Vasculature and Innervation of the Inner ear of Camel (Camelus Dromedarius)

*Safwat Ali¹, A. Esmat A¹, Shihata M. Soliman² and Atef M. Erasha ³

¹Department of Anatomy and Embryology, Faculty of Veterinary Medicine, Minia University.

² Department of cytology and histology, Faculty of Veterinary medicine, Minia University.

³ Department of Anatomy and Embryology, Faculty of Veterinary Medicine, University of Sadat City.

Corresponding author: asafawato@yahoo.com

Abstract: The arterial blood supply and innervation of the inner ear especially the cochlea of the camel were examined both macroscopically and microscopically using different techniques. The aim of this study to observe any variation between the arterial blood supply and innervation of the camel and the other mammals. The results of this study show variation between the camel and the other domestic animals in the course of the main arterial blood vessel, which supply the inner ear; caudal cerebellar artery. Also the angle of vestibulocochlear nerve and facial nerve at internal acoustic meatus is recorded. The cochlear artery and nerve show type of modification in the modulus of the cochlea, which influences in the morphology of the cochlea and consequently in physiological function.

Key words: camel, inner ear, vestibulocochlear nerve, caudal cerebral artery, modulus, internal acoustic meatus, spiral ganglia.

Introduction

The camel studies are still quantitatively marginal compared to other ruminant species. This marginality is linked first to the low camel stock compared to cattle for example, and to the limited geographical distribution of this species. Secondly, for funding agencies and main decision makers, camel is rarely considered as a productive animal, but rather as an animal from the past (Faye, 2014 ).

Despite of great contribution of the camel for the livelihood in different parts of the world in which other animals face difficulties, camels are the most neglected domestic animals by the scientific community. Therefore the value camels should have to get emphasis and awareness should have to be created to the community about health care and management of camels (Gebreyohanes and Assen, 2017).

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The morphological description of the arterial blood supply and innervation of the inner ear of the camel is necessary. No doubt that the inner ear of the camel plays an important role in these harsh conditions of the desert and maintain of both normal hearing and equilibrium of the camel. A detailed histological and SEM description of the healthy camel cochlea is required to observe any variation in nerve and blood supply may direct or indirect influence the hearing ability of the camel.

The arterial blood supply and innervation are well described in most mammals like cats, sheep, equine but the inner ear and especially the blood supply of the inner ear of the camel have been poorly investigated and illustrated in literature so far.

The inner ear can be divided into the osseous and membranous labyrinth (Ekdale, 2009).The membranous labyrinth is housed in a similar but slightly larger osseous labyrinth, a complex excavation in the temporal bone (Seeley, Stephens, & Tate, 2002).

The central chamber of the osseous labyrinth, the vestibule, houses the utriculus, the sacculus and the semicircular ducts (Reece and Rowe, 2017). The cochlear duct passes up the spiral canal of the cochlea, which is an excavation very similar to the inside of a snail’s shell (Frandson et al., 2009).

The cochlear nerve, vestibular nerve, and facial nerve run together with the labyrinthine artery within the internal auditory canal at the fundus of the canal (Kӧnig and Liebich, 2013), the facial nerve and superior division of vestibular nerve are located above transverse crest. The cochlear nerve and the inferior division of the vestibular nerve are located under the crest (Nomura, 2013).

The facial nerve passes to the internal acoustic meatus, accompanied by the vestibulocochlear nerve. It enters the facial canal, a passage within the petrous temporal bone, with a sharp caudal convexity, the genu of the facial nerve, where the nerve is enlarged to form the geniculate ganglion at the summit of the bend (Dyce et al., 2010).

The osseous cochlea surrounding the cochlear canal in a spiral around a central pillar of bone, the modiolus, contains in turn the spiral lamina, a thin shelf of bone that travels up the modiolus, which contains the spiral ganglia (Slepecky, 1996).

The hair cells of the organ of corti; organ of hearing are associated with terminals of sensory neurons, the cell bodies of which are located within the spiral ganglion. Afferent fibers of the sensory neurons join to form the cochlear nerve. This nerve joins the vestibular nerve to become the vestibulocochlear nerve (cranial nerve VIII), which carries action potentials to the brain (Seeley, Stephens, & Tate, 2002).

The width of the cochlea; the width of the basal turn regarded as one of the most important adaptations to the perception of very high frequencies. The high frequency limit and the best hearing frequency were significantly positively correlated with cochlear width (Wannaprasert, 2013). Also the increase number of nerve cells in the spiral ganglion results in better frequency

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discrimination across the higher range of frequencies used for echolocation (Fleischer, 1976; Solntseva, 2010).

In human the artery of the inner ear arises from the vertebral artery system. The labyrinthine artery usually arises from the anterior inferior cerebellar artery, though occasionally it comes directly from the basilar artery (Nomura, 2013). In horse the labyrinthine artery is a very small vessel which usually arises from the caudal cerebellar artery and enters the internal acoustic meatus (Getty and Sisson, 1975). This study aimed to determine any different between the atrial blood supply and innervation of the inner ear of the camel and the other mammals. Also to clarify the full details can be employed as references for further research on the camel’s inner ear organ and for comparative with other mammals. Finally this study explains how the arterial blood supply and innervation of the inner ear of the camel modified adapting to structure nature of the camel inner ear.

Materials and methods

For the present study of the inner ear of twelve healthy adult heads of the camel of varying ages (2.5 to 5.5 years old) were collected from the local slaughterhouse in Minia Governorate, Egypt were used to identify the morphology and measurements of the inner ear. The specimens were dissected at the department of Anatomy and Embryology (Faculty of Veterinary Medicine, Minia University).

Three heads used for Scanning Electron Microscopy, a slice of hemisectioned cochlea was taken from the inner ear of the camel and, fixed in mixture of paraformaldehyde solution (2.5%) and glutaraldehyde solution (2.5%) in phosphate buffer (pH 7.3) for 24 hours. The sample was washed in 0.1M phosphate buffer, dehydratedin graded ethanol, critical point-dried in liquid carbon dioxide, and then coated with gold palladius in a sputtering device. The sample was then examined and photographed using JSM-5400LV scanning electron microscope operated at 20 KV in the EM center of Assiut University.

Three heads used for Light Microscopy the temporal bones were fixed in mixture of paraformaldehyde solution (2.5%) and glutaraldehyde solution (2.5%) in phosphate buffer (pH 7.3) for 24 hours. Then completely decalcified in 5% EDTA (3week), dehydrated in a graded alcohol series, and embedded in paraffin. Serial 10 mm-thick sections were cut parallel to the modiolus. All sections were stained with hematoxylin-eosin.

Three heads used for computed aid tomography scans. The CAT examinations were conducted within 2 hr. after the heads were collected. Serial CAT scans were done using a Hitachi CAT (CT-W450-10A, Hitachi, Japan). The scanned images, 1.5 cm thick, of the head were taken from the external occipital protuberance caudally to the level of the canine teeth rostrally. Bone window images were used to evaluate the head parts related to the bone landmarks levels, the tomographic scan angle was 90 degree on the head midline nasal and frontal surfaces (scanning conditions: 130 kV, 100 MA, the windows width and level (W/L): 1126/213).

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Three heads used for arterial blood supply of the inner ear subjected to the latex gum milk technique. The root of the injection was through the basilar artery specimens were. The specimens were injected with formalin mixture solution of 10% formalin 2% phenol, and 1% glycerin for fixation then specimens were injected by latex colored with red ROTRNG ® ink. Finally specimens were placed in formalin mixture solution for 3-4 days, before they were subjected to manual dissection.

Results

I- The cerebellar surface of the inner ear (Fig. 2,5):

The cerebellar surface of the inner ear is clearly separated from cranial bone by capacious place. It is relatively concave, and is characterized by two large depressions. The first is the internal acoustic meatus (Fig. 2/B), placed posteroventraly directly overlying the cochlea, is shallow. The second depression (Fig. 2/A), the subarcuate fossa, is posterolateral to the internal auditory meatus, overlying the pars mastoidea.

II- The internal auditory meatus:

The internal auditory meatus (Fig. 2/B), is located on the medial side of the petrosal part of the temporal bone provides communication between the endocranial cavity and the inner ear. The bottom; at the fundus of internal acoustic meatus, four foramens for facial and vestibulocochlear nerve can be detected. A clear transvers crest run oblique posterodorsal (Fig. 2/ E) divided the four foramens into two foramens anteriordorsal and two posteroventral. The anterior portion of anteriordorsal foramens for facial nerve (Fig. 2/C), which is the largest and the other portion (Fig. 2/D) which lie posterior, for branches to the utricle and the ampulla of the anterior and lateral membranous semicircular ducts. The anterior portion of the posteroventral foramens (Fig. 2/H) for cochlear nerve and the other posterior portion (Fig. 2/J) for nerve to the ampulla of the posterior semicircular duct.

At the internal acoustic meatus, the Facial nerve passes through the dorsal opening of the internal auditory meatus nearly at 45 degree on horizontal plane (Fig. 5/2) to enter the petrosal bone of the temporal bone. The ventral portion of the internal auditory meatus is pierced by various branches of vestibulocochlear nerve at 34.8 degree on horizontal plane (Fig. 5/1), and some of these openings are discernible on (Fig. 2).

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Figure 1. Coronal computed tomography image (C.T) of the camel temporal bone show 1. The pons; 2. Sphenoid bone; 3. Mastoid process ; 4. Inner ear; 5. Facial nerve ; 6.geniculate ganglia; 7.The middle ear.

III- Arterial blood supply ( Fig. 7,3 )

The artery of the inner ear of the camel is the labyrinthine artery (Fig. 3/6) arises from the vertebral artery system. In all samples the labyrinthine artery arises from caudal cerebellar artery (Fig. 3/2). The direct detachment from the basilar artery (Fig. 3/1) not exists in camel.

The labyrinthine artery of the camel is very small vessel. Its diameter, length and angle with caudal cerebullar artery at site of origin vary from specimen to other and vary from right to left side in two specimens. In all specimens the diameter of the labyrinthine artery is approximately 0.5 mm. In two samples in the level which the caudal cerebellar artery detached the labyrinthine artery received a branched arise directly from basilar artery.

In internal acoustic meatus at the fundus, the labyrinthine artery divides into two branches, the cochlear and vestibular artery. The cochlear artery enters the modiolus; a pillar of bone presents in the center of the cochlea, and become tortuous. The cochlear artery subdivides to several twigs to spiral ganglia and the membranous labyrinth. The cochlear artery (Fig. 7/3) passes through spiral lamina; a bone projects from the inner wall of the cochlear canal, via perforation made by the dendrites from the spiral ganglion cells (Fig. 4/8) in the interscalar septum this twigs conveys radiating arterioles to the spiral ligament and stria vascularis.

The spiral ligament and stria vascularis (Fig. 9) of the camel is extended and occupies wide space in lateral wall of the cochlea. The stria

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Fig. 2, A, Subarcuate fossa; B, Internal acoustic meatus; C, Facial nerve foramen; D, Foramen for utricle and the ampullae of the anterior semicircular canal nerve; H, Foramen for cochlear nerve; J, Foramen for saccule and the ampulla of posterior semicircular canal; E, Ridge divided the upper and lower part of internal acoustic meatus.

vascularis appear spongy and contain extensive meshwork of capillaries (Fig.4/ 5, 9).

The cochlea has bony canals, for the arterioles to run through it. They are numerous with a wide perivascular space (Fig. 4/6). The perivascular space around the radiating arteriole is made of loose connective tissue without bony tissue. There are many canals are observed not contain blood vessels.

The vestibular artery detached branches distributed to the utricle, sacula and semicircular ducts.

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Figure. 3. Image showing blood supply to right inner ear; ventral view of brain. 1. Basilar artery; 2.caudal cerebullar artery; 3.Abducent

nerve; 4. Facial nerve; 5.vestibulocochlear nerve; 6.labyrinthine artery; 7.branche from basilar artery.

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IV- Innervation

The inner ear of the camel was innervated by the vestibulocochlear nerve (Fig. 5/1), which divided into cochlear and vestibular nerve in the internal acoustic meatus at it’s the fundus. The vestibular nerve distributed into the utricle, sacula and semicircular ducts, while the cochlear nerve gave a branch to saccula and then enters the modiolus.

Cochlear nerve appears runs directly toward the helicotrema, parallel to the modiolus in hemisectioned cochlea (Fig. 8/2). While it

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Figure 4. Histological hemisectioned to modiolus; 1, modiolus; 2, scala vestibule, 3, scala tympani; 4, spiral lamina; 5, stria vascularis; 6, perivascular space contain blood vessels 7, cochlear nerve; 8, cochlear artery; 9 spiral ligament; 10, organ of corti.

pass through modiolus, the cochlear nerve form aggregations of nerve cell body; spiral ganglia (Fig. 4/4).

In histological section the spiral ganglia seems to be located in multiple cavities in the primary lamina and spired around modulus to form the spiral canal. These ganglia appear as large circular areas, with large number of nerve cells in compared with other mammals. In between these ganglia a perivascular space (Fig. 4/6) for cochlear artery. This feature is the most prominent structure in the histological section.

The dendrites from the spiral ganglion cells pass through the spiral lamina (Fig. 4/7) to perforate its free edge; perforated habenula and end in the organ of corti.

V- The facial nerve) Fig. 6)

The facial nerve passes through the internal acoustic meatus at its anterior portion of anteriordorsal foramens. It enters the petrous part of the temporal bone make canal called the facial canal) black arrow in Fig. 6). The canal makes a sharp curve in which the geniculate ganglia (Fig. 1/6) of facial nerve locate at the summit of the bend. Then the facial nerve passes along the wall of the tympanic recess ) Fig. 6/4), and is separated from the wall by mucosa in parts. In two samples, the facial nerve can protrude and became partially visual, where the stapedial nerve perforates the mucosa to innervate the stapedial muscle) Fig. 6/6).

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Fig. 5, 1, Vestibulocochlear nerve; 2, Facial nerve; 3, Internal acoustic meatus; 4, Subarcuate fossa; 5, Trigeminal ganglia; 6, The pone.

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Fig.7 Diagram showing arterial blood supply of the camel inner ear; 1, caudal cerebullar artery; 2, labyrinthine artery; 3, cochlear artery; 4, vestibular artery; 5, Cochlear duct; 6, Utricle and sacula; 7, semicircular ducts.

Fig. 6, 1, promontorium; 2, round window; 3, external auditory meatus; 4, tympanic recess; 5, facial

nerve aperture; 6, foramen for stapedial muscle; in the right diagram showing the pass of the facial

nerve beside the cochlea.

Disscution

The camel has the same general component and arrangement of the osseous labyrinth consequently the arrangement and branches of the arterial blood supply and innervation are similar to other animals.

During the pathway of the caudal cerebellar artery to internal acoustic meatus, it received anastomosis from basilar artery or run direct to internal acoustic meatus without any anastomosis. Both cases exist in same sample in all samples. The pattern of anastomosis is characteristic for each sample; differ from sample to anther in all samples, which has been examined. This pathway not well illustrated and neither present in any literature before.

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Figure 9. A SEM showing the interscalar septum, 1, stria

vascularis; 2, spiral ligament.

Fig.8 Diagram showing innervation of the camel inner ear; 1, vestibulocochlear nerve; 2,cochlear nerve; 3, vestibular nerve; 4, Utricle and sacula; 5, cochlear duct; 6, semicircular ducts.

In horse the labyrinthine artery usually arises from the caudal cerebellar artery and enters the internal acoustic meatus (Getty and Sisson, 1975). In human the labyrinthine artery may arise from basilar artery (Nomura, 2013). In all samples which are examined for the arterial blood supply of the inner ear of the camel the labyrinthine artery comes from caudal cerebellar artery. In both left and right side the caudal cerebellar artery has to make a loop underneath abducent nerve.

The pathway of the caudal labyrinth artery dorsal to abducent nerve is characteristic of the camel vertebral system of arterial supply of inner ear of the camel. We assumed that this loop is exist as a result of restoral displacement of caudal cerebral artery branching from basilar artery, this displacement forced the caudal cerebral artery to overlap the abducent nerve to descended to internal acoustic meatus.

In cerebropontine angle the vestibulocochlear nerve and facial nerve take certain angle between superficial origins from the pone to internal acoustic meatus. The angle is made as a way of accommodation of the nerves to reach its specific foramen successfully. The difference in angle between the facial and vestibule cochlear nerve due to presence of transverse crest which separate the entrance of the both nerves, result in placed one more dorsal and the other ventral.

The camel has considerable cochlear width; 11mm in compare with the cochlear width in the human 6.53 mm. In the modiolus of the camel presents spiral ganglia with large diameter in addition to presence of a wide and numerous perivascular spaces and wide spiral ligament and stria vascularis. This contributes to increase the total width of the cochlea of the camel. Subsequently it improves the high frequency limit and the best hearing frequency of the camel (Wannaprasert, 2013). Accordingly the histological finding of the present study showed that, the spiral ganglion of the cochlear nerve of the camel possesses a large number of nerve cells. This finding proved that the camel has better frequency discrimination across the higher range of frequencies used for echolocation (Fleischer, 1976; Solntseva, 2010).

The camel also possesses considerable amount of empty; a vascular perivascular space. We assumed that the perivascular space is an economic mechanism for increasing the width of the basement turn of the cochlea.

Conclusion

The inner ear of the camel has the same pattern of arrangement of both arterial blood supply and innervation. The causal labyrinthine artery make pathway by overlaying the abducent nerve. The vestibulocochlear nerve and facial nerve take different angle while pathing from pone to internal acoustic meatus. The camel possesses large diameter of both spiral ganglia and

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perivascular space in addition numerous perivascular space, there is a numerous a vascular perivascular space.

Acknowledgments

The authors would like to thank anyone helped in this work by his experience or efforts in collecting samples, CAT.

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