Okajimas Folia Anat. Jpn., 56(6) : 329-336, March 1980

Spatial Aspect of the Mouse Orbital Venous Sinus

By

TOSHIO YAMASHITA, AKIRA TAKAHASHI and RYOHEI HONJIN

Department of Anatomy, School of Medicine, Kanazawa University, Kanazawa 920, Japan (Director : Prof. Dr. Ryohei Honjin)

-Received for Publication, July 24, 1979-

Key Words: Mouse orbit, Orbital venous sinus, Orbital , Orbital muscle

Summary. The spatial aspect of the mouse orbital venous sinus and its topogra- phical relation to the venous system of the head were studied in serial sections by light microscopy. The orbital venous sinus was found to extend between the orbital wall and the muscle cone and had a huge invaginated sac, which began from the antero-medial part of the sinus and enveloped most of Harder's gland. The orbital venous sinus received almost all the venous drainage from the eyeball, muscle cone, Harder's gland and conjunctiva, and communicated with the , ptery- goid plexus, superficial temporal vein and . The mouse orbital venous sinus may correspond to the human superior and in- ferior ophthalmic . As well as draining blood from the orbital contents, it may play a significant role in producing exophthalmos when on the alert, in absorb- ing shock from the exterior to the orbital contents, and in promoting secretion from Harder's gland.

Introduction Materials and Methods

A large venous sinus occupying much The heads of 3 adult mice, pure strain of the retrobulbar space was reported KH-1 (Mus wagneri var. albula), were under the name of the "orbital venous removed, immersed in a mixture of 75 ml sinus" in the dog by Ulbrich (1909) and 70% ethanol, 20 ml 35% formalin and 5 in the rabbit by Davis (1929). The ex- ml pure acetic acid for 2 days and then istence of an orbital venous sinus in the decalcified according to the method of mouse was suggested by Kuga (1949). Plank and Rychlo (1952). The orbital Yamashita (1979) reported the mouse or- portion was excised, embedded in cel- bital venous sinus in a recent paper on loidin and sectioned serially at 30 the spatial aspect and fine structure of thickness in a coronal, sagittal or hori- the tarsal muscle of the mouse. zontal plane. The sections were stained The purpose of the present paper is to with hematoxylin-eosin or resorcin-fuch- descrbe the spatial aspect of the mouse sin and examined by light microscopy. orbital venous sinus and its topogra- Observations phical relation to the venous system of the head, on light microscopy of serial The mouse orbital venous sinus oc- sections of the complete orbital contents. cupied the retrobulbar space between

329 330 T. Yamashita, A. Takahashi and R. Honjin

the orbital wall and the extraocular extending between the retractor bulbi muscle cone, which is composed of four muscle and every one of the superior, rectus bulbi, a levator palpebrae superioris medial and lateral rectus muscles. It and a retractor bulbi (Figs. 1, 2 and 3). also had a huge invaginated sac which The upper part of the anterior border of originated from its antero-medial part. this sinus was found to touch the fatty Harder's gland was almost surrounded tissue located just behind the superior by this sac. orbital septum. Its lower part faced the The orbital venous sinus received al- intraorbital lacrimal gland located just most all of the veins deriving from the behind the inferior orbital septum. Its eyeball and other orbital contents (Text- medial part came in contact with the figure). The anterior ciliary veins were caruncle and the lacrimal sac. Its lateral three to four in number. They pierced part faced the posterior end of the sup- the sclera just behind the limbus, ran erior and inferior tarsal plates. The through the four rectus or two oblique orbital venous sinus had prolongations muscles and entered the orbital venous

Text-figure. A schema of the mouse orbital venous sinus and its connections with the venous system of the head (antero-medial view). a: , ac : anterior ciliary vein, c: a vein from the conjunctiva, cr : , cs : cavernous sinus, d: , e ethomoidal vein, el : a vein from the extraorbital lacrimal gland, f: facial vein, fd : frontal diploic vein, fn : a vein running along the frontal nerve, g: greater palatine vein, i : a vein from the intraorbital lacrimal gland, 1: a vein from the lacrimal sac, m: middle temporal vein, ma : a vein running along the maxillary nerve, n: nasal vein, o: orbital venous sinus, ppterygoid plexus, pc : posterior ciliary vein, s : spheno- palatine vein, so : supraorbital vein, ss : , st : superficial temporal vein, t: transverse facial vein, v: vortex vein. Mouse Orbital Venous Sinus 331 sinus. The four vortex veins left the from the , ran forwards sclera near the bulbar equator and soon between the , the mas- discharged into the orbital venous sinus. seter muscle and the intraorbital lacrimal The posterior ciliary veins, three to four gland, passed over the zygomatic arch in number, pierced the sclera around the and joined the transverse facial vein. exit of the , ran a short dis- The transverse facial vein received a tance along the dural sheath of the optic vein which arose from the lower-medial nerve, and then passed across the medial part of the anterior border of the orbital part of the retractor bulbi muscle to venous sinus, and ran along the zygo- enter the orbital venous sinus. The cen- matic arch to unite with the superficial tral retinal vein passed out of the optic temporal vein. The supraorbital vein, in nerve just behind the lamina cribrosa, its course along the supra-orbital margin, went backwards along the dural sheath received the frontal diploic vein and of the optic nerve and ran across the three veins which arose from the upper- lateral part of the retractor bulbi muscle medial and lateral parts of the anterior to enter the orbital venous sinus. The border of the orbital venous sinus. The venules in Harder's gland converged supraorbital vein was connected medially around its ducts to form two or three veins with the angular vein and laterally with which entered the orbital venous sinus. the superficial temporal vein. A small Veins derived from the conjunctiva also vein was seen which ran along the frontal entered the orbital venous sinus behind nerve, received the ethmoidal vein and the medial and lateral fornices. communicated between the angular vein The orbital venous sinus communicated and the cavernous sinus. with the cavernous sinus, the pterygoid , the facial vein and Discussion the superficial temporal vein by small branches, respectively (Text-figure). A Ulbrich (1909) reported that the dog or- vein arising from the posterior end of bital venous sinus joins the angular, the orbital venous sinus ran under the superficial temporal and iuferior orbital proximal portion of the muscle cone and veins. However, he did not describe the entered the cavernous sinus, after pas- anatomical relation of this sinus to the sing through the medial part of the superior and inferior superior orbital fissure. A vein arising reported in the dog by Fuchs (1905). from the inferior part of the orbital Davis (1929) noted that the rabbit orbital venous sinus pierced the orbital muscle venous sinus receives the four vortex and entered the pterygoid plexus. A veins and unites with the following four large medial branch of the pterygoid kinds of veins : the angular vein via the plexus ran between the masseter muscle supraorbital vein ; the retromandidular and the buccinator muscle. It joined a vein via the posterior ophthalmic vein, vein which ran along the maxillary which may correspond to the human nerve. This vein gave rise to the deep middle temporal vein ; the facial vein facial vein and joined the facial vein via the deep facial vein ; and the vertebral after running through the infraorbital vein via the internal ophthalmic vein foramen. This vein also proximally re- running through the superior orbital fis- ceived the sphenopalatine and greater sure. Based on these findings, he con- palatine veins and entered the cavernous cluded that this venous sinus may play sinus. The middle temporal vein arose an important role in the venous drainage 332 T. Yamashita, A. Takahashi and R. Honjin from the eyeball and other orbital con- in the orbital venous sinus could pro- tents. duce protrusion of the eyeball, which On the other hand, in the rat, Greene would then be effective in widening the (1935) did not describe the orbital venous visual field to facilitate detection of sinus, although he drew a vein which enemies or food. ran from Harder's gland to the pterygoid Koornneef (1977) suggested that the plexus. This vein may correspond to a soft fatty tissue occupying most of the communicating vein between the orbital human retrobulbar space may perform a venous sinus and the pterygoid plexus, shock-absorbing function. In our opinion, even though he'aid not actually reco- the orbital venous sinus of the mouse gnize the orbital venous sinus. In studies may also protect the orbital contents of on the connective tissue system of the the mouse from contusion by absorb- human orbit, Koornneef (1976, 1977) re- ing shock, in a similar way to the fatty ported that the human retrobulbar space tissue of the human orbit. Our results is occupied mainly by fatty tissue, and indicate that the orbital venous sinus he did not refer to an orbital venous almost encloses Harder's gland. This sinus. However, by orbital venography suggests that the sinus may also play and orbital computer tomography, Peeters a role in excretion from Harder's gland et al. (1977) demonstrated a venous mal- through compression of the gland as a formation of the human superior ophth- whole at the time of con jestion. almic vein which resembles the orbital venous sinus of the mouse. The present study shows that the References mouse orbital venous sinus receives al- 1) Davis, F. A.: The anatomy and histology most all the veins derived from the eye- of the eye and orbit of the rabbit. Trans. ball and other orbital contents and com- Amer. Ophthalmol. Soc., 27: 401-441, municates with the cavernous sinus, the 1929. pterygoid plexus, the facial vein and the 2) Fuchs, H.: Zur Entwicklungsgeschichte superficial temporal vein. This indicates des Wirbeltierauges. I. Ueber die En- that the orbital venous sinus may corre- twicklung der Augengefdsse des Kanin- spond to the human superior and inferior chens. Anatomische Hefte, 28: 1-257, 1905. ophthalmic veins and play an important 3) ,Greene, E. C.: The veins of the head role in the drainage of the blood from and . In : Anatomy of the rat the orbital contents to the extraorbital (Trans. Amer. Phil. Soc. N. S. Vol. 27), venous system. pp. 215-223, Philadelphia, Amer. Phil. Ulbrich (1909) reported a case of inter- Soc., 1935. mittent exophthalmos in a dog suffering 4) Koornneef, L.: The development of the from chronic dyspnea and venous con- connective tissue in the human orbit. jestion of the neck caused by deformity Acta morphol. neer1.-scand., 14 : 263-290, of the sternum. Peeters et al. (1977) also 1976. recognized intermittent exophthalmos in 5) Ibid. : Deteils of the orbital connective tissue system in the adult. Acta morphol. a patient with the above-mentioned intra- neerl.-scand., 15: 1-34, 1977. orbital venous malformation. According 6) Kuga, H.: About the vein of head of to the present findings, the mouse orbital the mouse - especially the communication venous sinus is of large extent, and its with the intracranial vein. Fukuoka acta space is apparently very large. This med., 40 : 54-64, 1949. suggests that increase in blood volume 7) Peeters, F., Kreiger, R., Verbeeten, B. Mouse Orbital Venous Sinus 333

jr. and Versteege, C.: The value of 9) Ulbrich, H.: Die venäsen Blutsinus in computer tomography, orbital venogra- der Orbita des Kaninchens. Arch. phy and carotid angiography in the Augenheilk., 65 : 179-188, 1909. diagnosis of exophthalmos. Radio!. din., 10) Yamashita, T.: The spatial aspect and 46: 430-438, 1977. fine structure of the tarsal muscle of 8) Plank, J. and Rychlo, A.: Eine Schnel. the mouse. J. Juzen Med. Soc., 88 : 1-12, lentkalkungsmethode. Zentralbl. allg. 1979. Pathol. pathol. Anat., 89: 252-254, 1952. 334 T. Yamashita, A. Takahashi and R. Honjin

Explanation of Figures

Abbreviations

b buccinator muscle. mm masseter muscle. e: eyeball. mn : maxillary nerve. f : fatty tissue. mt : middle temporal vein. fb : frontal bone. : orbital venous sinus. H: Harder's gland. on : optic nerve. i : inferior rectus muscle. r: retractor bulbi muscle. : intraobital lacrimal gland. so : superior oblique muscle. 1: lateral rectus muscle. sv : supraorbital vein. 1p : levator palpebrae superioris muscle. t: transverse facial vein. m: medial rectus muscle. tm : temporal muscle.

Plate I

Fig. 1. A sagittal section of the mouse orbit. Resorcin-fuchsin stain. x 20. Fig. 2. A coronal section of the mouse orbit at the level A indicated in Figure 1. Resorcin- fuchsin stain. x 20. Fig. 3. A coronal section of the mouse orbit at the level B indicated in Figure 1. Resorcin- fuchsin stain. x 20. 335

Plate I

T. Yamashita, A. Takahashi and R. Honjin