Australian Journal of Basic and Applied Sciences, 3(3): 2064-2077, 2009 ISSN 1991-8178

Corresponding Author: Ahmed I. Dakrory, Department of Zoology, Faculty of Science, Cairo UniversityE-mail: dakrory2001@yahoo.com

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Comparative Anatomical Study on The Ciliarly Ganglion of Lizards

(Reptilia - Squamata - Lacertilia)

Ahmed I. Dakrory

Department of Zoology, Faculty of Science, Cairo University

Abstract: The ciliary ganglion is a well-defined ovate ganglionic mass in the three species studiedUromastyx aegyptius, Sphenops sepsoides and Varanus griseus. The ganglion consists of bipolarneurons in the three species studied. In both Uromastyx and Sphenops the neurons are of two sizeslarge and small, while in Varanus they are of one and the same size. In the three species studied, theciliary ganglion has three roots, parasympathetic (motor), sympathetic and sensory roots. Theparasympathetic root is represented by the radix ciliaris brevis which arises from the ramus inferiorof the nervus oculomotorius. The sympathetic root arises from the internal carotid plexus and joinsthe ganglion in both Sphenops and Varanus while it jnoins the ciliary nerve in Uromaxtyx. Thesensory root is formed of the radix ciliaris longa which connects the ramus nasalis of the nervustrigeminus and the ciliary ganglion in Varanus and the ciliary nerve in Sphenops and both inUromastyx. The ciliary ganglion gives off one ciliary nerve in both Uromastyx and Sphenops whereas,it gives rise to two nerves in Varanus.

Key words: Ciliary ganglion - Lacertilia - Uromastys aegyptius - Sphenops sepsoides Varanus

griseus.

INTRODUCTION

The ciliary ganglion is a cranial parasympathetic ganglion that is located in the postorbital region of thehead in the majority of vertebrates. Such ganglion is well represented in reptiles, birds and mammals. However,it seems to be transitory or absent to large extent in Amphibia (Norris, 1908; Kuntz, 1914; Paterson, 1939;Dakrory, 2002). Among fishes, the ciliary ganglion is either present and well developed (Freihofer, 1978;Piotrowski and Northcutt, 1996; Dakrory, 2000 & 2003; Ali and Dakrory, 2008) or totally absent (Jenkin,1928; Chandy, 1955). In reptiles, the ciliary ganglion together with the ocular muscles and their nerves arevestigial in the blind snake Leptotyphlops cairi (Abdel-Kader, 2005).

Functionally, the ciliary ganglion plays a major role in both the accommodation of the eye and animalbehavior (Evans and Minckler, 1938; Bullock et al., 1977; Guyton and Hall, 1996). Dakrory (2003) observeda close relation of the ciliary ganglion development and habit of the fishes. The ganglion is well developedin the diurnal and surface feeding fishes and is poorly developed in the fishes living in turbid lightless water,nocturnal fishes and bottom feeding fishes.

The nature of the ciliary ganglion and its relation in reptiles has attracted the attention of anatomists a longtime ago; Haller von Hallerstein (1934), Evans and Minckler (1938), Santamaria-Arnaiz (1959), Soliman(1968), Mostafa and Hegazy (1990), Mostafa (1991) and Abdel-Kader et al. (2007). There was an obviouscontradiction between the observation of Haller von Hallerstein (1934) and that of Santamaria-Arnaiz (1959)on the formation of the ganglion. So, this point needs further investigation.

The ciliary ganglion possesses two roots; radix ciliaris brevis and radix ciliaris longa in lacertilian species(Soliman, 1968) and in Agama sinaita and Stenodactylus slevini (Mostafa and Hegazy, 1990), where as inEumeces schneideri extra-sympathetic root from the carotid plexus is observed.

The sympathetic connection with the ganglion in reptiles has not yet been well-defined (Soliman, 1968;Mostafa and Hegazy, 1990; Mostafa, 1991; Dakrory, 1994; Abdel-Kader, 2006; El-Bakry et al., 2007; Abdel-Kader et al., 2007). The number of the ciliary nerves arising from the ganglion varies from one to three amongreptiles.

There are conflicting points of view among investigators, not only rgarding the origin of the ciliaryganglion, but also in regard to the nature of its cells, the number of ganglion roots, its sympathetic connection

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and the number of ciliary nerves. This wide diversity in the opinions about the ciliary ganglion and itsrelationships seems to be a sufficient reason for the study of this subject.

From the present point of view, this study may anticipate for a new anatomical evidence from lacertilianto support ideas in the reptilian evolution. Also, it may help us to understand the phylogenetic relation betweenLacertilia and other reptiles.

MATERIAL AND METHODS

Three lacertilian species belonging to three different families were choosen for this study; Uromastyx

aegyptius (Family: Agamidae), Sphenops sepsoides (Family: Scincidae) and Varanus griseus griseus (Family:Varanidae).

Uromastyx aegyptius is also known as spiny-tailed lizard or dabb lizard. This species inhabits hard sandand gravel desert, preferring flat areas with light vegetation. It is primarily herbivorous, but occasionally eatyoung insects. It digs deep burrows in the hard soil usually with single entrance. It is diurnal species thatspends most of its walking hours basking in the sun near the burrow entrance especially at morning time. Thisspecies is adapted to the arid habitat. It is found throughout North Africa, Middle east across south-central Asiaand into India. Female dobb lizard can lay from 5 to 40 eggs. The eggs are laid (at July to August)approximately 30 days after copulation with an incubation time of 70-80 days. The specimens are collectedfrom Gabal Al-Maghara, South of El-Arish City, Northern Sinai, Egypt.

The embryos of Uromastyx were collected during the last days of the incubation period. After carefulremoving of the embryos from the shells, they were fixed immediately in an aqueous Bouin's fluid for 24hours.

Sphenops sepsoides is a sand dwelling fossorial species with extremely reduced limbs for sand locomotion.It is found in a wide variety of habitats; ranging from depressions of Western desert to the sand spots in therock wadies of Eastern desert and Sinai. It appears to be nocturnal and feeds entirely on fossorial insects (i.e.,insectivore), this species is ovoviviparous.

The embryos of Sphenops sepsoides are collected from two pregnant females in the lab. The fully formedembryos were fixed immediately in aqueous Bouin's fluid for 24 hours.

Varanus griseus griseus is a large diurnal lizard. It feeds on lizards, snakes, and rodents. This species livesin sandy areas throughout the Western and Eastern desert and Northern of Sinai. It is found in North Africaand Western Asia. The desert monitor lizards move in groups on searching for food.

Ten youngs (newly hatched) Varanus were collected from Romana tritories at El-Arish city, Northern ofSinai. These youngs, after being anaesthetized, were fixed in aqueous Bouin's fluid for 36 hours.

After fixation, the specimens of both Uromastyx and Varanus were passed into decalcificating EDTAsolution for about 30 to 50 days. Then washed in distilled water and transferred to 70% ethyl alcohol for 48hours. The embryos were embedded in paraffin wax then transversely serially sectioned at 10 μm thicknessin Uromastyx and 15 μm in both Sphenops and Varanus. The serial sections were then stained in Mallory'striple stain for Uromastyx and Varanus and in haematoxylin and then counter stained with eosin for Sphenops.The serial sections were drawn by the projector and graphic reconstructions of the ciliary ganglion were made.Photomicrographs for parts of the transverse sections were made to elucidate the position and relations of theganglion to the other structures of the head.

RESULTS AND DISCUSSIONS

Results: The ciliary ganglion in the three speices studied appears as a well-defined ovate ganglionic mass, which

is located posteriorly in the orbital region. The ciliary ganglion occupies a different position from one speciesto another.

In Uromastyx aegyptius, the ciliary ganglion (Fig. 5, G.C) located medial to both the eyeball (E) and theciliary nerve (N.C), dorsal to the rectus lateralis muscle (M.RL), ventrolateral to the rectus superior muscle(N.RS), and ventromedial to the ramus nasalis of the nervus trigeminus (R.NA.V).

In Sphenops sepsoides, such ganglion (Figs. 6 & 7, G.C) lies between the arms of the oblique U-shapedrectus lateralis muscle (M.RL). This muscle surrounds the ganglion dorsally, laterally and ventrally, it issurrounded medially by the optic nerve (OP.N).

In Varanus griseus griseus, this ganglion (Figs. 8 & 9, G.C) is situated ventrolateral to both the rectussuperior muscle (M.RS) and the ramus superior of the nervus oculomotorius (R.SP.III), ventromedial to both

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the ramus nasalis of the nervus trigeminus (R.NA.V) and the retractor occuli muscle (M.REO), dorsomedialto the bursalis muscle (M.BU) and dorsal and dorsolateral to the rectus lateralis muscle (M.RL).

The ciliary ganglion measure about 250 μm in Uromastyx aegyptius, 132 μm in Sphenops sepsoids and526 μm in varanus griseus griseus.

In the three studied lacertilian species, light microscopic investigation reveals that the ciliary ganglionconsists mainly of bipolar neurons. These cells are distinct and have the same size in Varanus (Figs. 1 & 9),while in both Uromastyx (Figs. 1 & 4) and Sphenops (Figs. 3 & 7) the ganglion consists of large (LN) andsmall (SN) cells.

In the three species investigated, the ciliary ganglion is connected with the ramus inferior of the nervusoculomotorius via the radix ciliaris brevis. The latter is large and stout in both Uromastyx and Varanus andit is small in Sphenops. It carries the preganglionic parasympathetic fibres of the nervus oculomotorius to theganglion, i.e., it is the parasympathetic (motor) root of the ganglion.

In Uromastyx aegyptius (Fig. 1, RCB), the radix ciliaris brevis arises from the dorsolateral side of theinferior oculomotor ramus just ventral to the origin of the rectus superior muscle. It runs forwards for a shortdistance, where it receives a fine branch from the radix ciliaris longa (Fig. 1) and continues to enter theganglion. In Sphenops sepsoides (Fig. 3, RCB) the radix ciliaris brevis separates from the dorsolateral side ofthe inferior ramus of the nervus oculomotorius medial to the rectus lateralis muscle. It runs anteriorly for ashort distance to enter the ganglion. In Varamus griseus griseus (Figs. 2 & 8, RCB), radix ciliaris brevisoriginates from the lateral side of the inferior ramus of the oculomotor nerve. It extends anterolaterally, passingdorsal to the rectus lateralis muscle, medial to the retractor oculi muscle, ventromedial to the radix ciliarislonga, ventral to the ramus superior of the oculomotor nerve and ventromedial to the origin of the rectussuperior muscle. Anteriorly, the radix ciliaris brevis fuses with the radix ciliaris longa just, at the posteriorextremity of the ciliary ganglion (Fig. 8).

In the present study, the light microscopic examination elucidated that, there is a connection between theramus nasalis of the ophthalmic ramus of the nervus trigeminus and the ciliary ganglion, through the radixciliaris longa. It transmits the sensory fibres of the ramus nasalis to the ganglion; i.e., it represents the sensoryroot of the ganglion.

In Uromastyx aegyptius (Fig. 1, RCL), the radix ciliaris longa arises from the ventromedial side of theramus nasalis of the ophthalmic ramus of the trigeminal nerve. It runs anteriorly in a ventromedial directionpassing ventral to the ramus superior of the oculomotor nerve and dorsal to the rectus lateralis muscle.Thereafter, it continues forwards, running ventromedial to both the rami nasalis of the nervus trigeminus andsuperior of the nervus oculomotorius, ventral to the rectus superior muscle and lateral to the radix ciliarisbrevis where a fine medial branch originates. This fine branch fuses with the radix ciliaris brevis, as previouslymentioned (Fig. 1). Shortly antertior to this fusion, the ganglion is located. The main radix ciliaris longa,continues anteriorly passing lateral to the ganglion, dorsomedial to the rectus lateralis muscle and ventral tothe rectus superior muscle. Thereafter, it becomes dorsolateral and then lateral to the ganglion; where itincorporates within the connective tissue sheath of the ganglion (Fig. 4, RCL) without intermingling with itsneurons, till it leaves the ganglion with the ciliary nerve (Figs. 1 & 4).

In Sphenops sepsoides, the radix ciliaris longa separates from the medial side of the ramus nasalis of theophthalmic ramus of the trigeminal nerve (Fig. 3, RCL). It runs anteriorly and then shifts ventrally passingdorsal and then medial to the rectus lateralis muscle. Thereafter, it runs laterally touching the ciliary ganglionfrom its dorsal side (Figs. 1 & 7, RCL), i.e., it has no synaptic relation with the ganglionic cells. Finally, itenters the ciliary nerve together with the postganglionic nerve fibres.

In Varanus griseus griseus (Figs. 2 & 8, RCL), the radix ciliaris longa originates from the medial sideof the ramus nasalis of the ophthalmic ramus of the nervus trigeminus. It runs forwards in a ventromedialdirection extending ventrolateral to the ramus superior of the oculomotor nerve, dorsolateral to the ramusinferior of the oculomotor nerve and dorsomedial to the retractor oculi muscle (Fig. 8). Shortly anterior, itshifts ventrally and laterally to fuse with the radix ciliaris brevis. Shortly anterior to this fusion the ciliaryganglion is found (Figs. 2 & 8).

In the present study, the light microscopic investigation demonstrates that there is a sympathetic connectionbetween the ciliary ganglion and the sympathetic carotid plexus in both Varanus griseus griseus (Figs. 2 &9, R.SY), and Sphenops sepsoides (Figs. 3 & 7, R.SY), while in Uromastyx aegyptius, this connection is withthe ciliary nerve after its origin from the ganglion (Figs. 1 & 5, R.SY).

In both Uromastyx aegyptius and Sphenops sepsoides there is only one ciliary nerve originating from theganglion, while in Varanus griseus griseus two ciliary nerves are found.

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Fig. (1): Reconstruction of the ciliary ganglion of Uromastyx aegyptius in a lateral view; Fig. (2):

Reconstruction of the ciliary ganglion of Varanus griseus griseus in a lateral view; Fig. (3):

Reconstruction of the ciliary ganglion of Sphenops sepsoides in a lateral view. G.C, Ciliary ganglion;LN, Large neurons; N.C, Ciliary nerve; N.III, Oculomotor nerve; Nn.C, Ciliary nerves; R.IF.III,

Ramus inferior of the nervus oculomotorius; R.NA.V, Ramus nasalis of the nervus trigeminus;R.SP.III, Ramus superior of the nervus oculomotorius; R.SY, Sympathetic ramus connecting theciliary ganglion with the internal carotid plexus, RCB, Radix ciliaris brevis; RCL, Radix ciliarislonga; SN, Small neurons.

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Fig. (4): A photomicrograph of a part of a transverse section of Uromastyx aegyptius passing in the postorbitalregion showing the shape, position and types of neurons of the ciliary ganglion. X100 (Scale bar 2mm); Fig. (5): A photomicrograph of a part of a transverse section of Uromastyx aegyptius showingthe position of the ganglion, the sympathetic ramus and the origin of the ciliary nerve. X40 (Scalebar 1 mm); Fig. (6): A photomicrograph of a part of a transverse section of Sphenops sepsoides

demonstrating the position of the ciliary ganglion. X40 (Scale bar 1 mm); B, Brain; E, Eyeball; G.C,

Ciliary ganglion; IOR.S, Interorbital septum; LN, Large neurons; M.RIF, Rectus inferior muscle;M.RL, Rectus lateralis muscle; M.RS, Rectus superior muscle; N.C, Ciliary nerve; OP.N, Opticnerve; R.IF.III, Ramus inferior of the nervus oculomotorius; R.NA.V, Ramus nasalis of the nervustrigeminus; R.SY, Sympathetic ramus connecting the ciliary ganglion with the internal carotid plexus,RCL, Radix ciliaris longa; SN, Small neurons; TCO, Trabecula communis.

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FIG. (7): A photomicrograph of a part of a transverse section of Sphenops sepsoides passing in the postorbitalregion demonstrating the two types of neurons of the ganglion and the radix ciliaris longa touchingthe dorsal side of the ciliary ganglion. X100 (Scale bar 2 mm); Fig. (8): A photomicrograph of apart of a transverse section of Varanus griseus griseus showing both the origin of the radix ciliarislonga from the ramus nasalis, the radix ciliaris brevis and their fusion. X40 (Scale bar 1 mm); Fig.

(9): A photomicrograph of a part of a transverse section of Varanus griseus griseus illustrating boththe position and structure of the ciliary ganglion as well as its sympathetic root. X100 (Scale bar 2mm); B, Brain; G.C, Ciliary ganglion; LN, Large neurons; M.BU, Bursalis muscle; M.REO,

Retractor oculi muscle; M.RL, Rectus lateralis muscle; M.RS, Rectus superior muscle; OP.N, Opticnerve; R.NA.V, Ramus nasalis of the nervus trigeminus; R.SP.III, Ramus superior of the nervusoculomotorius; R.SY, Sympathetic ramus connecting the ciliary ganglion with the internal carotidplexus, RCB, Radix ciliaris brevis; RCL, Radix ciliaris longa; SN, Small neurons.

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In Uromastyx aegyptius (Figs. 1 & 5, N.C), one large ciliary nerve arises from the dorsolateral side ofthe ganglion. It receives a fine branch from the carotid plexus, directly after its origin as previously mentioned(Fig. 1). After this anastomosis the ciliary nerve extends posteriorly and laterally to enter the eyeball througha foramen in the cartilaginous sclera of the eyeball (Fig. 5, N.C). Within the choroid of the eyeball, the ciliarynerve runs ventrally in the anterolateral direction till it reaches the iris and the ciliary body where it terminates.In Sphenops sepsoides (Fig. 3, N.C), one ciliary nerve arises from the anterolateral side of the ganglion. Itextends anterolaterally being tateral to the optic nerve penetrating the rectus lateralis muscle. This nerve entersthe eyeball through its own foramen in the cartilaginous sclera, posterior to the entrance of the optic nerve.Within the eyeball the ciliary nerve runs anterolaterally in the choroid of the eye to reach the iris and ciliarymuscles where it ends.

In Varanus griseus griseus, two ciliary nerves, one lateral and the other medial, originate from the anteriorend of the ganglion (Fig. 1, Nn.CL). These nerves run ventral to both the ramus nasalis of the nervustrigeminus and the rectus superior muscle and dorsal to the rectus lateralis muscle. Thereafter, the ciliary nervescontinue running ventrolateral to the optic nerve, dorsal to the rectus lateralis muscle and medial to the eyeball.More forwards, the two nerves fuse together and continue till they reach the medial side of the eyeball. Herethey give off a fine branch for the blood vessels. The fused ciliary nerves, then pass laterally ventral to theeyeball. After a considerable forward course, the ciliary nerves enter the eyeball through a foramen excavatedin the cartilaginous sclera. Within the eyeball, the ciliary nerves run anterolaterally in the choroid giving finebranches for its blood vessels, till they reach the iris and ciliary muscles where they end.

Discussion:

A distinct ciliary ganglion is found in the posterior orbital region of the three examined species. Inaddition, an accessory ciliary ganglion was described by Christensen (1935) in the cat and by Godinho (1972)in the pig. From the description cited in the reptilian literature, the present author is inclined to record theabsence of such an accessory ciliary ganglion in reptiles.

According to the observed structure of the ciliary ganglion, two types of neurons are recognized; largeneurons and small ones, that are equally distributed in the ganglion of both Uromastyx and Sphenops, whereasthe ciliary of Varanus composed of only one type of neurons. Similar result that found in both Uromastyx andSphenops was described by Mostafa and Hegazy (1990) in both Agama sinaita and Stenodactylus slevini.However, in Agama pallida (Soliman et al., 1984), Eumeces schneideri (Mostafa and Hegazy, 1990) in theamphisbaenian Diplometapon zaruanyi (Dakrory, 1994) and in the serpent Natrix tessellata (El-Ghareeb et al.,2004), the ciliary ganglion is divided into two distinct regions, large neurons at the periphery and small onesat the centre. On the other hand, the ciliary ganglion of the studied Varanus griseus is undivided and theneurons are homologous all over the ganglion. Similar pattern structure was found in Anolis carolinensis

(Willard, 1915), Chalcides ocellatus (Santamaria-Arnaiz, 1959; Soliman and Hegazy, 1969), Ptyodactylus

hasselquistii, Lacerta virides, Acanthodactylus boskiana, Agama mutabilis and Mabyua quinquetaeniata

(Soliman, 1968), Tarentola mauritanica (Soliman and Mostafa, 1984), Acanthodactylus opheodurus (Mostafa,1990), Mabuya quinquetaeniata (Abdel-Kader et al., 2007) and Tropiocolotes tripolitanus (El-Bakry et al.,2007). The same finding was also observed in the ophidian studied by Galvao (1917), Hegazy (1976) andMostafa (1990 & 1991). In this respect, Haller von Hallerstein (1934) described the ciliary ganglion of reptilesand birds confirming the existence of two parts; the first is composed of small neurons, while the second isformed of large ones. This finding was mentioned in birds by Oehme (1968), Soliman et al. (1976) and Abdel-Kader and Fathy (2000). In this context, Bullock et al. (1977), stated that, the ciliary ganglion of chick iscomposed of two cell populations, one controlling the smooth muscles in the choroid and the other for the irisand ciliary body. The same was mentioned by Radzimirska (2003)in the domestic turkey, Meleagris gallopavo

domesticus.

In mammals, the ciliary ganglion is undivided into two regions in any case. These pattern structure wasobserved in cat (Taylor and Weber, 1969), guinea pig (Watanabe, 1972), in man (Stefani, 1972) and in boththe hedgehog and bat (Hegazy and Mostafa, 1990).

In the three species studied, the ciliary ganglion is connected with the ramus inferior of the nervusoculomotorius by a well-distinct branch; the radix ciliaris brevis. This was mentioned by Willard (1915) inAnolis carlinensis and by Abdel-Kader et al. (2007) in Mabuya quinquetaeniata. However, in Lacerta viridis,the ciliary ganglion receives another branch from the nervus oculomotorius, a little anterior to the entrance ofthe radix ciliaris brevis (Soliman, 1968). On the other hand, the radix ciliaris brevis is very extremely shortso that the ganglion appears touching the nervus oculomotorius in Lacerta agilis and Lacerta muralis

(Lenhosséck, 1912) and Ptyodactylus hasselquistii (Soliman, 1968; Abdel-Kader, 1990). In contrast, the ciliary

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ganglion is firmly attached to the ramus inferior of the nervus oculomotorius, i.e., the radix ciliaris brevis islacking and the preganglionic parasympathetic fibres are transmitted directly to the ganglion through theintermingling surface in the geckos Tarentola mauritanica (Soliman and Mostafa, 1984), Stenodactylus slevini

(Mostafa and Hegazy, 1990) and Tropiocotes tripolitanus (El-Bakry et al., 2007) and in the amphisbaenianDiplometopon zarudnyi (Dakrory, 1994).

Among birds, the preganglionic parasympathetic fibres, carried by the nervus oculomotorius are transmittedto the ciliary ganglion either through an anastomosing branch; the radix ciliaris brevis or through the directattachment of the ganglion to the ramus inferior of the nervus oculomotorius. The radix ciliaris brevis ismentioned in Struthio (Webb, 1957), in Upopa epops and Passer domesticus (Soliman et al., 1976) and inMerops albicollis (Abdel-Kader and Fathy, 2000). On the other hand, the ciliary ganglion is firmly attachedto the ramus inferior of the nervus oculomotorius with the absence of the radix ciliaris brevis in the chick(Carpenter, 1906), in Streptopelia senegalensis (Soliman et al., 1976) and in Gallinula chloropus (Abdel-Kader,1999).

Concerning mammals, Schwalbe (1879) reported that not all the higher vertebrates possess a short root,as it is the case in many mammals (sheep, calf, dog, rabbit), and the ganglion is situated directly on the trunkof the nervus oculomotorius. The same condition was described by Christensen (1935) in the cat, Godinho(1972) in the ruminants, W atanabe (1972) in the guinea pig, Hegazy and Mostafa (1990) in both the hedgehogand bat, Sinnreich and Nathan (2003) in the man and by Nowak et al. (2004) in the Egyptian spiny mouse,Acomys cahirinus. In the baboon Papio cenocephalus, on the other hand, the ciliary ganglion receives twobranches from the ramus inferior (Gasser and Wise, 1972).

Among fishes, the preganglionic parasympathetic fibres of the nervus oculomotorius are transmitted to theciliary ganglion by branch, i.e., the radix ciliaris brevis in Lampancyctus teucopsorus (Ray, 1950),Pseudorhombus arsius (Marathe, 1955) Polypterus senegulus (Piotrowski and Northcutt, 1996) and in Tilapia

zillii (Dakrory, 2003; Ali, 2005). On the other hand, such fibres are transmitted directly to the ganglion throughthe intermingling surface between them, i.e., no radix ciliaris brevis in Polycentrus schomburgkii (Freihofer,1978), Trichiurus lepturus (Harrison, 1981), Ctenopharyndodon idellus (Dakrory, 2000) and in both Mugil

cephalus and Gambusia affinis affinis (Dakrory, 2003).In the present study, the radix ciliaris longa transmits the sensory fibres from the ramus nasalis (branch

of the ramus ophthalmicus) of the nervus trigeminus to the ciliary ganglion or ciliary nerves or both. In thisrespect, the case in Squamata is variable. The radix ciliaris longa passes directly to the ciliary ganglion indifferent snakes and lizards belonging to different families. This was found in the lizards Varanus bivitatus

(Watkinson, 1906), Anolis carolinensis (Willard, 1915); Lacerta viridis, Acanthodactylus boskiana, Agama

mutabilis and Mabuya quinquetaeniata (Soliman, 1968), Agama pallida (Soliman et al., 1984), Agama sinaita,

Stenodactylus slevini and Eumeces schneidri (Mostafa and Hegazy, 1990). The same condition was alsorecorded in the snakes Psammophis sibilians and Cerastes vipera (Hegazy, 1976), Coluber elegantissimus,

Psammophis schokari and Spalecosophis diadema (Mostafa, 1991), Natrix tessellate (El-Ghareeb et al., 2004)and in Telescopus dhara (Abdel-Kader, 2006). This is the case found in the Varanus griseus of the presentstudy.

In the gecko Gymnodactylus kotschyi (Evans and Minckler, 1938) and in the amphisbaenian Diplametepon

zarudnyi (Dakrory, 1994), however, the radix ciliaris longa joins both the ciliary ganglion and the ciliary nervedistal to the ganglion a case which is somewhat similar to that found in Uromastyx aegyptius studied, wherethe radix ciliaris longa gives off a fine branch which enters the ganglion and the main nerve passes across theganglion then turns to enter the ciliary nerve. Again, in the lizard Chalcides ocellaus (Soliman and Hegazy,1969) and the snake Eryx jaculus (Hegazy, 1976), the radix ciliaris longa passes across the dorsal side of theciliary ganglion, then turns to enter the ciliary nerve. However, Santamaria-Arnaiz (1959), dealing withChalcides ocellatus, stated that the radix ciliaris longa passes in contact with the ciliary ganglion but did notenter it; a case which is homologous to that found in Sphenops sepesoides studied. Also, Osawa (1898) foundthat the radix ciliaris longa did not enter the ganglion, but it joined the ciliary nerves in Hatteria punctata.In birds, no direct connection appears to exist between the ciliary ganglion and the ramus ophthalmicus. Suchconnection, however, is carried out between the latter ramus and the ciliary nerves distal to the ganglion. Thisappears to be common in birds; as described by Soliman et al. (1976). However, a direct connection betweenthe ramus ophthalmicus and the ciliary ganglion were described. It was mentioned in Struthio (Webb, 1957),Upopa epops (Soliman et al., 1976) and in Merops albicollis (Abdel-Kader and Fathy, 2000). On the otherhand, Bonsdroff (1952) described, for the crona, two rami from the nervus trigeminus, which have the typicalrelations of the long root (radix ciliaris longa) of the ganglion.

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In mammals, the sensory fibres are carried to the ciliary ganglion through the ramus ophthalmicus of thetrigeminal nerve. In the rhesus monkey (Christensen, 1933), and in both the hedgehog Hemiechinus auritus

and in the bat Rhosettus aegyptiacus (Hegazy and Mostafa, 1990), the ganglion receives sensory fibresconstituting its sensory root via a branch which connects it with the long ciliary nerve of the nasociliarybranch. The communicating branch, i.e., the sensory root, however, is directly given off from the nasociliarybranch in the rhesus monkey (Kuntz, 1933), in domestic ruminants (Godinho and Getty, 1971) and in thebaboon (Gasser and Wise, 1972). However, there is no direct connection between the ciliary ganglion and thenasociliary branch in the cat (Dupas, 1924; Christensen, 1935) and in the rhesus monky (Bast, 1933) and hencethe so-called sensory root of the ganglion is not found. In such species, the connection, however, is carriedout between the long ciliary nerve of the nasociliary branch and one of the short ciliary nerves arising fromthe ganglion. At the point of union between the long and the short ciliary nerves distal to the ganglion,accessory ciliary ganglia are usually found, as stated by Christensen (1935).

A connecting branch between the ciliary ganglion and the ramus maxillaries of the trigeminal nerve wasrecorded in several mammalian species. It was described in the ox by Mobillio (1912), in the baboon byGasser and Hendricks (1969) and in the goat, sheep and ox by Godinho and Getty (1971). Only, Mobillio(1912) considered such a branch as a sensory root entering the ciliary ganglion, in addition to another rootoriginating from the nasociliary branch.

Schawlbe (1879) did not find any connection between the ciliary ganglion (ganglion oculomotorius) andthe nervus trigeminus in several vertebrate species. Jegorow (1887), however, asserted that such a connectionis constant and necessary for the existence of the ganglion, throughout the vertebrate series. On the other hand,Holtzmann (1896) found that the ciliary ganglion in amphibians birds and mammals is more intimatelyconnected with the nervus oculomotorius than with the trigeminal one.

From the above discussion, it is thoroughly evident that both roots; radix ciliaris brevis and radix ciliarislonga, communicate, for the most part, with the ganglion separately. This was also the case found in the bonyfish Tilapia zilli (Dakrory, 2003). This is in contrast to the condition found in Varanus griseus of this study,where both the radix ciliaris brevis and radix ciliaris longa are fused just posterior to the ganglion. This is thecase found in the cyprinid fish Ctenopharyngodon idellus (Dakrory, 2000).

In the present study, there is a sympathetic connection (sympathetic root) between the carotid plexus andthe ciliary galnglion in Sphenops sepsoides and between both the ganglion and its nerves distal to the ganglionin Varanus griseus and between the plexus and the ciliary nerve distal to the ganglion in Uromastyx aegyptius.Among reptiles, this condition is variable. Similar condition to that found in Sphenops and Varanus, i.e., thesympathetic root connects the ganglion was recorded in the gecko Gymnodactylus kotschi (Evans and Minckler,1938), in Ptyodactylus hasselquistii and Mabuya quinquetaeniata (Soliman, 1968), Tarentola mauritanica

(Soliman and Mostafa, 1984) and Eumeces schneidri (Mostafa and Hegazy, 1990). In Ophidia it is found inthe serpent Eryx jaculus (Hegazy, 1976) and in the chelonian Trionyx japonicus (Ogushi, 1913). On the otherhand, a connection between the carotid plexus and the ciliary nerve found in Uromastyx aegyptius studied was,also described in the lizars Agama mutabilis (Soliman, 1968), Chalcides ocellaus (Soliman and Hegazy, 1969),Agama pallida (Soliman et al., 1984). The same results was mentioned by Hegazy (1976) in the snakesPsammophis sibilans and Cerastes vipera, in the snakes studied by Mostafa (1991) and in the snake Telescopus

dhara by Abdel-Kader (2006). It is also found in the amphisbaenian Diplometopon zarudmyi (Dakrory, 1994).However, the sympathetic connection with the ciliary ganglion or with the ciliary nerves was not found inLacerta viridis and Lacerta ocellatus (Weber, 1877), Lacerta muralis (Lenhossék, 1912), Acanthodactylus

boskiana and Lacerta viridis (Soliman, 1968), Acanthodactylus opheodurus (Mostafa, 1990) and in Agama

sinaita, Stenodactylus slevini (Mostafa and Hegazy, 1990), in Mabuya quinquetaenata (Abdel-Kader et al.,2007) and Tropiocolates tripolitanus (El-Bakry et al., 2007). It is also absent in the serpents Spalerosophis

diadema (Mostafa, 1990) and Natrix tessellate (El-Ghareeb et al., 2004). Such connection was found to be alsolacking in the chelonian Chelydra serpentina and Chelone imbricate (Soliman, 1964).

Among fishes, such connection, i.e., sympathetic root, appears to be found in most bony fishes (Dakrory,2003; Ali, 2005).

In birds, there is no connection between the ciliary ganglion or the ciliary nerves and the internal carotidplexus. This was confirmed by several authors as Webb (1957), Oehme (1968), Soliman et al. (1976) andAbdel-Kader and Fathy (2000). Thus, it can be stated that the absence of the sympathetic root is a commoncharacter among birds so far described.

In this respect, the condition observed in birds is quite different from that in mammals. Kurus (1956)stated that, the sympathetic connection (Sympathetic root) between the ciliry ganglion and the carotid plexusis, generally, present in mammals. The sympathetic root of the ganglion was described by Winkler (1932) in

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the rhesus monky, Taylor and Weber (1969) in the cat and by Hegazy and Mostafa (1990) in the hedgehogand the bat. However, Lenhossék (1912) mentioned that the sympathetic root may be absent in human being.This root was found to be absent in the ox (Schachtschabel, 1908) and in the goat, steep and ox (Godinho andGetty, 1971). On the other hand, Cunningham (1931) and Kuntz (1934) mentioned that the sympathetic rootof the ganglion in man may or may not be incorporated with the nasociliary branch.

In this study, there is only one ciliary nerve arising from the ciliary ganglion in both Uromastyx aegypius

and Sphenops sepsoides and two nerves in Varanus griseus griseus. Among reptiles, the number of ciliaryneves ranges from one to three. One ciliary nerve was found in Chalcides ocellatus (Santamaria-Arnaiz, 1959;Soliman and Hegazy, 1969), Ptydactylus hasselquistii, Acanthodactylus boskiana and Lacerto viridis (Soliman,1968), Acanthodactylus opheodurus (Mostafa, 1990) and Diplometopon zarudnyi (Dakrory, 1994). The samewas present in the snakes Psammophis sibilans and Eryx jaculus (Hegazy, 1976), in all serpents studied byMostafa (1991). There are two nerves in Varanus bivillatus (Watkinson, 1906), Anolis carolinensis (Willard,1915), Mabuya quinquetaeniata (Soliman, 1968; Abdel-Kader et al., 2007), Agama mutabilis (Soliman, 1968),Tarentola mauritanica (Soliman and Mostafa, 1984), Agama pellida (Soliman et al., 1984) in all the lizardsstudied by Mostafa and Hegazy (1990), and in Tropiacolotes tripolitanus (El-Bakry et al., 2007). There arealso two in the snakes Cerastes vipera (Hegazy, 1976), Natrix tessellate (El-Ghareeb et al., 2004) andTelscopus dhara (Abdel-Kader, 2006). Also two ciliary nerves were found in the chelonians Chelydra

serpentine and Chelone imbricate (Soliman, 1964). Three ciliary nerves were present in the geckoGymnodactylus kotschyi (Evans and Minckler, 1938).

Among birds, the number of the ciliary nerves varies from species to another. Schwalbe (1879) mentionedthat the number of the ciliary nerves may vary from one (e.g., hen, owl and goose) to seven (e.g. parrots). Oneciliary nerve was detected in the chick (Carpenter, 1906) and also in Merops albicollis (Abdel-Kader andFathy, 2000). However, Seto (1931) found five ciliary nerves in the chick. Two ciliary nerves were presentin Streptopelia senegalensis (Soliman et al., 1976) and in Meleagris gallopavo domesticus (Radzimirska, 2003)three ciliary nerves were found in Passer domesticus (Soliman et al., 1976) and in Gallinula chloropus (Abdel-Kader, 1999). Four ciliary nerves were found in the crow (Oehme, 1968) and in Upupa epops (Soliman et al.,1976) and five nerves were found in Struthio (Webb, 1957).

The number of the ciliary nerves arising from the ciliary ganglion is also variable among mammals. Twociliary nerves were found in the cat by Taylor and Weber (1969) and in the baboon by Gasser and Wise(1972). Three ciliary nerves were found in Hemiechinus auritus and four ones in Rhosettus aegypticus arisingfrom the ciliary ganglion as mentioned by Hegazy and Mostafa (1990). Four to five ciliary nerves were presentin the rhesus monkey (Bast, 1933; Kuntz, 1933). Twelve to fifteen ciliary nerves were found in man byCunningham (1931).

Concerning the development of the ciliary ganglion, Béraneck (1884), dealing with Lacerta agilis, relatedthe origin of the ganglion to the nervus oculomotorius. The description given by Hoffmann (1886) of thedevelopment of this ganglion is quite different from that of Béraneck (1884), although both authors dealt withthe same species. Hoffmann (1886) stated that the cells of the ciliary ganglion separate from the ophthalmicganglion (nervus trigeminus). Lenhossék (1912), on the other hand, dealing with Lacerta agilis and Lacerta

muralis, agreed with the finding of Beranéck (1884), but he mentioned that the ciliary ganglion, in the twospecies, is principally formed from cells arising in the central nervous system. Also Santamaria-Arnaiz (1959),dealing with Chalcides ocellatus, mentioned that there is no reason to think that the ciliary ramus of theophthalmic ganglion forms a part of the ganglion. However, Haller von Hallerstein (1934) reported that boththe nervi oculomotorius and trigeminus share in the formation of the ciliary ganglion in reptiles and birds. Thesame finding was also mentioned by Evans and Minckler (1938) in the gecko Gymnodactylus kotschyi. Theauthor supports Santamaria-Arnaiz (1959). This view of the author is evident from his observation on both theUromastyx aegyptius and Sphenops sepsoids, where the sensory fibres of the radix ciliary longa pass directlyto the ciliary nerves without any relations to the ganglionic cells of the ganglion.

Regarding the matter in birds, Rex (1900) found that the ciliary ganglion in the duck makes its appearanceas a distinct thickening in the course of the nervus oculomotorius. But he did not follow the origin of theganglion cells. Carpenter (1906) offered a complete account of the development of the ciliary ganglion in birds.He stated that the ciliary ganglion of the chick appears as a collection of actively dividing “accompanying”cells near to the distal extremity of the nervus oculomotorius. Carpenter regarded these “accompanying” cellsas medullary cells which have migrated into the nerve from the neural tube. He further mentioned that a smallnumber of the ophthalmic ganglion cells migrate to the ciliary ganglion, passing along a communicating ramusfrom the ophthalmic branch of the nervus trigeminus. Recently, Lee et al. (2003) suggested that the ciliaryganglion of the chick has a dual, neural crest and placoidal origin.

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Among mammals, the illustration given by Reuter (1897) and Kuntz (1913) of the development of theciliary ganglion in the pig embryos is quite different. Reuter (1897) related the ganglion to the oculomotornerve. Kuntz (1913), however, believed that it arose from cells migrating from the neural tube along theoculomotor nerve and from others migrating from the semilunar ganglion along the ophthalmic branch of thetrigeminal nerve. From the reviews of Deery (1931) and Goodrich (1986), it seems that both the oculomotornerve and the ophthalmic branch contribute to the formation of the ganglion. On the other hand, Stewart(1920), stated that the rat neuroblasts, giving rise to the ciliary ganglion, reach their place through theophthalmic branch. In man, there are generally two different points of view on this subject. In this regard, His(1880 & 1888) and Streeter (1912), assigned the ciliary ganglion to cells arising from the semilunar ganglion,which is a direct descendant of the neural crest. However, Kuntz (1933) concluded that the ganglion appearsto be derived from both the oculomotor nerve and the trigeminal ganglion. Hara et al. (1982) concluded thatthe ciliary ganglion in dogs is composed of the oculomotor trigeminal and sympathetic nerves.

From the above mentioned discussion, it is obvious that, there are differences in the ciliary ganglion ofthe studied species, concerning the structural relations and even the number of ciliary neves. Again, it alsoshows similarities in number of ciliary roots and unity of the cellular (neurons) structure; hence all formed ofbipolar neurons. Though, there is only one ciliary nerve in Uromastyx and Sphenops yet this nerve is largeand stout in the former species. Thus we can conclude that, although ther is a specific variations regarding theciliary ganglion yet it is at an intermediate rank between Amphibia and fishes from one side and the birds andmammals from the other side.

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