron micrograph in Chameleo showing the interdigited cytoplasm of chameleon photoreceptor layer processes of retinal pigment epithelium

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cells with the photoreceptors single of the principal rod contain a well cones (SC). X 6000 developed Golgi zone (Ga).The single Fig.19:Electron micrograph of photore- rod (Sr) consists of an outer segment ceptor layer in Chameleo chameleon (ros),ellipsoid (e) and myoid (m).fine showing single cones with their charac- processes of Muller cells (F) and outer teristic outer segment (os), oil droplet limiting membrane (olm) are also (od), ellipsoid (e), parabloid (p) and located. X 6000 myoid (my).The outer limiting Fig.25:Electron micrograph of the membrane (olm) and cones nuclei (N) photoreceptor in Tarentola annularis also indicated. X 12000 retina showing the accumulation of a Fig.20:High magnification electron micro- large number of mitochondria in the graph of Chameleo chameleon of ellipsoid of the principal rod (Pmi), photoreceptor revealing rod outer accessory rod (smi). X 15000 segment (Ros),rod inner segments Fig.26:Electron micrograph of the photor- (RIS),a conical shaped outer segment of eceptor in Tarentola annularis showing a cone (os),oil droplet (od) and a cone a double rod .Its principal rod has a inner segment (CIS). X 18000 condensed ellipsoid (e) with peripheral Fig.21:High power electron micrograph of rounded and elongated mitochondria Chameleo chameleon photoreceptor (Pmi) and a parabloid (p).The accessory layer showing a part of a single cone rod has an ellipsoid (ae) containing with several mitochondria (mi) in close only mitochondria (mi). X 12000 position to a large oil droplet (od) and Fig.27:Electron micrograph of Tarentola lamellated outer segment (os). X 45000 annularis photoreceptor layer showing Fig.22:Electron micrograph of the inner a single rod with an outer segment (os) region of Eumeces schendrii photore- and an ellipsoid.The ellipsoid contains ceptor showing ellipsoid area (e) and rounded mitochondria (mi),while the myoid region (my) with prominent myoid region is rich with rough Golgi apparatus (Ga) and cytoplasmic endoplasmic reticulum (RER).The vacuoles (v).Microvillar processes (F) ellipsoid (e) and parabloid (p) of the of Muller cells are also shown. principal rod are also indicated. The X 18000 microvillar processes (F) of Muller Fig.23:Electron micrograph of myoid cells are also located. X 12000 region of Eumeces schendrii photo- Fig.28:Electron micrographs in the receptor showing prominent Golgi Tarentola annularis showing a group of apparatus (Ga), a large portion of nuclei (N) of photoreceptors of both Muller cells with fine microvillar single rod (Sr) and double rods (Dr). processes (F),and cytoplasmic pro- Processes of Muller cells (Mu) are cesses of Muller cells (Mu) beneath the extended between these cells and the outer limiting membrane(olm). photoreceptor fiber(Pf). X 6000 X 30000 Fig.29: An electron micrograph in Fig.24:Electron micrograph of photore- Tarentola annularis showing a myoid ceptor layer of Tarentola annularis region of double rods containing Golgi showing a group of double rods and zones (Ga) and a typical euchromatic single rods (Sr).Each double rod nuclease (N).The outer limiting consists of a principle rod with a large membrane (olm) and the microvillar condensed ellipsoid (e), parabloid (P) processes of Muller cells (F) are also and an accessory rod (are) with outer seen. X 18000 segment (aros).The myoid region (my)

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Discussion

The photoreceptor layer varied greatly microscopy in the bobtail goanna (Tiliqua in its histological and fine structural details rugosa),an Australian diurnal among the four different reptilain species. (Braekevelt,1989).He reported that the This variation is mainly contributed to the photoreceptors in this species were readily number, distribution and existence of the divisible into rods or cones based on principal cell type of this layer, the rods and morphological criteria. Single cones were the cones. These cells represent the actual dominant cell type with a cone, rod ratio of receptors of the retina and are highly about 80: 1. sensitive to light stimuli (El-dawi & In the present work, the photoreceptor Swelim,1995) .In principle, the rods layer of the retina of the diurnal lizard, mediate dim-light vision, whereas cones Chameleo chameleon contains only pure function in bright light (Blanks,1994).In cones differentiated into single and double addition rod provide great sensitivity, cones. Each double cone comprises a especially to blue-green light (scotopic principal cone and an accessory cone. Both vision),whereas cones provide visual acuity the principal and single cone possess a for pattern detection as well as colour characteristic large oil droplet, between vision (Blanks,1994). their outer and inner segments. Early In the present work, the investigations of photoreceptor organization photoreceptors layer of the viper Cerastes suggest that strictly the diurnal vertebrates cerastes appeared in both the light and ,including ,snakes, some birds and electron microscopes consisting of both majority of squirrel family have pure cone types of photoreceptors, rods and cones. retinae (Walls,1967) . Williams' and Fisher The cones were of two types, small single (1986) found that the diurnal lizards cones and large single cones. This morpho- sceloporus occidentalis has only cone logical architecture of the photoreceptors photoreceptors. Recently, some authors layer may accommodate with the living recorded that the pure-cone American habitat of this viper which has both Chameleon retina all visual opsins nocturnal and diurnal activity .In compa- including rod opsin are expressed rison with other vipers ,Underwood(1970) (Kawamura & Yokoyama 1997). reported the presence of both types of the In the present work, the photoreceptor photoreceptors in the retina of Heterodon layer of Tarentola annularis, a nocturnal platyhinos which has both nocturnal and lizard consist of pure rods. These rods are diurnal activity. of two types, single rods and double rods. On the other hand Wong (1989) The later comprise principal rods and described three morphological types of accessory rods. This histological finding cones (large single cone, small single cone accommodates with either studies on the and double cones ) in the retina of the retina of Gecko sp. and Hemidactylus sp. American garden snake Thamnophis sirtails (Pedler & Tilly,1964) and Tarentola sp. and ,which is active only during the day light Phyllodactylus sp. (Underwood,1970) .In (diurnal snake). other related species, Gecko gecko, the In the present study, the photoreceptor photoreceptor layer contains both single layer of the diurnal lizard, Eumeces and double rods (Crescitelli,1977). scheindrii consist mainly of single cones, in In the present work, the electron association with a very few number of rods. microscopic studies revealed certain No multiple photoreceptors were present common fine structural features the outer nor a photoreceptor mosaic was observed, segments of both rods and cones in the four although it is common feature in diurnal different reptilian species. Each segment lizards (Dunn,1966). consists of a stack of bimembranous discs, The fine structure of the retinal which revealed by other investigators as the photoreceptors has been studied by electron site of photopigments and represent the

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light capture area of the photoreceptors helping to condense light onto the outer (Braekevelt & Richardson,1996). segment( Borwein,1981). As a matter of fact, rod cells are The ellipsoid may act as a convex lens sensitive to light because they contain a to enhance the vision ability in these visual pigment called rhodopsin which is nocturnal animals. capable of trapping photons (Blanks,1994). On the other hand the mitochondria in The outer segment of rods of Tarentola the ellipsoid area of Eumeces schenrdii and annularis are typically elongated cylinders. Chameleo chameleon have another linear The outer segment of cones are much more orientation at the long axis of this area. This variable in shape than those of rods; they linear organization of the mitochondria tend to be small and conical as in Chameleo reflects an unneccessary requirement of the chameleon and small single cones in ellipsoid area in these diurnal animals for Cerastes cerastes and single cones of light condensation onto the outer segment. Eumeces scheindrii. The parabloid area was absent from The morphological architecture of the the rods and cones of Cerastes cerasts.This photoreceptor layer Chameleo chameleon subcellular structure consists of smooth reflects a diurnal adapted activity of these surface membranes of endoplasmic reticu- animal due to the presence of pure cones, lum, and an abundance of glycogen gran- similar studies, Kawamura and Yokoyama ules, which accumulate later though (1998) revealed the ability of similar development (Borwein,1981). This organ- species of Chameleon for night vision. elle may affect optical function in these In addition, the photoreceptor layer of the animals (Amemiya & Ueno,1977). Egyptian Gecko, Tarentola annularis Pedler (1969) found that in the accommodates with the nocturnal activity nocturnal gecko the parabloid merged with due to presence of pure rods, Kojima et al. the surrounding cytoplasm, but that it was (1992) reported that the retina of Gecko definitively demarkated in diurnal geckos. gecko has two kinds of visual pigments. The glycogen of the parabloid does not Taniguchi et al.(1999) found that despite seem to be depleted in frogs even after long the large morphological difference between starvation (Gourevitch,1954) or by light the diurnal and nocturnal gecko and dark stimulation (Yamada,1960). photoreceptor types. In the inner segment of certain types In the present work ,light and electron of photoreceptor in Chameleo chameleon, microscopic studies of the inner segment of Eumeces schenrdii and Tarentola annu- photoreceptor layer revealed the presence laris, a multiple profiles of rough endopla- of three different highly specialized areas smic reticulum and Golgi zones occupied a which varied greatly not only in the two vitreal position in respect to the associated major types of photoreceptors(rods and parabloid, this area is defined as the myoid. cones) but also in each types of cells in the In Cerastes cerastes this subcellular four different reptilian species. These areas structures was located directly vitreal to the are ; the ellipsoid, parabloid and myoid. ellipsoid. Bok, (1970) revealed that RNA The ellipsoid areas is an aggregation synthesized in the nucleus travels to myoid, of different sized mitochondria ,whose which is rich in ribosomes which are the distribution and orientation varied greatly site of protein synthesis. among the four different repitalian species. During photo mechanical movements In the Cerastes cerastes and Tarentola the myoid can shorten up to 90% of its annularis, the mitochondria have a radial length within two minutes to one hour in gradient with the smallest ones are at fish, amphibians and birds depending on periphery of the ellipsoid. This radial species (Ali,1971 and Reme & Sulser1977). gradient of mitochondria reflects a In Chameleo chameleon a large single functional significant in the ability of these oil droplet was found in the apex of the animals for the night vision, since the inner segment of the principal cones and ellipsoid area acts as a focusing device, single cones.

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But in Eumeces schendrii the large oil eyed'' fish, Anableps anableps L.J. droplet was found in the apex of the inner Morph.,140:405-442. segment of single cones. 7. Borwein, B. Borwein, D. Medeiros, J. In Cerastes cerastes a large number of and Mc Gowan, J. (1980): The ultrastru- dense micro droplet occupied an approx- cture of monkey foveal photoreceptors, with special reference to structure, shape, imately central position in the apex of the size and spacing of the foveal cones.Am. J. large cones inner segments. No oil droplet Anat.,159:125-146. or micro droplets were found in Tarentola 8. Braekevelt, C. R. (1972):Fine structure of annularis. The morphological structure of the retinal pigment epithelium and the droplets varied from large single as in photorecptor cells of an Australian amphibians, fish, and birds marsupial Setonix brachyurus. Can. J. (Hailman,1976, Kunz & Wise,1978, Kolb Zool.,51:1093-1111. & Jones,1987, Braekevelt 1989, Braekevelt 9. Braekevelt,C. R.(1975):Photoreceptor fine & Richardson,1996) to a less observed structure in the northen pike.(Escox lucius). smaller droplets as in geckos and snakes J. Fish. Res. Board Can. 4: 281-285. 10. Braekevelt, C. R.(1989):Photoreceptor (Ishikawa & Yamada, 1969,&Wong 1989). fine structure in the bobtail goanna (Tiliqua Oil droplets apparently selectively rugosa).Histo. Histopathol.,3:33-38. filter light and is so doing probably enhance 11. Braekevelt, C. R.(1992):Retinal epithelial contrast, reduce glare and lessen chromatic fine structure in the southern fiddler ray aberration(Meyer,1977).The most striking (Trygonorhia fasciata). Histo. Histopathol. feature of the retinas of diurnal form is the ,7:275-282. presence of brightly coloured oil droplets. 12. Braekevelt, C. R.(1994): Fine structure of The synaptic terminal is the photo- the retinal pigment epithelium in the Port receptor site where information is excha- Jackson Shark (Heterodontus phillipi). nged or transmitted and its structure is so Anat. Embroyl.,190:501-506. 13. Braekevelt, C. R. and Richardson, K. consistent that Pedler (1969) who studied (1996): Retinal photoreceptor fine structure 71 vertebrate species, regarded it as the in Australian Galah (Eolophus roseicap- most reliable indicator of whether the illus). Histo. Histopathol.,11:555-564. photoreceptor is cone like or rod like. 14. Cohen, A. (1963a): Vertebrate retinal cells and their organization. Biol. Rev. Cambridge Philos. Soc.,38:427-459. References 15. Cohen, A. (1963b): The fine structure of the visual receptors of pigeon.Exp. Eye. 1. Ali,M.A.(1971): Les reponses retinom- Res.,2:88-97. otrices: Caracters et mecanimes. Vision 16. Crescitelli, F. (1977): The visual pigments Res.,11:1225-1288 of geckos and other vertebrates :An essay 2. Amemiya, T. and Ueno, S. (1977): in comparative biology. In :Handbook of Electron microscopic and cytochemical Sensory phsiology, vol.VII 15. ed. By study on development of the paraboloid of Crescitelli, F. Berlin, Springer. accessory cone of chick retina. Cell Mol. 17. Davis,D. (1971): Histopathologic Technic Biol., 22: 313-321. and practical Histochemistry.Mc Graw- 3. Blanks, J.(1994):Morphology of the retina. Hill, New York 3rd ed.,112. In: Retina ed. by Ryan, S.J. Mosby, 18. Dickson, D. and Hollenberg, M. (1971): London, Chicago, Madrid, Sydney. The fine structure of the pigment 4. Bok, D. (1970): The distribution and epithelium and the photoreceptor cells of renewal of RNA in retinal rods. Invest. the newt, Triturus viridescens dorsalis. J. Opthalmol.,9:516-523. Morphol., 135:389-432. 5. Borwein, B. (1981):The Retinal Receptor: 19. Dunn, R. (1966): Studies on the retina of In Vertebrate Photoreceptor Optics, vol.23, the gecko Coleonyx variegatus 2.The ed. By Enoch, J. M. and Tobey, F. rectilinear visual cell mosaic.J. Ultrastruct. Springer, Verlag, Berlin, Heidelberg, New Res., 16:672-684. York. 20. El-Dawi, E. F. and Swelim, H. (1995): 6. Borwein, B. and Hollenberg, M. J. Comparative histological studies on the (1973):The photoreceptors of the ''four- retina of some Nile teleostes in correlation

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with their mode of life.Egypt J. Histol., 33. MacNichol, E.; Kunz, Y. W.; Levine, J. ; 18:221-233. Harosi, F. and Collines, B. (1978): 21. Fawcett, D.W. (1966):An Atlas of Fine Ellipsosomes: organelles containing a Structure. The cell, its organelles and cytochrome-like pigment in the retinal inclusions. Saundars, Philadelphia. cones of certain fishes. Science 200:549- 22. Gourevitch, A. (1954): La localisation 551. histologique du glycogene dans laretine des 34. Meyer, D. (1977): The avian eye and its poissons. C.R. Soc. Bio.,148:213-215. adaptations. In: Handbook of sensory 23. Hailman, J. (1976):Oil droplets in the eyes physiology .Vol VII / 5.The of adult anuran amphibians. A comparative in vertebrates,ed. By Crescitelli, F. Springer survey. J. Morphol.,148: 453-468. Verlag Berlin. 24. Hayat, M. (1970): Principles and techni- 35. Miller, W. and Snyder, A .(1973): Optical ques of Electron Microscopy. Harper and function of human peripheral cones. Vision Row, New York. 1st ed.,343. Res. 13:2189-2194. 25. Hogan, M. J.; Wood, I. And Steinberg, 36. Pedler, C. (1969): Rods and cones : a new R. (1974):Cones of human retina : approach. Int. Rev. Gen. Exp. Zool.4:219- Phagocytosis by pigment epithelium of 274. human retinal cones. Nature London, 37. Pedler, C. and Tilly, R. (1964): The nature 252:305-307. of the gecko visual cell. A light and 26. Hughes, A .(1977):Topography of vision in electron microscopic study, vision. Res., 4 Mammals of contrasting Life Styles: :499-510. ''Comparative Optics and Retinal 38. Reme, C. and Sulser, M.(1977): Diurnal Organization''. In: The visual system in variation of autophagy in rod visual cells vertebrates, Handbook of Sensory in the rat. Graefe's Arch. Opthalmol., Physiology , Crescitelli, F. ed. By Springer, 203:261-270. Berlin ,Heidelberg, New York,715:613- 39. Schlutze, M. (1867): Uber stabchen und 756. zapfen der Retina. Arch. Mikrosk. Anat., 27. Ishikawa, T. and Yamada, E. (1969): A 3:215-247. typical mitochondria in the ellipsoid of the 40. Schlutz, M. (1873):''The retina", In:Manual photoreceptor cells of vertebrate retinas. of Human and Comparative Histology, vol. Invest. Ophathalmol., 8:302-316. III, ed. By Stricker, S. New Syndentham 28. Kawamura, S. and Yokoyama, S.(1997): Soc., London, 218-298. Expression of visual and nonvisual opsins 41. Taniguchi Y.; Histomi O.; Yoshida M in American chameleon. Vision. Res., and Tokunaga, F. (1999): of 37:(14) 1867-1871. visual pigments in geckos. FEBS lett 29. Kawamura, S. and Yokoyama, 19;445(1):36-40. S.(1998):Functional characterization of 42. Underwood, G.(1970):The eye, In :The visual and nonvisual pigments of American Biology of the Reptilia.ed. By Gans, C. chameleon.(Anolis carolinensis).Vision vol.II Academic press London and New Res., 38:(1) 37-44. York. 30. Kojima, D.; Okano, T.; Fukada, Y.; 43. Walls, G. L. (1967):The vertebrate eye and Shichida, Y.; Yoshizawa, T. and Ebery, its adaptive radiation. New York Hafner. T.B. (1992):Cone visual pigment is present 44. Williams, D. and Fisher, S.K. (1986):In in gecko rod cells. Proc. Natl. Acad. Sci. vitro maintenance of pure-cone retina. USA.89:6841-6845. Invest. Opthamol. Vis. Sci.,27 :666-673. 31. Kolb, H. and Jones, J. (1987): The distin- 45. Wong, R. (1989):Morphology and ction by light and electron microscopy of Distribution of Neurons in the Retina of the two types of cone containing colorless oil American Garter Snake (Thamnophis droplets in the retina of the turtle. Vision sirtalis).J. Comp. Neurol.,283: 587-601. Res.,27:1445-1458. 46. Yamada, E. (1960):observation on the fine 32. Kunz, Y. and Wise, C. (1978):Structural structure of photoreceptors elements in the differences of cone oil droplets in the light vertebrate eye. J. Elect. Microsc., 9:1-14. and dark-adapted retina of Poecilia 47. Young, R. (1971):The renewal of rod and reticulata. P. Experientia, 34:246-249. cone outer segments in the rhesus monkey. J. Cell Bio., 49:303-318.

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دراسات بالميكروسكىب الضىئي و الميكروسكىب االلكترووي علي طبقة مستقبالت الضىء في شبكة العيه في بعض السواحف.

)فيروز خطاب , فهمي خطاب , واجي فارش و أمان هللا محمد زكي ( )قسن علن الحيواى-كلية العلوم- جاهعة عيي شوس(

تتضمموي همملٍ الة اقممة هاا ًممة الت كيمم الٌسممي و ا الممةقيب ل ماممة هسممتام الضممو لشمكية العيي بيي أًواع هختلفة هي الزااحف هٌها الٌها ي كالح بما اوا ابيمة ا أم الحيما ا الليلو هثل الم ص باعو الٌاظ ا زااحف لها ًشاط ليلو ا ًها ي هثل الحية الوا ًة. ا قة إختلفت طماة هستام الضو إخت فا كمي ا بيي الزااحف او بعمة,ا كماى هملا اإلخممت و اا مم فممو اوشمممكا ال ئيسممية لهمملٍ الخ اممما كاوشممكا الوخ اطيممة ا اوشمممكا العضواة.فاة إحتمو شممكة العميي الوا ًمة علمو هخما اظ أحايامة مخي ي ا هخما اظ أحايامة كمي ي هع اجوي عصمو , كوا إحتو هستام الضو فو شمكية أم الحيما علمو هخما اظ أحاياة مخي ي ا قليمل همي العصممو, بيٌوما إحتمو هملٍ ال مامة فمو الح بما اوا ابيمة علمو هخما اظ فامظ بعضممها أحمايي الت كيمم ا الممعن ايخمم كٌمائو الت كيمم . إشمتولت الوخمما اظ كٌائية الت كي علو احةي أقاقية ا أخ ى هساعةي. ا قة ظه هلٍ ال ماة فو الم ص باعو الٌاظ ا بها هسمتام الضمو همي الٌموع العضوي فاظ ا كماى بعضمها أحمايي الت كيم ا ايخم كٌمائو الت كيم .ا قمة إشمتولت أاضما العصمو كٌائية الت كي علو احةي أقاقية ا أخ ى هساعةي .ا قة تويز هسمتام الضمو هي الٌوع العضوي فمو المم ص بماعو المٌاظ فامظ ب مو ق اعهما الخا جيمة هاا ًمة بمالا ع الةاخلية لٌفس الخ اا. احتو الوٌ اة الةاخلية لوستام الضو فو كل هي المم ص بماعو المٌاظ ا الحيمة الوا ًمممة علمممو أعمممةاي كميممم ي هت ا مممة همممي الويتوكوًمممة اا شمممةاةي الكثافمممة.بيٌوممما إًتشممم الويتوكوًة اا فو هلٍ الوٌ اة فو الٌوعيي اوخ اي )الح با اوا ابيمة ا أم الحيما ( بشمكل هتماعة ا تويز بالت كي الوا وع افها الةاخلية. ا قة إحتو أاضا الا مع الةاخليمة فمو ك كممة أًممواع فاممظ هممي الزااحممف علممو هٌ اممة اا ممحة هممي الما ابلواممة )ت وممع كثيممف هممي ال ليكوجيي( بيٌوا إختفت هلٍ الوٌ اة فو الحية الوا ًة.

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