The muscles important to the function of the visual apparatus constitute three groups: the intraocular muscles, the extraocular muscles, and the palpebral muscles. The intraocular muscles are those that lie entirely internal to the sclera and act to regulate pupillary diameter and the shape of the lens. The extraocular muscles insert on the sclera and effect rotation and retraction of the eyeball as a whole. The palpebral muscle group includes a number of muscles of the lids and head that regulate the shape and position of the palpebral fissure.
The dilator and sphincter muscles of the iris and the ciliary muscles lie entirely within the eyeball. They are composed of smooth muscle fibers. The iris musculature acts reflexly to regulate the amount of light that reaches the retina. The ciliary muscle accomplishes visual accommodation (focusing) by altering the tension of the zonular fibers. These muscles are described in detail under the headings “Iris” and “Ciliary Body,” of which they are integral parts.
The extraocular muscles, or musculi bulbi, are striated muscles: the dorsal, medial, ventral, and lateral rectus muscles; the dorsal and ventral oblique muscles; and the retractor bulbi muscle. The expression of myosin heavy chain type-2B is restricted to extraocular muscles such as the rectus lateralis and retractor bulbi muscles.
The extraocular muscles rotate the globe around three mutually perpendicular axes passing through the center of the globe. The dorsal and ventral rectus muscles rotate the globe around a medial to lateral axis. The medial and lateral rectus muscles rotate the globe about a superior to inferior axis, and the oblique muscles rotate the eyeball around the axis bulbi. In addition, the eyeball can be retracted into the orbit along the optic axis by the retractor bulbi muscle as well as the recti muscles functioning as a group. Contraction of two or more muscles simultaneously accomplishes oblique movements. The dog is able to rotate the eye through approximately 90 degrees of arc in the dorsal plane and 60 degrees in a sagittal plane. The rotation produced by the oblique muscles is more limited, amounting to only approximately 30 degrees. The oblique muscles also help fix the eye against the posterior pull of the rectus muscles because the pull of their tendons includes an anterior vector. The sense of proprioception in the extraocular muscles is recognized by palisade endings located at the proximal and distal muscle tendon junction. Depending on the affected muscle, myositis with associated swelling may result in ventral, ventromedial, or medial strabismus.
The m. retractor bulbi is a striated muscle, derived from the lateral rectus that originates from the periosteum within the orbital fissure, lateral to the optic nerve. The retractor bulbi passes laterally between the dorsal and lateral rectus muscles and divides into dorsal and ventral components that come to lie dorsal and ventral to the optic nerve. Each component again bifurcates, forming four flat fasciculi. These diverge as they run anteriorly deep to the rectus muscles to insert on the equator of the eyeball approximately 1 cm posterior to the corneoscleral junction. The fasciculi are very broad and thin at their insertions, and in some specimens, adjacent fasciculi nearly meet to form a complete muscular cone around the posterior aspect of the eyeball. The conical space between the diverging fasciculi of the retractor bulbi and the optic nerve is filled with intraperiorbital fat.
The primary action of the retractor bulbi muscle is to pull the eyeball deeper into the orbit. This displaces the base of the cartilage of the third eyelid with its encircling gland, causing the free edge of the third eyelid to sweep across the cornea (see section on the third eyelid). The retractor bulbi may also play a part in the rotatory movements of the eye. Watrous and Olmsted (1941) reported that following excision of all other extrinsic muscles in the dog, the retractor bulbi was eventually capable of moving the eye in all directions. Blood supply to the retractor muscle is derived from the muscular branches of the external ophthalmic artery. The abducent nerve supplies general somatic efferent axons to the retractor muscle.
The four mm. recti are named for the position of their insertion on the globe. They originate in proximity to one another at the apex of the periorbital cone. The dorsal rectus originates between the optic canal and the orbital fissure. The lateral, medial, and ventral recti originate ventral to the orbital fissure in order from dorsal to ventral. From their origin they diverge toward their insertions on the dorsal, lateral, medial, and ventral aspects of the eyeball. Over most of their course, the rectus muscles are deep to the periorbita and superficial to the fascicles of the retractor bulbi. Dorsally, the m. levator palpebrae superioris is interposed between the dorsal rectus and the periorbita.
The global and orbital layers of canine rectus muscles have different passive viscoelastic properties. The mean elastic modulus (stiffness) of the global layer is approximately 35% greater than the orbital layer and the mean elastic modulus of both layers of dog rectus muscles is significantly greater than that of fastand slow-twitch skeletal muscles.
The muscle bellies of the rectus muscles are oval in transverse section, measuring approximately 9 mm wide by 2 mm thick at their broadest point. The medial rectus is slightly larger than the other recti, which are comparable in size. At approximately the equator of the globe, the muscles form flat tendons that insert on the sclera anterior to the insertion of the m. retractor bulbi, 3 to 7 mm posterior to the corneoscleral junction. Anterior to the equator of the lens, the dorsal rectus passes dorsal to the tendon of insertion of the dorsal oblique muscle. The tendon of the ventral rectus passes deep to the ventral oblique muscle. The actual distal locations of insertion of the tendons of the extraocular muscles vary among breeds at least perinatally. Kleckowska et al. (2006) found that the tendons of the dorsal, ventral, and lateral recti muscles of American Staffordshire terriers insert further from the limbus than those of the dogs of Bordeaux. On the other hand, the muscular funiculi of the retractor bulbi of the dogs of Bordeaux were overall more posteriorly attached than those of the American Staffordshire terriers.
The action of the rectus muscles has been described. The oculomotor nerve is motor to the dorsal, medial, and ventral recti. The abducent nerve innervates the lateral rectus. The rectus muscles are supplied by the muscular branches of the external ophthalmic artery. Venous return is by means of muscular branches of the external ophthalmic veins.
The m. obliquus dorsalis arises at the dorsomedial margin of the optic canal closely associated with the origin of the other extraocular muscles. It runs anteriorly within the periorbita between the dorsal and medial recti. At approximately the posterior pole of the eyeball, the muscle gives rise to a thin, round tendon that passes over a small cartilaginous trochlea located at the phylogenetic origin of the muscle on the medial wall of the orbit near the medial angle of the eye.
The trochlea is a small, oval plate of hyaline cartilage in the periorbita. It is firmly anchored to the medial orbital wall by three ligamentous thickenings of the periorbita. The longest of these runs from the anterior end of the trochlea to the periosteum at the medial commissure of the eyelids. A short ligament anchors the trochlea to the dorsal orbital margin, and a third runs from the posterior aspect to the periosteum of the zygomatic process of the frontal bone.
The tendon of the dorsal oblique muscle runs through a groove in the trochlea formed by a prominence on its medial face near the anterior end. A synovial sheath (vagina synovialis m. obliqui dorsalis) is present at this point. As the tendon passes over the trochlea, it turns through an angle of approximately 135 degrees to the muscle belly to run obliquely caudodorsolaterally to its insertion on the sclera deep to the tendon of the dorsal rectus muscle.
The dorsal oblique muscle consists of central and peripheral layers made up of Type I (dark) and Type 2 (light) muscle fibers. The mean total area of the dorsal oblique muscle (N = 6) is 9.95 (±4.01) mm2 of which 44.8% (±4.4) corresponds to the central layer (Vivo et al., 2004). The dorsal oblique muscle is the only structure innervated by the fourth cranial nerve (n. trochlearis).
The m. obliquus ventralis is the only extraocular muscle that arises from a site remote from the apex of the orbit. The ventral oblique originates from a small depression in the palatine bone near the junction of the palatomaxillary and palatolacrimal sutures. In prepared skulls this site may appear as a foramen, because the attachment plate is thin and easily lost. The muscle courses dorsolaterally, passing ventral to the insertion of the ventral rectus. It is fusiform in shape and roughly circular in transverse section. At the ventrolateral aspect of the orbit, it gives rise to two short tendons. The shorter tendon inserts deep to the insertion of the lateral rectus. The superficial portion passes lateral to the lateral rectus to insert on the superiolateral aspect of the eyeball. The ventral oblique is supplied by branches of the malar artery. The muscle is innervated by the oculomotor nerve.
Christiansen et al. (1992) studied the effect of cranial nerve III denervation on the canine extraocular musculature. This study suggested a variable response to denervation depending on the muscle fiber type and influenced by whether the individual muscle fibers were singly or multiply innervated. They found significant, persistent atrophy of the singly innervated fibers of extraocular muscle. The multiinnervated fibers were predominantly spared from denervation atrophy. These results suggest a relative neurotrophic independence of multiinnervated fibers in canine extraocular muscle.
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