Diseases of the Brainstem and Cranial Nerves of the Horse: Relevant Examination Techniques and Illustrative Video Segments

IN-DEPTH: NEUROLOGY

Robert J. MacKay, BVSc (Dist), PhD, Diplomate ACVIM

1. Introduction (pons and cerebellum) and myelencephalon (me- This lecture focuses on the functions of the portions dulla oblongata). Because the diencephalon was of the brainstem caudal to the diencephalon. In discussed in the previous lecture under Forebrain addition to regulation of many of the homeostatic Diseases, it will not be covered here. mechanisms of the body, this part of the brainstem controls consciousness, pupillary diameter, eye 3. Functions (Location) movement, facial expression, balance, prehension, mastication and swallowing of food, and movement Pupillary Light Response, Pupil Size (Midbrain, Cranial and coordination of the trunk and limbs. Dysfunc- Nerves II, III) tion of the brainstem and/or cranial nerves therefore In the normal horse, pupil size reflects the balance of manifests in a great variety of ways including re- sympathetic (dilator) and parasympathetic (con- duced consciousness, ataxia, limb weakness, dys- strictor) influences on the smooth muscle of the phagia, facial paralysis, jaw weakness, nystagmus, iris.2–4 Preganglionic neurons for sympathetic and strabismus. Careful neurologic examination supply to the head arise in the gray matter of the in the field can provide accurate localization of first four thoracic segments of the spinal cord and brainstem and cranial nerve lesions. Recognition subsequently course rostrally in the cervical sympa- of brainstem/cranial nerve dysfunction is an impor- thetic nerve within the vagosympathetic trunk. tant step in the processes of diagnosis and treat- After synapse in the cranial cervical ganglion adja- ment. cent to the guttural pouch, the post-ganglionic sympathetic neurons continue to the smooth muscle of 2. Anatomy and Nomenclature the orbit and act to cause pupillary dilation. Emo- The brainstem includes the diencephalon, mesen- tional and other influences on sympathetic pupillary cephalon (midbrain), and rhombencephalon (hind- tone are governed by hypothalamic centers that act brain).1 With the exception of the olfactory nerves through upper motor neuron (UMN) tracts descend- (I), all cranial nerves are arrayed along the brains- ing from the midbrain. Interruption of pre- or post- tem. The hindbrain is divided into metencephalon ganglionic sympathetic nerves to the eye causes

NOTES

AAEP PROCEEDINGS ր Vol. 57 ր 2011 353 IN-DEPTH: NEUROLOGY Horner’s syndrome, with miosis of the pupil, ptosis component of the facial nerve contains fibers from (reflecting hypotonia of the dorsal tarsal (Mueller’s) the tongue (taste) and middle ear. muscle), and spontaneous sweating and vasodilata- tion over the side of the face. Parasympathetic Balance and Equilibrium (Medulla, Cranial Nerve VIII), preganglionic neurons arise in the midbrain and exit Hearing (Medulla, Cranial Nerve VIII, Forebrain) the skull in the oculomotor nerve (III). These neu- The vestibular system is responsible for orientation rons synapse behind the eye in the ciliary ganglion. of the horse relative to gravity. The receptor is in Post-ganglionic neurons pass along the optic nerve the bony labyrinth of the inner ear. The membra- to innervate the ciliary muscle and constrictor of the nous labyrinth includes 3 semicircular ducts con- pupil. The afferent part of the pupillary light reflex taining endolymph that connect to vestibular nerve passes via the optic nerves and optic tracts, past the endings at the cristae ampullares. Vestibular neu- thalamus, to terminate in the midbrain. There is rons pass centrally through the internal acoustic extensive decussation of these tracts both in the meatus to penetrate the rostral medulla and termi- chiasm and midbrain. nate in 4 vestibular nuclei. These nuclei have nu- merous projections to the nuclei controlling Eye Position (Midbrain, Pons, Cranial Nerves III, IV, VI) extraocular muscles, the cerebellum, and the spinal From nuclei in the midbrain and pons, the oculomo- cord. The vestibular system controls the conjugate tor, trochlear, and abducens nerves exit the cranial movements of the eyes during movement of the head cavity through the orbital fissure and ramify in the through extensive connections with the nuclei of periorbital tissues to innervate the muscles of the cranial nerves III, IV, and VI. Vestibular-cerebel- eye. The oculomotor nerve also supplies the levator lar pathways pass through the caudal cerebellar palpebrae and pupillary constrictor muscles, and peduncle. These pathways function to smoothly co- the abducens nerve innervates the retractor bulbi ordinate the movements of the eyeballs, trunk, and muscle. Lesions in these nerves (or nuclei) cause limbs with those of the head. Vestibulospinal true strabismus. tracts descend ipsilaterally to synapse on LMN and facilitate extensor muscles of the limbs while inhib- Mastication (Pons, Cranial Nerve V) iting flexor muscles. Some vestibulospinal tracts cross and reduce extensor tonus in contralateral The lower motor neurons of the trigeminal nerve limbs. arise in the pons and pass through the petrous tem- Unilateral disease involving the peripheral part of poral bone in the foramen ovale adjacent to sensory the vestibular system causes asymmetric ataxia trigeminal neurons and are distributed to the mus- with preservation of strength. The poll rotates to- cles of mastication: masseters, pterygoids, tempo- ward the side of the lesion, and the head and neck rals, and rostral digastricus. With unilateral may be turned toward the lesion. The body leans, damage to the trigeminal nucleus (or nerve), there is falls, or rolls toward the side of the lesion, and the deviation of the lower jaw toward the normal side. horse may stagger in tight circles. Because there is By 2 weeks after injury, there is obvious muscular some visual compensation for vestibular ataxia, atrophy. Bilateral severe involvement of the tri- blindfolding exacerbates the signs. In horses with geminal nuclei (or nerves) causes a dropped jaw, central vestibular disease, head tilt may be either weak jaw tone, slight tongue protrusion, and inabil- toward or away from the side of the lesion. The ity to prehend or chew feed. latter presentation is known as paradoxical central vestibular disease and usually follows involvement Facial Expression and Movement (Medulla, Cranial Nerve of vestibular connections within the cerebellum. VII) Unilateral vestibular disease often causes spontane- The facial nerves arise from nuclei in the rostral ous or positional nystagmus, and physiological (ves- medulla and exit the calvarium with CN VIII via the tibular) nystagmus may be absent or abnormal internal acoustic meatus. The nerve courses when the head is moved toward the side of the through the facial canal in the petrous temporal lesion. In peripheral disease, the nystagmus is al- bone adjacent to the middle ear and emerges ways horizontal, rotatory, or arc-shaped, with the through the stylomyastoid foramen. The facial fast phase away from the lesion. With central in- nerve is distributed to the muscles of facial expres- volvement of the vestibular system, nystagmus also sion including those of the ear, eyelid, nose, and lips may be vertical. Typically, the eye on the affected and the caudal belly of the digastric muscle. With side rotates ventrally in the orbit, whereas the eye involvement of the nucleus or proximal nerve, there on the normal side rotates dorsally (especially when is drooping of the ear and lip, ptosis, collapse of the the head is extended). This abnormal eye position nostril, and the muzzle is pulled toward the normal is termed vestibular strabismus. Bilateral vestib- side. Saliva often drools from the affected side of ular disease is characterized by severe symmetric the mouth, and the horse has difficulty prehending ataxia and wide, sweeping movements of the head food, especially grain. There may be exposure ker- from side to side. Neurons of the cochlear division atitis. The facial nerve also contributes parasym- of cranial nerve VIII pass from receptors in the pathetic neurons to lacrimal glands. The sensory middle/inner ear to auditory centers in the midbrain

354 2011 ր Vol. 57 ր AAEP PROCEEDINGS IN-DEPTH: NEUROLOGY and thalamus. A variety of local reflexes are Tongue Movement (Cranial Nerve XII, Medulla) initiated by stimulation of the cochlear nerve. In Neurons of the hypoglossal nerve originate in the addition, there is projection of conscious pathways hypoglossal nucleus in the caudal aspect of the me- for hearing from the thalamus to the cortex (tempo- dulla and emerge from the medulla as a horizontal ral lobe?). Deafness is congenital in some row of rootlets, which combine to form the nerve as “splashed white” blue-eyed horses of several differ- it enters the hypoglossal foramen. After emerging ent breeds; otherwise, deafness is rarely recognized from this foramen, the hypoglossal nerve runs for- in horses. ward and ventrally in association with the guttural pouch and stylohyoid bone to innervate the geniohy- Taste (Cranial Nerves VII, IX, X, Medulla, Forebrain) oideus and muscles of the tongue. Interruption of Taste buds are found on the surface of the tongue the hypoglossal pathways causes hemiparesis of the and also in the soft palate, pharynx, lips, and tongue, evident as deviation of the apex of the cheeks. Sensory gustatory innervation is provided tongue away from the affected side. Within 1 to 2 by the facial nerve (rostral two thirds of the tongue), weeks, atrophy of the tongue becomes noticeable. glossopharyngeal nerve (caudal one third of the tongue), and vagus (pharynx and palate). General Regulation and Smoothing of UMN Activity (Cerebellum) sensory innervation to the rostral two thirds of the The cerebellum sits in the caudal fossa of the skull tongue is provided by the trigeminal nerve, which and is separated from the cerebral hemispheres by probably also contributes gustatory information. the tentorium cerebelli. It is divided into the floc- Perception of taste involves the forebrain, including culonodular lobe and the much larger body of the the limbic system. Deficiencies in the sense of taste cerebellum. The cerebellar body consists of a me- are very difficult to detect by clinical testing. dian region, the vermis, and 2 lateral cerebellar hemispheres. Connections with the rest of the Movement of Pharynx and Larynx (Cranial Nerves IX, X, XI, CNS are via 3 peduncles: Efferent connections Medulla) pass through the rostral peduncle and afferent path- Motor innervation of the larynx and pharynx origi- ways enter the cerebellum via the middle and caudal nates in neurons in the nucleus ambiguus, a fusi- peduncles. The cerebellum regulates and smoothes form structure extending the length of the medulla. motor activity initiated by the UMN system. It This nucleus provides axons for the glossopharyn- also acts to maintain equilibrium and appropriate geal, vagus, and spinal accessory (internal branch) body posture during rest and motion. Propriocep- nerve roots. These roots form nerves that inner- tive information is gathered via afferent connections vate the soft palate, pharynx, larynx, and cranial from the spinal cord (spinocerebellar and cuneocer- esophagus via the pharyngeal plexus and cranial ebellar tracts) and vestibular system and is notified and recurrent laryngeal nerves. The vagus nerve of UMN activity via extensive connections with provides most of the motor fibers to pharyngeal mus- brainstem UMN nuclei (including the olivary nu- cles, and the glossopharyngeal muscle is the princi- cleus). Efferent cerebellar neurons project to ves- pal sensory nerve for the caudal one third of the tibular nuclei and other parts of the brainstem, tongue and the pharynx. The nucleus ambiguus is including the thalamus. There is virtually no pro- continued in the spinal cord, as the nucleus of the jection of cerebellar efferents into the spinal cord. external branch of the spinal accessory nerve (inner- Cerebellar disease is usually diffuse and manifests vation of trapezius and parts of brachiocephalicus as symmetric ataxia without weakness. There is and sternocephalicus). The facial and hypoglossal defective regulation of the rate, range, and force of nerves innervate several of the muscles that control movement. Limbs may appear spastic, with exces- movements of the hyoid apparatus; therefore, im- sive (hypermetric) or inadequate (hypometric) flex- paired movement of the hyoid apparatus caused by ion during protraction. Signs are most obvious paralysis of these nerves could affect movements of when there is a change in the force or direction of the larynx and pharynx. Clinically, such effects voluntary movement. At rest, the body may sway, are minor in horses at rest but can be revealed by laterally or backward and forward, and there may be intense exercise. Unilateral (hemiplegia) or bilat- coarse head bobbing or tremor that is exacerbated eral vagal dysfunction causes pharyngeal paralysis, by voluntary movement, such as reaching the head which interferes with swallowing and manifests as out for food. Extensor muscle tone is increased and signs of dysphagia: coughing and gagging during limb reflexes may be hyperactive. With diffuse cer- eating with return of saliva, feed, and water through ebellar cortical disease, the menace response is ab- the nostrils and mouth. Bilateral anesthesia of the sent, although vision is normal. proximal glossopharyngeal nerves does not cause dysphagia. With unilateral laryngeal hemiplegia, there is exercise-induced respiratory stridor and as- 4. Clinical Examination of Brainstem Function piration of feed into the trachea. In horses with Note that all parts of the CNS contributing to a bilateral laryngeal paralysis, inspiratory stridor oc- particular neurologic function are covered in this curs at rest, and there is aspiration pneumonia. section.2,4,5

AAEP PROCEEDINGS ր Vol. 57 ր 2011 355 IN-DEPTH: NEUROLOGY Orientation and Coordination of the Head flick of the ear, respectively. Test facial innerva- Evaluate the orientation of the head from directly in tion of lacrimal glands by performing Schirmer tear front. Any head “tilt” is described from the pa- tests. tient’s perspective; thus, if the poll is rotated to the horse’s left (i.e., clockwise from the examiner’s point Size of Pupils and Pupillary Light Reflex of view), the abnormality is described as a left head Stand in front of the horse while holding the nose- tilt. Carefully blindfold the horse and observe the band of the halter and swing the light back and forth effect on head position. Blindfolding removes vi- from one side to the other to obliquely and briefly sual input to head position and exacerbates abnor- illuminate each eye without causing constriction of malities caused by vestibular disease. Observe the the pupils. Unequal pupillary size is termed aniso- head and neck from the side. Persistent horizontal coria, a constricted pupil is miotic, and a dilated or low position of the head may indicate neurologic pupil is mydriatic. From this examination, deter- or muscular weakness of the neck, whereas ex- mine whether or not the pupils are of equal size and tended head position may be found in horses with if the diameter of each pupil is appropriate for the upper cervical vertebral problems or guttural pouch conditions. In this way, refine the diagnosis of ani- disease. Offer feed or a treat to the horse and ob- socoria to miosis or mydriasis affecting a single eye. serve the way in which the horse moves its head in Move closer to the horse and again swing the light response. Horses with cerebellar disease often from one eye to the other to elicit pupillary light make jerky or bobbing movements of the head as reflexes (without dazzle reflexes). Next, aim the they move toward the offered feed. light at the skin below one eye. Redirect the beam directly into the eye. This strong light should elicit Muscles of Mastication both a dazzle reflex in the ipsilateral eye and pupil- If the mouth hangs open and the tongue protrudes, lary light reflexes in both eyes. The dazzle reflex is there probably is bilateral paresis of the muscles an avoidance reaction to bright light. There is that close the jaw (temporalis, masseter, and ptery- blinking, retraction of the eyeball, and movement of goid). Grasp the upper and lower jaws at the level the head away from the light. A normal pupillary of the interdental space and attempt to pull the light reflex is immediate constriction of the pupils of lower jaw downward. The jaws pull apart easily in both eyes in response to light directed into one eye. horses with bilateral paresis of the masticatory mus- If the direct (i.e., ipsilateral) pupillary light reflexes cles. Tuck the forelock behind one of the ears and are normal on both sides, no further testing is nec- compare the temporalis muscles from in front of the essary. If one is abnormal, then consensual (indi- horse. Turn the head from side to side and observe rect) reflexes should be tested. To perform the and palpate the masseter muscles. The pterygoid consensual reflex, watch the pupil in one eye while muscles and cranial belly of the digastricus muscle an assistant shines the light into the opposite eye. are located on the medial side of the mandible, so they are not readily palpable. Peel back the upper Position and Movement of the Eyeballs and lower lips and examine the alignment of the While continuing to stand in front of the horse, upper and lower jaws. With acute unilateral pare- observe the position and size of the pupils while the sis of the masticatory muscles, even before atrophy head is held level (i.e., a line through the center of is apparent, the lower jaw may be deviated toward each eyeball is parallel to the ground). While keep- the normal side. ing the head level, lift the chin slowly. The eyeballs should remain stationary while the chin moves up- Facial Tone ward; thus, the eyes rotate ventrally relative to the Examine the head carefully for symmetry of facial long axis of the head. In horses with vestibular expression, particularly with respect to the ears, disease, abnormal eye positions are exaggerated by eyes, and muzzle. With complete unilateral facial this maneuver. If the pupils are in abnormal posi- paralysis, there is drooping of the ear, upper eyelid tions, try to position the head in such a way (usually (ptosis), and lower lip and immobility, narrowing, by rotation) that the pupils are normally oriented and lengthening of the affected external nare. The relative to the transverse axis of the head. For muzzle is deviated away from the affected side, and example, a horse with vestibular disease often has saliva may drool from the mouth. Any to all of ventral deviation of the eyeball on the side of the these components can be affected separately. Next, lesion and dorsal deviation on the opposite side. evaluate facial nerve function by testing “flick” re- Eye position can be normalized relative to the axis of flexes on each side of the face. Each of these re- the head simply by rotating the head in the direction flexes requires intact trigeminal sensory branches, of the ventrally deviated eye. The abnormal posi- central connections in the hindbrain, as well as function of the eyes in horses with vestibular disease is tioning facial nerves. To test these reflexes, touch termed vestibular strabismus. True strabismus is in turn the commissure of the lips, the medial and eye deviation that cannot be corrected by reposition- lateral canthi of the eye, the supraorbital fossa, and ing the head and usually reflects an anatomic anom- the ear. Appropriate responses are retraction of aly or dysfunction of nerves to the extraocular the commissure of the lip, blinking of the eye, and muscles. Further assess abducens nerve function

356 2011 ր Vol. 57 ր AAEP PROCEEDINGS IN-DEPTH: NEUROLOGY by performing a modified corneal reflex. Hold the movements as the horse attempts to move the tube eyelids closed and, through the eyelid, push the eye- into the esophagus. ball medially. The normal response to this maneuver is retraction (adduction) of the eyeball. Move Tongue the horse’s head in a horizontal arc from side to side Pull the jaws slightly apart and observe the move- and observe the movements of the eyeballs. Signs ments of the unrestrained tongue. With unilateral of physiologic nystagmus should normally be elicit- weakness, the tongue curls toward the normal side. ed—namely, a series of horizontal movements of the Grasp the tongue from one side after inserting the eyeball consisting of a rapid phase in the direction of hand through the interdental space. Note resis- head movement followed by a slow phase in the tance of the tongue to being stretched and look for opposite direction. Each fast phase is accompanied atrophy and muscular fasciculations. Gently pinch by an eye blink. Physiologic nystagmus is normal the side of the tongue with a hemostat and look for and should be distinguished from eye movements reflex retraction. Pull the tongue out one side of characteristic of vestibular disease: spontaneous the mouth, release it, and look for retraction of the nystagmus, which occurs when the head is station- tongue back into the mouth. In normal horses, one ary and in a neutral position, and positional nystag- or two chewing movements occur as the tongue is mus, which only occurs when the head is moved to quickly retracted. certain positions. In horses with asymmetric ves- References tibular disease, physiologic nystagmus often is abnormal or absent when the head is moved toward 1. Sisson S, Grossman JD. The anatomy of the domestic ani- mals. 3rd ed. Philadelphia: Saunders, 1941;784–856. the side of the lesion. 2. Mayhew IG. Large animal neurology. 2nd ed. Oxford: Wiley- Blackwell, 2008;94–131. Swallowing 3. MacKay RJ. Anatomy and physiology of the nervous system. In: Auer JA, Stick JA. Equine surgery. 3rd ed. St. Louis: It is difficult to assess competence for swallowing Saunders Elsevier, 2006;630–641. during a physical examination. On the basis of his- 4. De Lahunta A, Glass E. Veterinary neuroanatomy and clini- tory and observation, note whether feed, water, or cal neurology. 3rd ed. St. Louis: Saunders Elsevier, 1983; 319–447. saliva return through the nose, especially when the 5. MacKay RJ. Diagnostic procedures. In: Auer JA, Stick JA. horse eats or drinks. Pass a nasogastric tube into Equine surgery. 3rd ed. St. Louis: Saunders Elsevier, 2006; the pharynx and assess effectiveness of swallowing 642–658.

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