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Anatomy of the Guinea Pig Temporal Bone Nebil Goksu, Nalan Karademir, Rifki Haziroglu, Ismet Bayramoglu, Yusuf Kemaloglu and Necmettin Akyeldiz Ann Otol Rhinol Laryngol 1992 101: 699 DOI: 10.1177/000348949210100814 The online version of this article can be found at: http://aor.sagepub.com/content/101/8/699

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Ann Owl Rhinol LaryngollOl:1992

ANATOMY OF THE GUINEA PIG TEMPORAL BONE RIFKI HAZIROGLU, DVM ISMET BAYRAMOGLU, MD

NEBIL GOKSU, MD NALAN KARADEMIR,

DVM

YUSUF KEMALOGLU, MD NECMETTIN AKYILDIZ, MD

ANKARA, TuRKEY

The middle ear of guinea pigs has long been used for experimental studies, but no detailed information about its temporal bone anatomy is available. In 18 adult guinea pigs, the temporal bone, eustachian tube, and inner ear anatomy, in addition to the anatomy of the middle ear, were investigated under the dissection microscope. In addition to properties of the eardrum, ossicles, air cell system, and cochlea previously described, the appearance of Huschke's foramen and the crista stapedis in an adult guinea pig ear, the structure of the eustachian tube, the architecture of the internal auditory canal, and the communication of the mastoid cells with the tympanic bulla are described. Differences and similarities among guinea pigs, other experimental animals, and humans are discussed to show the advantages and disadvantages of the guinea pig ear for experimentation. KEY WORDS -

anatomy, guinea pig, temporal bone.

INTRODUCTION

In our study, we investigated the temporal bone, eustachian tube, and inner ear anatomy in addition to the anatomy of the middle ear and its contents. Differences and similarities between human and guinea pig ears are assessed. We believe that this study will be a helpful guide for investigations that might be carried out on the ossicles, facial nerve, eustachian tube, mastoid cells, and inner ear of guinea pigs.

eardrum was dissected to expose the tympanic cavity. The bony lamina hiding the malleoincudal complex was removed to expose the relation of the malleoincudal complex to the epitympanic cavity, the lateral semicircular canal, and the superior semicircular canal, as well as the relation with the stapes and the other structures of the tympanum (Fig 2). After the malleoincudal complex was taken away, the wall of the bony facial canal was removed to reveal the course of the nerve within the temporal bone (Fig 3). In an attempt to show the inner ear structures, the basal parts of the cochlea and the bony ridge between the oval and round windows were dissected away (Fig 4). The course of the eustachian tube was followed by dissecting from the tympanic cavity toward the nasopharyngeal opening (Fig 5). Finally, the temporal bone as a whole was reflected laterally from the skull to reveal its medial aspect and the various structures of this bone, including the entry of the nerves (Fig 6).

MATERIALS AND METHODS

RESULTS

We studied 18 healthy guinea pigs, weighing 500 to 650 g, from the Central Institute of Hygiene. After painlessdecapitation and skinning, the temporal bones were exposed and all soft tissues were removed. The structures neighboring the temporal bone were identified (Fig IA,B). With use of a dissection microscope, each step was photographed. We started the dissection by removing the lateral bony plates of the "squamosal" and "mastoidlike process" portions of the temporal bone, thus revealing the epitympanic and retrotympanic air cell systems (Fig IC,D). Second, the tympanic ring was removed and the lateral portion of the external ear canal was drilled. Then the

Temporal Bone. The temporal bone of the guinea pig lies posterior and inferior to the squamosal bone. In general the guinea pig temporal bone consists of a mastoidlike process, a tympanic bulla, a tympanic ring, a petrosal segment, and a poorly developed squamosal portion that is covered by the posterior projection (tympanic hook) of the squamosal bone. Posterior to the bulla and inferior to the mastoidlike process lies a bony projection of occipital bone. The tympanic ring that forms the bony external ear canal is fused firmly to the lateral aspect of the bulla, but leaves an opening in the inferior aspect. This opening is obliterated by soft tissue that is in continuity with

Guinea pigs have long been used for animal experimentation because they are small, tame animals that are easy to control. Detailed information related to the general structure of the guinea pig is available, 1,2 but in spite of numerous otologic studies carried out on this animal, limited information about the structure of its middle ear and eustachian tube is available. Asarch et al3 and Sehitoglu et al4 have described the guinea pig middle ear and its contents.

From the Department ofOtorhinolaryngology, Gazi University School of Medicine (Goksu, Kemaloglu, Bayramoglu, Akyildiz), and the Department of Pathology, Ankara University School of Veterinary Medicine (Haziroglu, Karademir), Ankara, Turkey.

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Fig 1. Photographs taken through dissection microscope, showing A) right temporal bone of guinea pig, B) temporal bone after removal of tympanic hook (TH) of squamosal bone (SB), C) epitympanic cell (EC) and its contents after removal of lateral wall of squamosal portion (SP), and D) retrotympanic cell and its subspaces after removal of lateral wall of mastoidlike process (MLP) and tympanic ring (TR). B - branch of facial nerve, BT - tympanic bulla, EEC - external ear canal, FH - foramen ofHuschke, FN - exit point of facial nerve (stained in D), H - handle of malleoincudal complex (MIC), IC - inferior part of retrotympanic cell, LSC -lateral semicircular canal, OB - occipital bone, P - bony process of occipital bone, PB - parietal bone, SAC and SPC - superoanterior and superoposterior parts of retrotympanic cell, respectively, SSC - superior semicircular canal, TM tympanic membrane, TMJ - temporomandibular joint, TIM - tensor tympani muscle, asterisk - removed edge of tympanic hook.

the ear canal skin (Fig l A). Air Cell System. The temporal air cell system of the guinea pig is divided into two groups: epitympanic and retrotympanic cells. The epitympanic cell communicates with the bulla by a hiatus that contains the anterior portion of the malleoincudal complex. Through this hiatus the tensor tympani muscle with its bony canal is visible. The prominences of the superior and lateral semicircular canals are seen at the posteromedial wall of this space (Fig l C). The retrotympanic cell could be described as three subspaces: inferior, superoposterior, and superoanterior (Fig 10). The inferior subspace directly communicates with the inferoposterior bulla (Fig 2). The superoposterior part is separated from the inferior one by a bony ridge that contains a branch of the facial

nerve. The superoanterior part opens to the superoposterior cell. Removing the medial wall of this cell reveals the space that contains the incudal part of the malleoincudal complex; this space (attic) opens to the superoposterior part of the bulla. Tympanic Bulla. The tympanic bulla is a semispherical cavity that is bounded by the tympanic ring laterally, the mastoidlike process posterolaterally, and the epitympanic cavity superiorly. The tympanic membrane, which is extremely thin and devoid of a fibrous layer, lies in a smooth groove formed by the lateral wall of the bulla (Fig l A), The diameter of the tympanic sulcus and thus the tympanic membrane is much greater than the tympanic ring's diameter, so that a hidden space is formed anterior to the tympanic membrane.

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Fig 2. Photograph taken through dissection microscope, showing tympanic space and its contents viewed from lateral side after removal of tympanic ring, tympanic membrane, lateral wall of tympanic bulla, squamosal portion, and mastoidlike process, and bony lamina hiding ossicular complex between epitympanic cell (Be) and tympanic cavity. C - cochlea, ET eustachian tube (stained), FN - facial nerve (stained), IP - incudal part ofMIC, LP -lenticular process of MIC, LSC lateral semicircular canal (opened), MPmalleolar part of MIC, OW - oval window, PE - pyramidal eminence, RWround window, S - stapes, SMT - stapedius muscle tendon, ST - sinus tympani, asterisk - inferoposterior part of bulla (tympanic cavity), two-way arrow - passage between inferior part of retrotympanic cell (IC) and inferoposterior part of bulla. Other abbreviations as in Fig 1.

The most prominent structure in the bulla is the cochlea, which projects mediolaterally, posteroanteriorly, and to a lesser degree superoinferiorly. The

Fig 3. Photograph taken through dissection microscope showing medial wall of tympanic cavity after removal of ossicles and lateral bony wall of facial nerve in addition to structures removed in Fig 2. B - branch of facial nerve (stained), C - cochlea, CS - crista stapedis, EC epitympanic cell, ET - eustachian tube (stained), FN facial nerve (stained), FP - footplate of stapes, LSC lateral semicircular canal, RW - round window, SSCsuperior semicircular canal, ST - sinus tympani, TIMtensor tympani muscle (stained).

apical turns of the cochlea partially hide the hiatus of the eustachian tube, which lies in the anteromedial wall of the bulla (Figs 2 and 3). The oval window sealed with the stapes; the round window; the pyramidal eminence; the tendon of the stapedius muscle; the sinus tympani; the semicircular canal; and the tensor tympani muscle are visible at the superior part of the medial wall (Figs 2, 3, and 7A). The inferior part of the bulla is smooth and covered by a thin mucosa and extends posteriorly in a trough shape to communicate with the inferior retrotympanic space (Fig 2).

Ossicles. In the guinea pig, the head of the malleus and the body of the incus are fused, forming a malleoincudal complex. The fusion line of the malleoincudal complex between the malleolar part and the incudal part can be identified at a high magnification as a shallow groove (Figs 2, 7, and 8). As in humans, the handle of the malleoincudal complex is located within the two layers of the tympanic membrane (Fig IA), and the long process of the malleoincudal complex articulates with the stapes via the lenticular process (Figs 2, 7A, and 8). The stapes of the guinea pig is almost identical to that of the human with the exception of the presence of the crista stapedis, a bony bridge between the crura of the stapes above the footplate (Figs 3 and 7). There are two muscles: the stapedius muscle, which lies in a bony canal (pyramidal eminence) just beneath the facial canal and inserts into the neck of the stapes (Figs 2, 7A, and 8); and the tensor tympani muscle, which lies in a bony groove (the hiatus), its tendon inserting into the neck of the handle (Figs 1C, 4, 7A, and 8). Eustachian Tube. This is a J-shaped structure that lies in a bony hiatus at the anteromedial aspect of the bulla and leaves the bulla to reach the nasopharynx

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Fig 4. Photograph taken through dissection microscope, showing medial wall of tympanic cavity after removal of footplate ofstapes, cochlea, and bony canal of facial nerve along its whole intratemporal course in addition to structures removed in Fig 3. B - Branch of facial nerve (stained), Cosseous spiral lamina of cochlea, CN cochlear nerve (stained), ET -eustachian tube, FN - facial nerve (stained), I, II, Ill - first, second, and third parts of FN, respectively, LSC - lateral semicircular canal, S - stapes, TIM - tensor tympani muscle, V - vestibule.

(Figs 2-5). The entire guinea pig eustachian tube, unlike that of the human, is made of cartilage. It is crescent-shaped in cross section and lies in a bony

groove that extends almost to the nasopharyngeal opening (Fig 4).

Facial Nerve. After leaving the brain stem, the facial nerve enters the temporal bone through a foramen that is located superior to the entry of the cochlear nerve and anterior to the vestibular nerve. In the guinea pig, the acoustic-vestibular-facial nerve bundles enter the temporal bone directly, and no distinct internal meatus is found, but a transverse and a vertical bony crest are clearly observed (Fig 6). After a 1- to 2-mm course in the petrous portion, the facial nerve turns in an upward direction at the medial aspect of the basal tum of the cochlea, and connects with the middle ear portion of the nerve, which courses horizontally and posteriorly. Here, it courses near the oval window in an eyebrow fashion (Figs 3 and 4). Then it makes a third junction, from which it courses laterally, giving off the chorda tympani nerve (Fig 7), and it leaves the temporal bone via a foramen located posterosuperior to the tympanic ring. Just after the third junction, a tiny branch of the nerve, in a bony crista separating the retrotympanic air cells, is apparent, coursing in a posterior direction (Figs IA,B,D and 2).

Fig 5. Photograph of eustachian tube from tympanic cavity to nasopharyngeal opening, taken through dissection microscope after removal of medial and inferior wall of tympanic cavity, cochlea, and ossicles. CN - cochlear nerve, EP - extratympanic part of ET, ET - eustachian tube, FN - facial nerve, IP - intratympanic part ofET, N - nasopharyngeal opening of ET.

Inner Ear. The inner ear of the guinea pig consists of the cochlea (Figs 2 and 3), semicircular canals (Figs 1C, 2, and 3), and vestibule (Fig 4). The cochlea has 3.25 turns and projects into the bulla, just behind the eardrum and the handle of the malleoincudal complex. The round window lies in a horizontal plane that is perpendicular to the oval window plane (Figs 2, 3, and 7A). The prominences of the lateral and superior semicircular canals are visible in the epitympanic space (Fig IC). The lateral semicircular canal lies just above the facial canal (Fig 3) and anteriorly

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Fig 6. Photograph taken through dissection microscope, showing posterior aspect of temporal bone. BT - posterior aspect of tympanic bulla, CA - cochlear aqueduct. CC - carotid canal. CN - exit point of cochlear nerve. ES - bony niche overlying endolymphatic sac, FN - entry of facial nerve. MLP - posterior aspect of inferior part of mastoidlike process, PSC - posterior semicircular canal. SF subarcuate fossa. SS - groove of sigmoid sinus, VC - vertical crest. TC - transverse crest. VN - exit point of vestibular nerve.

communicates with the superior semicircular canal. which turns superiorly and posteriorly to meet the posterior semicircular canal just behind the vestibular nerve entry (Fig 6). Two trough-shaped impressions resembling the utricle and the saccule. as in the human, could be seen. From the posterior aspect of the temporal bone, the bony niche of the endolymphatic sac could easily be seen (Fig 6). DISCUSSION

As noted by others.v' the guinea pig temporal bone and its contents are similar to those of the human, but there are some exceptions that become important for experimental studies. 1. The dimensions of the eardrum and tympanic

ring are greater in the guinea pig than in the human in relation to the temporal bone dimensions, and, unlike in the human and rat, 5 the tympanic membrane of the guinea pig is devoid of a pars flaccida. 2. A foramen resembling Huschke's foramen (an opening found in the first 2 years of life in humans") is observed in the guinea pig (Fig lA). 3. The air cell system is simplified and consists of mainly four large cells, without fine trabeculations as in the human (Fig l CD). 4. The guinea pig temporal bone contains a very large and smooth hypotympanum, known as the bulla (Fig lA). This was emphasized by Asarch et al 3 and Sehitoglu et al." Hellstrom et aJ5 described a similar

Fig 7. Schematic view of A) structures on medial wall of tympanic cavity and B) footplate of stapes (FP) and crista stapedis (CS). CT -chorda tympani. FL - fusion line between malleolar part (MP) and incudal part (IP) of malleoincudal complex (MIC). FN - facial nerve in its bony canal. H - handle of MIC. LP - lenticular process of MIC. PE pyramidal eminence. RW - round window. S stapes. SMT - stapedius muscle tendon, TTM tensor tympani muscle. COCHLEA

A

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FL

Fig 8. Ossicles. A) Photograph. B) Drawing. CR - crura of stapes, FP - footplate, S - capitulum of stapes, single asterisk - attachment of stapedius muscle, double asterisk - attachment of tensor tympani muscle. Other abbreviations as in Fig 7.

C ~. ...

. S*

...•R .•....•.

)

"'0"

A hypotympanum in rats.

(Fig 6).

5. As noted in the previous studies.v' there are two ossicles: the malleoincudal complex and the stapes (Fig 8). In rats, the ossicular chain is almost identical to that in humans. S

Hellstrom et al s emphasized that the ventilatory and drainage scheme of the rat middle ear is similar to that of the human, because of the communications among the eustachian tube, the attic region, and the middle ear cavities, and so they suggested that the rat middle ear might have advantages compared with the guinea pig and chinchilla, especially in tubal blockade studies.

6. At the base of the stapes, the crista stapedis is persistent (Figs 3 and 7), as in the human ernbryo.f This bony ridge is observed in chinchillas," but not in rats.! 7. The cochlea projects well into the bulla (Figs 2 and 3). 8. The entire eustachian tube is cartilaginous. 9. The exit ofthe facial nerve is in a posterosuperior position between the tympanic ring and the mastoidlike process (Fig lA,B). 10. The cochlea consists of 3.25 turns. 11. The guinea pig lacks an internal auditory meatus ACKNOWLEDGMENf -

In conclusion, the temporal bone and ear structures of the guinea pig are good models for the human ear, and they can be manipulated with great ease if differences and similarities are known. For experimental studies, the histologic characteristics of middle ear mucosa are important, in addition to the architecture of the middle ear. Therefore, one must select the type of animal carefully, considering the aim of the study and the anatomic properties of the species.

We are grateful for the help given by G. Osmanlioglu, MD, from the Central Institute of Hygiene.

REFERENCES 1. Paterson JS. The guinea pig. In: Warden AN, Lane-Petter

W, eds. UF AW handbook. The care and management of laboratory animals. 2nd ed. Tunbridge Wells, England: Courier, 1957: 203-42. 2. Cruickshank R. The care and management of experimental animals. In: Cruickshank R, ed. Medical microbiology. 11th ed. London, England: ES Livingstone, 1968:999-1024. 3. Asarch R, Abramson M, Litton WB. Surgical anatomy of the guinea pig ear. Ann Otol Rhinol Laryngol 1975;84:250-5. 4. Sehitoglu MA, Uneri C, Celikoyar MM, Uneri A. Surgical anatomy of the guinea pig middle ear. Ear Nose Throat J 1990;

69:91-7. 5. Hellstrom S, Salen B, Stenfors LE. Anatomy of the rat middle ear. A study under the dissection microscope. Acta Anat (Basel) 1982; 112:346-52. 6. Anson BJ, Donaldson JA. The ear: developmental anatomy. In: Anson BJ, Donaldson JA, eds. Surgical anatomy of the temporal bone. 3rd ed. Philadelphia, Pa: WB Saunders, 1981:2342. 7. Browning GG, Granich MS. Surgical anatomy of the temporal bone in the chinchilla. Ann Otol Rhinol Laryngo11978; 87:875-82.

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Anatomy of the guinea pig temporal bone.

The middle ear of guinea pigs has long been used for experimental studies, but no detailed information about its temporal bone anatomy is available. I...
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