Ординатура / Офтальмология / Английские материалы / Slatter's Fundemental of Vetrinary Ophthalmology 4th edition_Maggs, Miller, Ofri_2008

light in trauma cases indicates that the brain disturbance (e.g., hemorrhage, edema) is advancing and the oculomotor neurons in the midbrain are nonfunctional (Figure 16-14). This progression often accompanies severe contusion of the midbrain with hemorrhage, usually along the midline, which may cause brain swelling and herniation of the occipital lobes ventral to the tentorium cerebelli, accompanied by compression and displacement of the midbrain or oculomotor nerve (or both).

The cause of unilateral or bilateral miotic pupils in acute brain disease is not known. It probably represents facilitation of the oculomotor parasympathetic neurons released from higher-center inhibition owing to its functional disturbance. Pupillary changes may take place hourly after head trauma. Unilateral mydriasis that in some cases may be accompanied by miosis of the other pupil is probably brought about by compression of the ipsilateral oculomotor nerve; the pupils, though anisocoric, may be slightly reactive.

Experiments in dogs have shown that compression of the brainstem tectum at the level of the rostral colliculus causes miosis. Compression of CN III produces mydriasis.

Lesions Causing Pupillary Light Reflex

Abnormalities in Visual Patients

Abnormalities in pupillary constriction that are not accompanied by visual deficits localize the lesion to the oculomotor nerve

after it has exited the mesencephalon. As noted previously, the oculomotor nerve provides (1) somatic efferent innervation to the dorsal, medial, and ventral recti muscles, the ventral oblique muscle, and the levator palpebral muscles and

(2) parasympathetic innervation to the iridal sphincter. Both functions may be affected by lesions to the nerve. Therefore such a patient will present with three clinical signs (see Figure 16-11):

•A fixed, dilated pupil, due to loss of parasympathetic innervation to the iris sphincter. This sign is also called internal ophthalmoplegia.

•Ventrolateral strabismus, due to loss of innervation to the dorsal, medial and ventral recti and the ventral oblique muscles. This sign is also called external ophthalmoplegia.

•Ptosis of the upper eyelid, due to loss of innervation to the levator palpebral muscle

Common sites for lesions of the oculomotor nerve are the cavernous sinus or orbital fissure. Therefore tumors or inflammations at these sites cause cavernous sinus syndrome and orbital fissure syndrome, respectively. Because CNs IV, V, and VI also pass through these sites, both syndromes are also characterized by deficits in the function of these nerves.

It is possible for patients with oculomotor nerve lesions to present with internal ophthalmoplegia, indicating loss of parasympathetic oculomotor function, without loss of innervation to the eyelid and extraocular muscles. In other words, these patients will present with fixed, dilated pupils but no strabismus or ptosis. This presentation is possible because of the topographical arrangement of the fibers in CN III: The parasympathetic fibers are superficial and medial to the motor fibers. Therefore compression during midbrain swelling or displacement may affect the former but not the latter.

Fixed, dilated pupils caused by parasympathetic denervation are also a characteristic sign of dysautonomia. Because patients also suffer from concomitant sympathetic denervaiton, the disease is discussed later in this chapter.

Additional Causes of Pupillary Light Reflex Abnormalities

PLR abnormalities and anisocoria may also be caused by several processes that are unrelated to neurologic disease:

•Iris degeneration with atrophy causes ipsilateral mydriasis with a variable response to light (sometimes none). This is more common in older animals.

•Glaucoma causes ipsilateral mydriasis as increased intraocular pressure paralyzes the pupillary sphincter.

Table 16-3 Pupillary Reactions in Intracerebral Injury

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FIGURE 16-13. Unilateral mydriasis due to an old trauma that caused sectioning of the left optic nerve.

FIGURE 16-14. Bilateral mydriasis following head trauma.

Therefore there is no direct or indirect PLR in the affected eye. The consensual reflex to the contralateral eye is often lacking, because sustained elevation of intraocular pressure also damages retinal function.

•Anterior uveitis causes stimulation and spasms of the pupillary constrictor and ciliary muscles, resulting in miosis. Alternatively, anterior uveitis may cause posterior synechia, thus affecting pupil motility.

•Ocular disorders causing pain (e.g., keratitis) induce activation of the oculopupillary reflex. Therefore ocular pain leads to ipsilateral miosis due to spasms of the ciliary and iridal muscles.

•Feline leukemia virus infection occasionally results in static anisocoria. An RNA virus has been found in the short ciliary nerves and ciliary ganglia of some cats with this condition.

LESIONS CAUSING STRABISMUS

Function of the Extraocular Muscles

Innervation and action of the extraocular muscles are summarized in Figure 16-15 and Table 16-4. The globe has three axes of rotation, and the muscles are grouped into three opposing pairs. Each muscle in the pair acts in a reciprocal manner with its partner, similar to flexor and extensor muscles in the limbs.

Such a pair of extraocular muscles is termed yoke muscles. When the two eyes move in the same direction the movement is called conjugate. Around a horizontal axis, passing transversely through the center of the globe, the medial rectus muscle adducts and the lateral rectus muscle abducts the globe. Around the anterior-posterior axis, through the center of the globe, the dorsal oblique intorts the globe (rotates the dorsal portion medially toward the midline), and the ventral oblique extorts the globe (moves the same point laterally away from the midline). The dorsal and ventral rectus muscles rotate the globe dorsally and ventrally, respectively.

The extraocular muscles of both eyes do not function independently. Rather, they act together in a synergistic or antagonistic manner to provide conjugate movements of the two eyes in the same direction at the same time. This is demonstrated, for example, by the action of the medial and lateral rectus muscles in horizontal conjugate movement. When the eyes move conjugately to the right, facilitation of abducent neurons to the lateral rectus of the right eye and inhibition to those of the left eye are required in conjunction with inhibition of the oculomotor neurons to the medial rectus of the right eye and facilitation to those of the left eye. The medial longitudinal fasciculus (MLF) functions in coordinating this activity.

Functions of the extraocular muscles in domestic animals do not compare exactly with those in humans because of anatomic differences in the position of the eye with respect to the muscle insertion. Another difference between humans and animals is the presence of a retractor bulbi muscle, which is present in many mammalian species (but absent in birds and reptiles). As the name implies, this muscle, innervated by CN VI, is responsible for retracting the globe in response to pain or threats.

Lesions Causing Strabismus

Strabismus, an abnormal position of the eye, results from lesions of the nuclei or cranial nerves that innervate the striated extraocular muscles (CNs III, IV, and VI). It may also occur in some head positions with lesions in the vestibular system. When a strabismus is suspected, the eye movements are tested to verify the paralysis of the extraocular muscles. The head of the patient is moved vertically or horizontally while symmetry of ocular movements is evaluated. Movements of the head require a simultaneous conjugate response by both eyes to maintain fixation on objects in the visual field. The vestibular and cervical proprioceptive systems exert considerable influence on the nuclei of the cranial nerves that innervate the extraocular muscles in order to move the eyes so that they remain fixated on the visual target. One of the major pathways involved in connecting the vestibular system to these nuclei is the MLF.

Lesions of the vestibular system or MLF may cause an abnormal ocular position when the head is in certain positions. This appears as strabismus but usually can be corrected by repositioning of the head (see following section). Strabismus resulting from faulty extraocular muscle innervation persists in all positions of the head.

It should be remembered that strabismus may be also be caused mechanical and muscular disorders within the orbit that restrict movement of the globe. Common causes include tearing of extraocular muscles following traumatic proptosis, and orbital fractures that cause incarceration of muscles.

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Strabismus due to Disorders of the Vestibular System

Strabismus that occurs only in certain positions of the head indicates lesions in the vestibular system. It can occur peripherally with lesions in the inner ear and vestibulocochlear nerve (CN VIII) or centrally with lesions in the vestibular nuclei of the medulla or vestibular pathways in the cerebellum. The strabismus involves the eye on the same side as the vestibular abnormality, is usually a ventrolateral strabismus, and is present with only some positions of the head. It is most evident when the head and neck are extended. Normally, in small animals, both eyes elevate and remain in the center of the fissures so that no sclera is visible. This normal ocular elevation is less obvious in horses and least in cattle. In vestibular disease the eye on the affected side fails to elevate normally in the palpebral fissure. Sclera is evident dorsally in the “drooped” eye. The ventrolateral strabismus associated with vestibular disease can be differentiated from the strabismus of an oculomotor nerve lesion based on of the presence of abnormal nystagmus and signs of vestibular system disturbance in the former. Furthermore, in oculomotor nerve lesions there is inability to adduct the eye normally on testing of normal nystagmus, as well as ptosis and mydriasis. (Nystagmus and lesions to the vestibular system are further discussed later, under Vestibular System.)

Strabismus due to Lesions in Innervation of the

Extraocular Muscles

OCULOMOTOR PARALYSIS. Lesions of the oculomotor nucleus, or oculomotor nerve lesions, cause a lateral and slightly ventral strabismus— exotropia—primarily from loss of innervation of the medial rectus and secondarily from the denervation of the dorsal and ventral recti muscles and the ventral oblique muscle (see Figures 16-11 and 16-15, B). There is experimental evidence to support the direction of this strabismus, although it is difficult to explain the ventral deviation on the basis of the anatomy of the oblique muscle. Due to the lesion, eye adduction is deficient due to denervation of the medial rectus muscle. This can be observed on testing of normal vestibular nystagmus: As the head is moved in a dorsal plane, side to side, the eyes normally develop a jerk nystagmus with the quick phase in the direction of the head movement. The jerklike movement toward the nose is adduction resulting from contraction of the medial rectus innervated by the oculomotor nerve (CN III). This adduction, as well as lid opening and pupillary constriction, will be reduced by lesions to CN III.

Ptosis, ventrolateral strabismus, and a dilated, unresponsive pupil accompany a complete loss of oculomotor nerve function.

Causes of oculomotor nerve dysfunction were discussed in previous sections (see Pupils in Patients with Intracranial Injury and Lesions Causing Pupillary Light Reflex Abnormalities in Visual Patients). Depending on the location of the lesion, patients may present with or without other CNS and visual deficits.

Exotropia may also be seen in hydrocephalic animals that have an enlarged cranial cavity. Both eyes often deviate ventrolaterally, and therefore the syndrome is called sunset eyes. This abnormality is thought to result from a malformation of the orbit that occurs when the cranial cavity is distorted by the

early development of the brain abnormality. The eyes adduct and abduct normally on testing of normal vestibular nystagmus, and no ptosis or pupillary abnormality is present. Therefore this exotropia is not related to oculomotor dysfunction.

ABDUCENT PARALYSIS. Lesions of the abducent nucleus or nerve cause paralysis (palsy) of the lateral rectus and retractor bulbi muscles. Paralysis of the retractor bulbi muscle prevents the eye from retracting in response to a threatening gesture. This can be tested by performing the menace test while holding the upper eyelid open. Globe retraction and the resulting third eyelid elevation may be observed in a normal animal. Paralysis of the lateral rectus muscle causes unilateral esotropia (medial strabismus), resulting in asymmetry (see Figure 16-15, C). Compared with the normal eye, the affected eye cannot be abducted fully. The clinician can detect this difference by moving the patient’s head from side to side in a horizontal plane and observing the extent of abduction and adduction of each eye.

TROCHLEAR PARALYSIS. Lesions of the trochlear nucleus or nerve paralyze the dorsal oblique muscle, causing dorsolateral strabismus. In species with a round pupil, such as the dog, it is difficult to detect this type of strabismus; however, ophthalmoscopic examination may show that the superior retinal vein is deviated laterally from its normal vertical position because of the abnormal rotation caused by the tone in the unopposed ventral oblique muscle. In cats, which have vertical pupils, the dorsal aspect of the pupil deviates laterally with a lesion of the trochlear neurons (see Figure 16-15, D). In cattle and sheep, which have horizontal pupils, the medial portion of the pupil is deviated dorsally (Figure 16-16). Trochlear nerve (CN IV) lesions are rare. This abnormality is seen in polioencephalomalacia in ruminants and is thought to represent a unique susceptibility of the trochlear neurons to this metabolic encephalopathy.

LESIONS CAUSING EYELID ABNORMALITIES

Third Eyelid Abnormalities

Normally the mammalian third eyelid is kept in its position ventromedial to the eye by the tone in its smooth muscle, which keeps it retracted. This is a function of its sympathetic innervation. The normally protruded position of the eye in the orbit also contributes to the normal position of the third eyelid.

The third eyelid may protrude for a number of reasons. Except possibly in the cat, this protrusion is a passive event. The third eyelid protrudes passively when the globe is retracted actively by the retractor bulbi (CN VI). In the cat, slips of

FIGURE 16-16. Infection with Listeria monocytogenes caused ventrolateral strabismus in this sheep. (Courtesy Merav H. Shamir.)

FIGURE 16-17. Horner’s syndrome in this golden retriever presents with third eyelid prolapse, miosis, and ptosis of the upper lid in the right eye. No primary cause was diagnosed, and the syndrome was defined as idiopathic, which is a common condition in this breed.

striated muscle from the lateral rectus and levator palpebrae superioris attach to the two extremities of the membrane and may contract and contribute actively to this protrusion.

Protrusion of the Third Eyelid

Protrusion of the third eyelid is a typical feature of the following diseases:

HORNER’S SYNDROME. A constant partial protrusion of the third eyelid occurs in Horner’s syndrome because of loss of the sympathetic innervation of the smooth muscle that normally keeps it retracted (Figure 16-17). The syndrome is discussed separately later in this chapter.

TETANUS. Brief, rapid, passive protrusions (“flashing”) of the third eyelid occur in tetanus owing to the effect of tetanus toxin on neurons that innervate the extraocular muscles. This effect causes brief contractions of the muscles, especially if the animal is startled. Contraction of the retractor bulbi muscle causes passive flashing of the third eyelid. The reaction is most noticeable in horses but also occurs in other species.

FACIAL PARALYSIS. In an animal with facial paralysis the orbicularis oculi is paralyzed and the efferent branch of the menace response is interrupted, preventing the blinking response to a threatening gesture. However, in response to the menace the globe is retracted, causing a brief rapid protrusion of the third eyelid. Facial paralysis is discussed separately later in this section. Paralysis of the orbicularis oculi with ventral relaxation of the lower lid may also make the third eyelid appear protruded in cases of CN VII paralysis even though it is actually in its normal position.

“HAWS SYNDROME.” The so-called haws syndrome in cats consists of bilateral protrusion of the third eyelid. The condition is sometimes associated with diarrhea and loose stools, but in most cases the cause is unknown and the syndrome is classified as idiopathic. It has been proposed that haws syndrome is due to an imbalance in sympathetic and parasympathetic tone—that is, a decrease in sympathetic tone, causing the protrusion of the third eyelid, and an increase in parasympathetic tone. In some cases, the latter may cause greater intestinal motility, shorter fecal passage time, and diarrhea. A torovirus-like agent has also been proposed. The syndrome may persist for 4 to 6 weeks but is usually self-limiting. Protrusion of the third eyelid may be treated symptomatically with topical sympathomimetics (1% phenylephrine solution) though this is usually not required. If diarrhea is present, it also is treated symptomatically.

DYSAUTONOMIA. Bilateral protrusion of the third eyelids occurs in dysautonomia because of sympathetic denervation. However, the patient’s pupils are dilated in dysautonomia (due to parasympathetic denervation), thus distinguishing the disease

from Horner’s syndrome, in which the patient presents with third eyelid protrusion and pupillary constriction. The syndrome is discussed separately later in this chapter.

CONGENITAL MYOTONIA. This is an inherited disease of dogs and cats, characterized by persistence of active muscle contraction after the stimulation or voluntary movement has stopped. Bilateral protrusion of the third eyelids is one of the clinical signs associated with the disease.

NONNEUROGENIC CAUSES. Several nonneurogenic processes may cause prolapse of the third eyelid. Severe dehydration or emaciation are common causes of bilateral prolapse; decrease in the amount of orbital tissue causes enophthalmos, resulting in passive prolapse of both third eyelids. Enophthalmos and secondary third eyelid prolapse may also be caused by atrophy of the orbital fat or the temporal and pterygoid muscles after trauma or inflammation, and in senility. Paradoxically, an increase in the volume of orbital tissue (e.g., retrobulbar abscess, retrobulbar tumor) may cause protrusion of the third eyelid as the mass pushes the nictitating membrane. The resulting protrusion is usually unilateral.

Lesions Causing Abnormalities of the Palpebral

Fissure

Innervation of the Upper Eyelid

In small animals, the size of the palpebral fissure primarily depends on normal tone in the levator palpebrae superioris muscle. This muscle is innervated by somatic efferent fibers of the oculomotor nerve (CN III), providing for elevation of the upper eyelid. Sympathetic tone to Müller’s muscles of the eyelid helps maintain eyelid elevation. In large animals superficial facial muscles (e.g., the frontalis muscle) innervated by the facial nerve (CN VII) insert in the upper eyelid and help keep the fissure open.

Eyelid closure (blinking) is mediated by the orbicularis oculi muscle. It is innervated by the facial nerve, and its function is observed when the menace response is tested.

Lesions Increasing the Size of the Palpebral Opening

In small animals, the size of the palpebral fissure is basically unaffected by facial nerve paralysis, although it may be slightly larger because of loss of tone in the orbicularis oculi. Facial paralysis is discussed separately later in this chapter.

Occasionally in animals with serious cerebellar disease that involves the cerebellar nuclei, one palpebral fissure is slightly wider or one third eyelid is mildly elevated. These signs have also been produced experimentally with lesions in the nuclei of the cerebellum.

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strabismus with decreased ability to adduct the eye normally because of denervation of the extraocular muscles (see Figure 16-11). Lesions were discussed previously under Oculomotor Paralysis.

•Horner’s syndrome—sympathetic denervation causes loss of sympathetic tone to the levator palpebrae muscle, leading to ptosis. A lesion in the sympathetic innervation also produces enophthalmos, an elevated third eyelid, and miosis (see Figure 16-17). The syndrome is discussed separately later in this chapter.

•Facial nerve paralysis or paresis causes drooping of the upper eyelid in horses due to denervation of superficial facial muscles. Therefore the ptosis will be accompanied by inability to blink. Otitis media can affect facial neurons in all large animals, and rarely guttural pouch mycosis can involve such neurons in horses. Facial nerve paralysis is discussed in the next section.

•Hemifacial spasm—A narrowed palpebral fissure occurs with spasm of the facial muscles on one side.

•Tetanus

•A small palpebral fissure occurs following extensive atrophy of the muscles of mastication, as the eye retracts into the orbit. This atrophy can result from an extensive myositis of these muscles or from their denervation due to lesions of the mandibular nerve component of the trigeminal nerve.

Facial Nerve Paralysis

Lesions of the facial nucleus or the nerve up to the level of its termination into branches that supply the different muscle groups result in complete facial palsy or paralysis. Clinical signs of facial paralysis are as follows (Figure 16-18):

•Facial asymmetry: Paralysis is evident in the asymmetric position of the eyelids, lips, and nose. The palpebral fissure in affected small animals may be slightly wider than normal owing to paralysis of the orbicularis oculi. In large animals, the loss of tone in the frontalis muscle—which contributes fibers that elevate the upper eyelid—causes slight ptosis.

Lesions Decreasing the Size of the Palpebral Opening

A decrease in the size of the palpebral fissure is usually caused by ptosis, or drooping of the upper eyelid. Neurogenic causes include the following:

•A lesion in the oculomotor nucleus or nerve causes denervation of the levator palpebral superioris muscle, leading to ptosis. With complete oculomotor paralysis the ipsilateral pupil is dilated and is unresponsive to light directed into either eye (due to loss of parasympathetic innervation of the sphincter). There is also a lateral and slightly ventral

FIGURE 16-18. Unilateral facial paralysis (idiopathic) in a dog. Note the widened palpebral fissure, dry cornea, and drooping jaw. (Courtesy Dr. G.A. Severin.)

The ears may droop in those animals with normally erect ears, although if the ear cartilage is stiff, as in most cats and some dogs, it may keep the ear erect despite paralysis.

•Drooling of saliva: The lip may droop on the affected side, allowing saliva to drip from the corner of the mouth. It is helpful to extend the head with a finger between the mandibles and examine the corner of the lips for asymmetry. On the paralyzed side more mucosa is exposed, and drooling may be apparent.

•Displacement of the nasal philtrum: Acutely, the nose may be pulled toward the normal side, owing to the unopposed nasal muscles, especially in horses. In dogs there is slight deviation of the philtrum from its normal vertical position. During inspiration the nostril may not be opened as wide as usual on the affected side.

•Lack of blinking: In facial paralysis, eyelid closure is weak or absent. Lack of normal blinking, as well as absence of the menace response and the palpebral and corneal reflexes, is observed. In cases of suspected unilateral facial nerve paralysis, the eyelids of both sides are palpated simultaneously for strength of closure.

•Corneal desiccation and ulceration: Parasympathetic innervation to the lacrimal gland originates in the parasympathetic nucleus of the facial nerve (see Figure 16-6). These fibers run together with the motor fibers of the facial nerve till the genu. Therefore lesions to the facial nerve may also affect parasympathetic innervation to the lacrimal gland if they are located before the genu. In such cases, the patient will present with both facial paralysis and reduced tear production. Furthermore, as blinking is required to spread the tearfilm on the cornea, facial paralysis will cause desiccation of the cornea even if tear production is normal. In animals with chronic facial paralysis, dry eye and corneal ulceration may be the major clinical difficulty in management. These cases are not responsive to conventional dry eye therapy. If tear production is reduced because of lacrimal gland denervation, the patient may be treated with cholingergic drugs such as pilocarpine. Third eyelid flaps should be considered to prevent exposure of the cornea.

Lesions of individual branches of the facial nerve along their course produces paralysis restricted to the muscle groups innervated by those branches. Injury to the buccal branches of the facial nerve on the side of the masseter muscle causes the lips to droop and the nose to be pulled toward the normal side. This pattern is seen in horses that have been kept recumbent for surgery for prolonged periods without padding of the head. Eyelid and ear function is normal. On the other hand, injury to the auriculopalpebral nerve at the zygomatic arch causes paresis of the ear and eyelid muscles.

The facial and vestibulocochlear nerves are closely associated and may be affected by the same lesion in the medulla or in the petrosal bone. Both a medullary neoplasm and otitis media or interna can affect the function of these two cranial nerves at these two locations, respectively. It is important to distinguish between the two locations because of the poor prognosis for medullary lesions. Medullary lesions usually affect other brainstem structures, resulting in additional CNS signs that aid in localization of the lesion. Structures that may be affected by medullary neoplasms include the upper motor neuron, causing tetraparesis or hemiparesis; the ascending

Table 16-5 Frequency of Signs and Causes of Facial

Paralysis

CAUSES

SIGNS*

Data from Kern TJ, Erb N (1987): Facial neuropathy in dogs and cats: 95 cases (1975-1985). J Am Vet Med Assoc 191:1604.

*Total of signs greater than 100% as some animals presented with more than one sign.

reticular activating system, resulting in signs ranging from depression to coma; and the abducent nucleus, causing esotropia. General proprioception may also be affected, resulting in ataxia. On the other hand, otitis may cause sympathetic denervation, in which case the clinical signs of facial and vestibulocochlear nerve dysfunction will be accompanied by signs of Horner’s syndrome.

CAUSES OF FACIAL NERVE PARALYSIS. Frequency of the causes of facial nerve paralysis and associated disorders is shown in Table 16-5. In cats and horses, facial nerve paralysis is more commonly traumatic. In all species, otitis media involves the facial nerve as it passes through the facial canal in the petrosal bone, close to the tympanic bulla. The entire area of distribution of the facial nerve is usually affected by the resulting paresis or paralysis. Signs of vestibular ataxia and nystagmus are usually present, because the vestibulocochlear nerve in the inner ear is also involved. Lesions to the sympathetic fibers that pass near the middle ear will also cause concomitant signs of Horner’s syndrome.

Injury to the petrosal bone may cause hemorrhage in the middle and inner ears and bleeding from the external ear canal through a ruptured tympanum, usually in association with fracture of the basioccipital or petrosal bone. Facial and vestibulocochlear nerve function may be affected. In guttural pouch mycosis in horses, extensive inflammation may cause paralysis of the adjacent facial nerve in addition to Horner’s syndrome.

In dogs (and less commonly in cats) permanent or temporary spontaneous facial paralysis of unknown etiology occurs. Cocker spaniels, Pembroke corgis, boxers, and English setters are at greater risk, with dogs older than 5 years being predisposed. Temporary cases resolve within 4 to 6 weeks. Tarsorrhaphy, use of a third eyelid flap, and topical therapy may be necessary to prevent corneal dessication. An association with hypothyroidism in some cases has been confirmed in dogs.

LESIONS OF ADDITIONAL CRANIAL NERVES

Trigeminal Nerve Dysfunction

Sensory innervation to the eye, adnexa, and periocular region is via branches of the ophthalmic and maxillary nerves from the trigeminal nerve (CN V). Although the ophthalmic nerve branches are predominately medial and the maxillary are lateral, there is extensive overlap in the areas they innervate. The only autonomous zone of ophthalmic nerve innervation is a small area of skin dorsomedial to the medial angle of the eyelids. The only autonomous zone of the maxillary nerve innervation is ventrolateral to the lateral angle of the eyelids. Sensory deficits in the periocular skin will cause loss of the palpebral reflex, which is elicited by touching the medial and lateral canthi. Sensory deficits are uncommon compared with facial nerve paralysis and can be mistaken for it. However, animals with only a trigeminal nerve lesion blink spontaneously and when the eye is menaced, helping in the diagnosis.

The trigeminal nerve also provides sensory innervation to the cornea through long ciliary nerves originating in the ophthalmic branch. Loss of sensory innervation may cause corneal insensitivity, with resulting ulceration from local persistent minor trauma, or neurotrophic keratitis (see Chapter 10).

The most common cause of trigeminal nerve dysfunction is trauma. Bilateral mild injury (neurapraxia) of the mandibular branch has been seen in dogs after prehension of large objects. Bilateral disease of the trigeminal nerve motor neurons causes a drooped jaw that cannot be closed. The patient has difficulty grasping food or retaining it in the oral cavity. Manipulation of the jaw reveals muscle atonia, and neurogenic atrophy of the temporal muscles follows if paralysis persists. Unilateral disease may be difficult to discover until muscle atrophy appears. The lower jaw may be directed toward the side of the lesion by the unopposed tone in the normal pterygoids, and chewing may be asymmetric, although this abnormality is difficult to detect. The condition resolves spontaneously in 4 to 5 weeks if the dog is fed soft foods and the mandible is fastened to the maxilla. Recovery of the corneal reflex is slower than return of mandibular control. Lesions to the trigeminal nerve may also occur in conditions that affect multiple cranial nerves (see following section).

Multiple Cranial Nerve Disorders

Numerous conditions result in disorders of one or more of the nerves associated with the eye and adnexa. As mentioned previously (see Oculomotor Paralysis), neoplasms or inflammations in the orbital fissure or cavernous sinus may affect CNs III, IV, V, and VI. In cases of retrobulbar neoplasia or abscess, both CNs II and III may be affected. Numerous systemic diseases, including Cryptococcus neoformans infection, pseudorabies, GME, myasthenia gravis, listeriosis, equine focal protozoal encephalitis, and polioencephalomalacia in ruminants, may also cause multiple cranial nerve dysfunction. Some of these diseases are discussed in Chapter 18.

AUTONOMIC INNERVATION AND

ABNORMALITIES

The autonomic nervous system is a physiologic and anatomic system with central and peripheral components. It consists of higher centers situated in the hypothalamus, midbrain, pons,

and medulla. The hypothalamus is the primary integrating center for the autonomic nervous system. Nuclei in its rostral portion subserve the parasympathetic division of the autonomic system. These hypothalamic nuclei receive afferent input from the cerebrum (by numerous pathways), thalamic nuclei, and ascending general visceral afferent pathways. The hypothalamus influences the activity of the metabolic centers in the reticular formation of the midbrain, pons, and medulla.

In general, autonomic innervation is composed of two neurons interposed between the CNS and the organ innervated. The cell body of the first neuron is located in the gray matter of the CNS, and its axon passes through a cranial or spinal nerve to the peripheral ganglion, where it synapses with the cell body of the second neuron. The first neuron is therefore called the preganglionic neuron. The cell body and dendritic zone of the second neuron are in a peripheral ganglion, and its axon, the postganglionic axon, terminates in the innervated structure.

Anatomically and physiologically the autonomic system is grouped into two divisions. The sympathetic system (thoracolumbar) has cell bodies of preganglionic neurons in the intermediate gray column of the spinal cord from approximately the first thoracic to the fifth lumbar spinal cord segment. With few exceptions, the neurotransmitter released at the postganglionic axon in the sympathetic system is norepinephrine (Figure 16-19). The parasympathetic system (craniosacral) has cell bodies of preganglionic neurons in sacral segments of the spinal cord and in the nuclei of the brainstem associated with CNs III, VII, IX, and XI. The neurotransmitter released at the postganglionic axon in the parasympathetic system is acetylcholine (Figure 16-20).

Parasympathetic Lower Motor Neuron Innervation

The anatomy and diseases of the parasympathetic parts of the autonomic nervous system that pertain to the eye were discussed at the beginning of the chapter (see Pupillary Light Reflex and Lesions Causing Pupillary Light Reflex Abnormalities in Visual Patients).

Sympathetic Lower Motor Neuron Innervation

Preganglionic cell bodies are located in the first three segments of the thoracic spinal cord (see Figures 16-5 and 16-21). Their axons join the thoracic sympathetic trunk inside the thorax and pass through the cervicothoracic and middle cervical ganglia and forward in the cervical sympathetic trunk, as part of the vagosympathetic trunk. Ventromedial to the tympanic bulla, the cervical sympathetic trunk separates from the vagus and terminates in the cranial cervical ganglion, where the preganglionic axons synapse. The cell body of the postganglionic axon is in the cranial cervical ganglion.

The postganglionic axons for sympathetic ocular innervation in dogs and cats pass rostrally through the tympanooccipital fissure with the internal carotid artery and then between the tympanic bulla and the petrosal bone into the middle ear cavity, closely associated with the ventral surface of the petrosal bone. The axons continue rostrally between the petrosal and basisphenoid bones to join the trigeminal ganglion and ophthalmic nerve. The ophthalmic nerve enters the periorbita through the orbital fissure.

Postganglionic sympathetic axons are distributed together with ophthalmic nerve branches to smooth muscles of the orbit, Müller’s muscle of the upper lid (and analogous sympathetically

FIGURE 16-19. Adrenergic neuromuscular junction of the sympathetic system and actions of adrenergic agonists on the iris dilator. A, Norepinephrine (Ne) is released by axon terminal and binds to sites on iris dilator muscle, causing contraction. B, Epinephrine (Ep) and phenylephrine (Ph) are direct-acting adrenergic agonists that bind to those same sites on the iris dilator muscle, causing contraction. C, Hydroxyamphetamine (Hydroxy) is an indirect-acting adrenergic agonist that acts on nerve fiber, causing release of Ne. D, Once released from effector site, Ne is taken back up by nerve ending. E, Cocaine, an indirect-acting adrenergic agonist, prevents reuptake of Ne, allowing it to remain in the neuromuscular junction and rebind to the effector site. (From Remington LA [2005]: Clinical Anatomy of the Visual System, 2nd ed. ButterworthHeinemann, St. Louis.)

innervated tissue in the lower lid), third eyelid, ciliary muscle, pupillary dilator, and receptors in the iridocorneal (drainage) angle (see Figures 16-6 and 16-21). The exact function of autonomic innervation in control of aqueous outflow facility in the drainage angle is unknown. Normal tone of sympathetically innervated ocular structures keeps the eye protruded, the palpebral fissure widened, the third eyelid retracted, and the pupil partially dilated.

ACh

ACh

ACh Physo

FIGURE 16-20. Cholinergic neuromuscular junction of the parasympathetic system and actions of cholinergic agonists on the iris sphincter. A, Acetylcholine (ACh) is released by the axon terminal and binds to sites on the iris sphincter muscle, causing contraction. B, Pilocarpine (Pi) is a direct-acting cholinergic agonist that binds to those sites on iris sphincter muscle, causing contraction. C, Once released from the effector site, ACh is broken down by acetylcholinesterase (AChe), which prevents ACh from rebinding to site. D, Physostigmine (Physo) is an indirect-acting cholinergic agonist that inhibits AChe, allowing ACh to remain active in the neuromuscular junction. (From Remington LA [2005]: Clinical Anatomy of the Visual System, 2nd ed. Butterworth-Heinemann, St. Louis.)

Diseases of the Sympathetic System

HORNER’S SYNDROME

Clinical Signs. Loss of sympathetic innervation causes a lack of tone in the orbital smooth muscle and the eye retracts slightly, producing enophthalmos. Loss of tone in Müller’s muscle in the upper eyelid causes slight narrowing of the palpebral fissure resulting from incomplete elevation of the upper lid (ptosis). As sympathetic tone contributes to maintaining the third eyelid in retracted position, denervation (combined with retraction of the eye) causes protrusion of the third eyelid. Lack of normal sympathetic tone in the pupillary dilator causes miosis and anisocoria (see Figure 16-17). These four signs, collectively called Horner’s syndrome, are associated with lesions in any portion of the sympathetic pathway from the hypothalamus to the first three thoracic