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ANATOMICAL STUDIES ON THE NERVUS VAGUS OF ALTICUS KIRKIIMAGNUSI (KLAUSEWITZ, 1964)

Ahmed Imam Dakrory 1 and Rania Sayed Ali 2 . 1. Zoology Department, Faculty of Science, Cairo University. 2. Zoology Department, Faculty of Science, Helwan University. . Manuscript Info Abstract . . Manuscript History Received: 03 October 2019 Final Accepted: 05 November 2019 Published: December 2019

In Alticus kirkii studied the nervus vagus arises from the brain by one root and leaves the cranial cavity through the jugular foramen. The intracranial dorsal cutaneous vagal ramus has its own ganglion. It carries all the somatic sensory fibres of the vagus nerve. The vagus nerve has a single lateral jugular (epibranchial) ganglion. The first vagal branchial trunk lacks the ramus pharyngeus and the third one lacks the ramus pretramaticus. The nervus vagus anastomoses twice with the cranial sympathetic nerve. The nervus vagus carries general somatic sensory fibres to the skin, general viscerosensory fibres to the pharyngeal epithelium, special viscerosensory fibres to the gill rackers and the taste buds and visceromotor fibres to the levators and the adductor arcuales branchiales and the obliquus ventrales muscles of the second, third and fourth holobranchs, as well as to the transverses dorsalis and ventralis muscles. It also carries vegetative fibres (parasympathetic) for the blood vessels, thyroid glands and the muscles of the gill filaments.
Other studies were performed on one cranial nerve or a group of cranial nerves in some other bony fishes. Kassem et al. (1988) and Bauchot et al. (1989) gave an account on the eye muscles nerves in Chaetodon trifasciatus and Tridentiger trigonocephalus, respectively. In addition, De Graaf (1990) studied the innervation of gills in Cyprinus carpio by dissection. The most recent studies performed on bony fishes are presented by some other authors such as Dakrory (2003) who studied the ciliary ganglion and its anatomical relations in some bony fishes. In addition, Ali and Dakrory (2008) studied the eye muscle nerves of this species; Dakrory et al. (2018a&b) studied the eye muscle nerves and the nevus glossopharyngeus of Garra tibanica.
It is evident from the aforementioned historical review that there are numerous works on the cranial nerves of fishes, but nearly no studies had been made concerning the cranial nerves of Blinniidae. Although the previously mentioned studies of different authors may threw light on the subject of the cranial nerves of fishes, yet it cannot be stated that the cranial nerves of a Blinniidae is similar to other fishes; and what are the differences if present? Thus it was suggested that a detailed microscopic study on the vagal nerve in Alticus kirkii magnusi will be very useful. The main and fine branches of this cranial nerve, its distribution, its relation with other nerves and with the other structures of the head, its analysis and the organs they innervate are studied thoroughly, hoping that it may add some knowledge on this important subject and also to the behaviour and phylogeny of this group of fishes.

Material And Methods:-
The specimens of the rock skipper fish, Alticus kirkiimagnosi (family: Blenniidae ; order: Blinniiformes ) were captured from the Red Sea at Ras Mohamed, Sharm El-Sheihk, South of Sinai during March 2008. This is a marine primarily tropical fish (Aizawa and Doiuchi, 2013;Mehraban and Esmaeili, 2018); the body is naked without scales, the head is blunt and the pelvic fins lie anterior to the pectoral ones; the palate is toothless and jaws have comb-like fixed teeth (Randall, 1995). The adult fish has no swim bladder but has a basisphenoid bone (Randall, 1995). This species is oviparous and the ggs are demersal and adhesive (Breder and Rosen, 1966), and are attached to the substrate via a filamentous, adhesive pad or pedestal and the Larvae are planktonic, often found in shallow, coastal waters (Watson, 2009).
Adults are found in the intertidal zone of exposed rocky shores, often out of the water (Randall, 1995). They actively shuttle back and forth between rock pools and air (skipper) (Martin and Bridges, 1999).Breathe air when out of water (Martin and Bridges, 1999). It is oviparous (Breder and Rosen, 1966), the eggs are demersal and adhesive (Breder and Rosen, 1966), and are attached to the substrate via a filamentous, adhesive pad or pedestal (Watson, 2009). Larvae are planktonic, often found in shallow, coastal waters (Watson, 2009).
Heads of these specimens were cut and fixed in aqueous Bouin"s solution for 24 hours. They were then washed several days with 70% ethyl alcohol. The specimens were decalcified using EDTA solution for three to four weeks, changing the solution every four days. The heads were then dehydrated, cleared, mounted and embedded in paraffin wax and serially sectioned transversally at 10 micrometers thick. After sectioning, the serial sections were mounted and stained with triple Malory stain (Pantin, 1946).
The serial sections were drawn with the help of a projector. From these sections an accurate graphic reconstruction for the vagus nerve was made in a lateral view. Parts of some selected sections were photomicrographed to show the position of the vagus nerve and its relation to the other cranial structures.

Results:-
In Alticus kirkii studied, the nervus vagus originates from the mid-lateral side of the medulla oblongata by a single stout root. This root (Figs. 1 & 2, RO. X) arises from the medulla oblongata posterior and ventral to the origin of the posterior lateral line nerve. It runs posterior in the ventrolateral direction, passing lateral to the medulla oblongata (MO) and medial to the ganglion of the intracranial dorsal vagal ramus. Here, it gives off a lateral nerve, which is the intracranial dorsal vagal ramus (Figs. 1 & 2, RO. ICDV). This ramus will be described shortly latter on. Posterior to the origin of this branch, the nervus vagus continues passing lateral to the medulla oblongata and medial and then ventromedial to both the ganglion of theintracranial dorsal vagal ramus and the posterior lateral line nerve. Thereafter, it shifts posteroventrally to leaves the cranial cavity together with and medial to the posterior lateral line nerve by penetrating the meninx primitive through the jugular foramen. The later foramen is in the form of incisura and lays medial to the opisthotic bone (OP. OT) and lateral to the exoccipital one (EO) (Fig. 3  It ends posteriorly at the anterior orifice of the jugular foramen. From this ganglion arise two nerves; one from its anterodorsal extremity and the other from its ventrolateral side. The anterodorsal nerve (Fig. 1, R. ICDV) extends forwards in a dorsal direction, within the cranial cavity, being medial to the membranous labyrinth and lateral to the medulla oblongata. Here, it gives off two fine nerves that ramify and end in the meninx primitiva that protects the brain in this region (Fig. 1, Nn. MP.). Thereafter, the anterodorsal nerve continues anterodorsal to leave the cranial cavity through the parietal bone and ramifies and ends as fine nerves in the skin of postotic region.  Shortly anterior the dorsal bundle give raise a ventral branch, which fuses with the second branchial vagal trunk anterior to its origin from the jugular ganglion. The remainder of this dorsal bundle forms the first branchial vagal trunk. The visceral trunk is out of our scope in this study. From the anteroventral end of the jugular ganglion arise the second (X 2 ) and third (X 3 ) branchial vagal trunks (Fig. 1).

First Branchial Vagal Trunk "X 1 ":-
In the blenniid species studied, the first branchial vagal trunk (Figs. 1, 5& 6, X 1 ) extends forwards for a long course passing dorsal to the jugular ganglion, lateral to the cranial sympathetic nerve and dorsolateral to the internal jugular vein. Here, it anastomoses with the cranial sympathetic nerve by a fine anastomosing branch ( Fig. 1, R. CM. N. X + N. CSY). Thereafter, this trunk continues anteriorly passing dorsal to the second branchial vagal trunk, lateral to the internal jugular vein and medial to the third levator arcus branchialis muscle. More forwards, it becomes ventrolateral, ventral and then ventromedial to the internal jugular vein, dorsomedial and medial to the later muscle, dorsolateral to the third efferent branchial vessel and lateral to the second branchial vagal trunk. Here, it gives off a motor nerve to the second levator arcus branchialis muscle (Fig. 1, N. LAB. 2). Shortly anterior, it enters the second holobranch, just ventromedial to the fusion of the second efferent branchial vessel with the circus cephalicus. Here, it divides into a small, ventromedial ramus pretrematicus X 1 (Figs. 1&7, R. PR. X 1 ) and a large dorsolateral ramus posttrematicus X 1 (Figs. 1&7, R. PT. X 1 ). It also gives a motor nerve to the second adductor arcus branchialis muscle (Fig. 1, N. ADB. 2).

Ramus Pretrematicus Of X 1 :-
After its separation from the ramus posttrematicus X 1 , this ramus (Figs. 1&7, R. PR. X 1 ) extends posteroventraly running ventromedial to the second epibranchial bone and dorsolateral to the second adductor arcus branchialis muscle. Here, it gives off a fine nerve to the later muscle. Thereafter, the main ramus penetrates the muscle to become lateral to the pharyngeal cavity and ramifies to innervate the pharyngeal taste buds. One or more of these ramification pass to the gill rackers dorsal to the second ceratobranchial bones of the holobranch.
Ramus Posttrematicus X 1 :-After its separation from the pretrematic ramus X 1 , the posttrematic ramus (Figs. 1&7, R. PT. X 1 ) extends posteroventrally dorsolateral to the second epibranchial bone and medial to the efferent branchial vessel. Here, it gives off fine branches to the gill filaments. Thereafter, it shifts anteriorly to become ventrolateral to the second ceratobranchial cartilage giving rise   To few nerves to the gill filament. More forwards, it becomes dorsal to the efferent blood vessel and ventral to the ceratobranchial bone. Thereafter, the posttrematic ramus (Fig. 1, R. PT. X 1 ) gives off three fine branches to the gill filaments and two nerves to the gill rackers. More forwards, the posttrematic ramus gives off a nerve to the connective tissue and gill filament. Shortly forwards, the posttrematic ramus enters the isthmus. In the isthmus, the posttrematic ramus runs anteromedially passing ventromedial to the ceratobranchial bone. Here, it gives rise to a branch to the roof of the isthmus. This branch ramifies to innervate the epithelium covering the isthmus and the taste buds in this region (Fig. 1, Nn.TB). Thereafter, the posttrematic ramus gives off a motor nerve to the second obliquus ventralis muscle (Fig. 1, N. OV.2) and a sensory one to the taste buds and epithelium of the isthmus. Finally, it runs anteromedially to end as fine nerves between the follicles of the thyroid gland (Fig. 1, N. THG).  (Fig. 1). After that, it runs anteromedially, passing ventral to the internal jugular vein, medial to the first vagal branchial trunk and dorsal to the second pharyngeobranchial cartilage (Fig. 6, X 2 ). Here, it gives off two successive branches; one to the transverses dorsalis muscle (Fig. 1& 8, N. TD) and the other to the third levator arcus branchialis muscle (Fig. 1, N. LAB. 3). Again, after a short cephaled distance, the main trunk gives off the ramus pharyngeus (Fig. 1& 8, R. PH. X 2 ). The Ramus Pharyngeus X 2 :-After its separation from the second vagal branchial trunk, the ramus pharyngeus (Figs. 1&8, R. PH. X 2 ) runs medially to become dorsal to the pharynx. Here, it gives rise to a ventral branch which, immediately ramifies in the epithelial lining of the lateral part of the pharyngeal roof (Fig. 1, N. EP). The main ramus continues anteromedially for a distance, then, it ramifies in the dorsal side of the pharynx to innervate its epithelium and the taste buds in this region (Fig. 1, N. EP).

Ramus Pretrematicus X 2 :-
The pretrematic ramus (Figs.1, 6&8, R. PR. X 2 ) runs posteroventrally passing lateral to the pharyngobranchial bone and medial to both the third levator arcus branchialis muscle and then to the third epibranchial bone. Thereafter, it turns forwards running medial to the later bone and dorsomedial to the ceratobranchial bone just anterior to their articulation. Here, it gives off three fine nerves to the gill rackers (Fig. 1, Nn. GR). More forwards, it gives off a dorsal branch to the gill rackers. Thereafter, this ramus shifts ventromedially giving rise to two successive nerves to the gill rakers (Fig. 1, Nn. GR). More and more forwards, the pretrematic ramus X 2 continues in the same position and finally it ramifies into small nerves that end in the gill rackers and the epithelium of the third holobranch (Fig. 1, Nn. GR).

Ramus Posttrematicus X 2 :-
The ramus posttrematicus X 2 (Figs. 1&8, R. PT. X 2 ) runs forwards extending ventromedial to the internal jugular vein, medial to the first vagal branchial trunk and dorsal to the epibranchial bone. Thereafter, it shifts ventrolaterally passing dorsolateral to the third efferent branchial vessel and ventromedial to the third levator arcus branchialis muscle to enter the third holobranch. Here, it gives off a motor branch for the third adductor branchialis muscle (Fig. 1, N. ADB. 3) and a lateral branch for the dorsal gill filaments. Thereafter, it continues backwards for a distance and then turns its course anteroventrally, extending ventrolateral, ventral and ventromedial to both the third efferent branchial vessel and the third ceratobranchial bone. Here, it gives off branches to the gill filaments (Fig. 1, Nn. GF). Thereafter, the ramus posttrematicus X 2 gives off two lateral nerves to the gill filament (Fig. 1, Nn. GF). More forwards, the ramus posttrematicus X 2 (Fig. 1, R. PT. X 2 ) gives off another three nerves to the gill filaments. Shortly cephaled, it enters the isthmus where, the third holobranch fuses with it. Here, the ramus posttrematicus X 2 gives off two motor nerves; one enters and ends in the third obliquus ventralis muscle (Fig. 1, N.OV.3) and the second passes to the transversus ventralis muscle Fig. 1, N.TVE) where it achieves its final fate. Finally, this ramus ends in the epithelium covering the isthmus.

Third Vagal Branchial Trunk X 3 :-
The third vagal branchial trunk arises from the anteroventral end of the jugular ganglion, just posterior to the origin of the second trunk, as previously mentioned (Fig. 1, X 3 ). It runs forwards and fuses with the lateral nerve of the ventral bundle of the vagal medial divison.
This trunk runs forwards in ventromedial direction passing medial to the fourth levator arcualis branchialis muscle and dorsal to the fourth holobranch, ventrolateral to the internal jugular vein and ventromedial to the jugular ganglion (Fig. 5, X 3 ). Here, it gives off a lateral motor nerve which runs forwards to end in the fourth levator arcus branchialis muscle (Fig. 1, N. LAB. 4). Shortly anterior, the third vagal branchial trunk divides into medial division representing the rami pharyngeus and pretrematicus and a lateral ramus posttrematicus (Fig. 1, R. PH.X 3 & R. PT. X 3 ). A separate ramus pretremticus appears to be lacking.

Ramus Pharyngeus X 3 :-
This ramus (Fig. 1, R. PH. X 3 ) runs forwards in the medial direction passing ventral to the fourth efferent branchial vessel and dorsal to the fourth levator arcus branchialis muscle. After a course, it reaches the dorsolateral corner of the pharynx. Here, it gives off two branches to the epithelial mucosa of roof of the pharynx and the pharyngeal teeth.
After that, the ramus pharyngeus,runs anteroventrally for a short distance extending lateral to the pharynx and medial to fourth adductor arcus branchialis muscle. Entering the holobranch, it runs forwards medial to the ceratobranchial cartilage and lateral to the pharyngeal cavity. Here, it ramifies and ends in the epithelium, the gill rackers and teeth of the holobranch (Fig. 1).

Ramus Posttrematicus X 3 :-
After its separation from the medial division, the ramus posttrematicus (Figs. 1& 5, R. PT. X 3 ), runs anteriorly for short course gives off a motor nerve to the fourth adductor branchialis muscle (Fig. 1, N. ADB. 4). Thereafter, it enters the fourth holobranch, just dorsolateral to the fourth efferent branchial vessel and immediately posterior to the articulation of the fourth epi-and ceratobranchial bones. Here, it gives off fine branches to the dorsal gill filaments. Thereafter, it runs forwards ventrolateral to the fourth ceratobranchial bone and lateral to the efferent branchial vessel, giving rise to several branches to the gill filaments (Fig. 1, Nn. GF). Shortly forwards, it becomes ventral to the ceratobranchial cartilage and lateral to the efferent blood vessel. Here, it gives off two branches to the epithelial lining of pharynx. More forwards, this ramus enters isthmus and gives raise a dorsal nerve. This nerve extends dorsolateral to the fourth obliquus ventralis muscle, and ramifies into several fine branches that end in the epithelium and the ventral oral taste buds of the isthmus. Finally, the main ramus extends medially to enter and end in the fourth obliquus ventralis muscle (Fig. 1, N. OV. 4).
Among cartilaginous fishes, Norris and Hughes (1920) in Squalus acanthias, stated that there are thirty or more rootlets for the nervus vagus. Five rootlets for this nerve were found in the cartilaginous fishes studied by Gohar and Mazhar (1964). In the skate, Raja eglanteria Boord, 1992& 1993), the vagus nerve arises as a series of superficial rootlets, the number and spacing of which vary considerably, not only among different specimens but also on the two sides of the same specimen. In this respect, Edgeworth (1935) stated that the rootlets of the nervus vagus in cartilaginous fishes vary from two to thirty; the most anterior of which are sensory forming the posterior lateral line nerve, while the most posterior ones are exclusively motor. In Rhinobatus halavi, the nervus vagus, including the posterior lateral line nerve arises by many rootlets (18-24 rootlets) as mentioned by Dakrory (2000). In jawless fish Petromyzon Marinus, the nerve in question has a single root (Barreiro-Iglesias, A., etal, 2008).
Among Amphibia, the nervus vagus arises by two roots as mentioned by Gaupp (1911), Soliman and Mostafa (1984) and Shaheen (1987). However, Wake et al. (1983) stated that the nervus vagus arises by three major and minor rootlets in the amphibians he studied.
In the bony fish studied, the distal or lateral vagal ganglion (jugular ganglion) is undivided. In many bony fishes, this ganglion is divided into a number of epibranchial ganglia. This ganglion is divided into three epibranchial ganglia; one for each the first and the second branchial vagal trunks and the third for the last branchial and the truncus visceralis in Lampanyctus leucopsarus (Ray, 1950), Polycentrus schomburgkii (Freihofer, 1978) and in Tilapia zilli (Ali, 2005;Dakrory and Ali, 2006). On the other hand, Herrick (1901) found that the lateral vagal (epibranchial) ganglion is divided into two parts only; one epibranchial and one intestinal (visceralis) in Argyropelecus hemigymnus. Also, Allis (1903) stated that, only the first epibranchial ganglion is separated, while the others are more or less fused in Scomber scomber. In Cyclothone acclinidens (Gierse, 1904), separate ganglia were described for the first two branchial trunks but the third branchial trunk was found to lack a ganglion entirely. Also, Polypterus senegalus has only two lateral epibranchial vagal ganglia (Piotrowski and Northcutt, 1996). However, the lateral vagal ganglion is divided into four epibranchial ganglia, one for each branchial vagal trunk, and one visceral ganglion for the truncus visceralis in Amia calva by Allis (1897), in Menidia by Herrick (1899), in Parasilurus asotus by Atoda (1936), in Pseudorhombus arsius by Marathe (1955), in Trichiurus lepturus by Harrison (1981), in Cyprinus carpio by de Graaf (1990) and in Ctenopharyngodon idellus by Dakrory (2000).
In the current study, the first and a large parts of each the second and third branchial vagal trunks as well as the visceral trunk arise from the nervus vagus as a large common division, while other parts of the second and third branchial vagal trunks originate as the second division from the main vagal nerve. However, in Ctenopharyngodon idellus by Dakrory (2000), the first and second branchial trunks arise as a common nerve, while the third and fourth ones, together with the visceral trunk originate at the same point from the main vagal nerve.
In this respect, Atoda (1936), Dalela and Jain (1968) and de Graaf (1990) found that all the branchial vagal trunks arise at the same point in Parasilurus asotus, Clarias batrachus and Cyprinus carpio, respectively. In Mastacembelus armatus (Bhargava, 1959), there are two trunks arising from the vagal ganglion; one innervating the viscera and the other splits into the four branchial nerves. However, two dorsal and three ventral trunks arise from the vagal mass in Amphipnous cuchia (Saxena, 1967).
The three branchial vagal rami and the ramus intestinalis in Chimaera manstrosa have a separate origin from the brain and each possesses its own independent ganglion (Cole, 1896). Ray (1950) mentioned that the widespread appearance of separate epibranchial ganglia, particularly, among those fishes which are generally regarded as primitive forms, suggests that this condition represents the basic pattern, from which specialization has progressed along the lines of fusion or reduction in the total number of ganglia. As already indicated, the same may occur in the vagal roots. Thus the nervus vagus may be considered as representing not one, but three or possibly four, or even more fused nerves. Comparing the case in different fishes, the same author added that the roots might have been 335 fused first and that subsequent distal progression of fusion happened in the ganglia of the more specialized forms. According to Ray's sight the condition in this study considered to be a high advances due to the presence of one root and one ganglion.
Typically, each of the branchial vagal trunks of fishes is divided into rami pharyngeus, pretrematicus and posttrematicus. In the present study, the first branchial vagal trunk lacks ramus pharyngeus and the third trunk lacks the ramus pretrematicus. On the other hand, in the bony fish, Cyclothone acclinidens (Gierse, 1904), the ramus pharyngeus was found to be completely lacking. Ray (1950) stated that there is only a ramus pharyngeus and a ramus pretrematicus for the third branchial vagal trunk, while the ramus posttrematicus is reduced in Lampanyctus leucopsarus. Among cartilaginous fishes, the last or fourth ramus posttrematic was found to want in the batoid Raja eglanteria (Sperry and Boord, 1993).
In the present study, the first vagal trunk receives a sympathetic branches arising from the cranial sympathetic nerve. In this respect, the posttrematic ramus of the first branchial vagal trunk receives a sympathetic branch arising from the sympathetic vagal ganglion in Ctenopharyngodon idellus (Dakrory, 2000). The first and third epibranchial ganglia receive sympathetic branches arising from the sympathetic vagal ganglion inLiza ramada (Ali, 2012), Liza aurat (Al-Harthi, 2016) and in Oreochromis niloticus (Almalki, 2017). A connection between the nervus vagus and the sympathetic ganglion is present in Pseudorhombus arsius (Marathe, 1955) and Takifugu niphobles (Funakoshi et al., 1996(Funakoshi et al., , 1997. Ray (1950) stated that the sympathetic trunk has a connection with one of the vagal nerves arising in the jugular foramen by a minute branch in Lampanyctus leucopsarus.
In this study, the nervus vagus carries special visceral sensory fibres for the taste buds and general ones for the lining epithelium of the pharynx and visceral arches. They carry, also, branchiomeric motor (visceromotor) fibres for the branchial muscles. In addition to these fibres, the nervus vagus carries also, general somatic sensory fibres for the skin covering the roof of the postotic region of the skull, and vegetative fibres (parasympathetic) for the blood vessels, thyroid gland and the muscles of the gill filaments.
In this study, the somatic sensory fibres of the vagus nerve are included in a separate nerve; the intracranial dorsal cutaneous vagal ramus which passes to the skin covering the postotic region of the skull. This was discussed previously.
The visceral sensory fibres are found in all the rami of the nervus vagus studied except the intracranial dorsal cutaneous vagal ramus . The pharyngeal and pretrematic rami carry only visceral sensory, whereas, the posttrematic rami carry, in addition to the visceromotor fibres, visceral sensory ones. The visceral sensory fibres of the vaugs, glossopharyngeal and facial nerves innervate the oropharyngeal epithelium and their taste buds. This means that the gustatory fibres, in fishes, are carried by three cranial nerves; the facial, glossopharyngeal and vagal nerves. This was confirmed by Herrick (1944) and Kinnamon (1987) in fishes and tetrapods. About the origin or source of the gustatory components of these three nerves, Landacre (1910) and Northcutt (1997) mentioned that these components have been thought to arise from a separate epibranchial neurogenic placode.
In lampreys, the gustatory fibres are carried by the nervi glossopharyngeus and vagus only. Such fibres are completely lacking from the facial nerve (Johnston, 1905 and1908b;Finger and Morita, 1985;Finger, 1987;Braun, 1998).