External Ocular Muscles Control Eye Movements and Internal Ocular Muscles Control the Pupil

Neuroanatomy Ch 13 566-591

Eye Movements

-external ocular muscles control eye movements and internal ocular muscles control the pupil

-Eye movement disorders are separated into 2 levels:

1. Nuclear and Infranuclear Pathways – involve brainstem nuclei of VN III, IV, and VI; the peripheral nerves arising from these nuclei, and the eye movement muscles

2. Supranuclear Pathways – involve brainstem and forebrain circuits that control eye movements through connections with nuvlei of CN III, IV, and VI

Extraocular Muscles, Nerves, and Nuclei –

Extraocular Muscles – there are 6 extraocular muscles; also involved in torsional movement (eye slightly rotated about its axis

1.  Lateral Rectus – abduction; CN VI

2.  Medial Rectus – adduction; CN III

3.  Superior Rectus – elevation + intorsion abduction; intorsion increases with adduction; CN III

4.  Inferior Rectus – depression + extorsion abduction; extorsion increases with adduction; CN III

5.  Inferior Oblique – elevation + extorsion adduction; extorsion increases with abduction; CN III

6.  Superior Oblique – depression + intorsion adduction; intorsion increases with abduction; CN IV

1. Superior oblique passes through the trochlea (a pulley-fibrous loop on medial superior orbital rim and inserts on superior surface of eye to produce intorsion

-muscles NOT extraocular muscles are levator palpebrae superioris (raises eyelid); pupillary constrictor and dilator muscles, and the ciliary muscle (adjusts thickness of lens in response to viewing distance)

Extraocular Nerves and Nuclei – CN III, IV, and VI nerves pass through cavernous sinus and enter orbit through superior orbital fissure

-oculomotor nerve (CN III) supplies all extraocular muscles except lateral rectus and superior oblique

-after entering orbit, it splits into 2 branches: superior division supplies superior rectus and levator palpebrae superioris; the inferior division supplies MR, IR, and IO muscles

-inferior division also carries preganglionic parasympathetic fibers to pupillary constrictor muscles and to ciliary muscles of the lens

-trochlear nerve (CN IV) – supplies superior oblique

-abducens nerve (CN VI) – supplies the lateral rectus, exits dura to enter Dorello’s canal, running between the dura and the skill

-CN III, IV, and VI nuclei, together with CN XII nucleus, constitutes the somatic motor column of cranial nerve nuclei; all lie near the midline, adjacent to ventricular system, and their fibers exit brainstem near the midline, except CN IV which exits dorsally

Subnuclei of the Oculomotor Nucleus (CN III) and Functions

Subnucleus / Muscles Innervated / Side Innervated
Dorsal / Inferior Rectus / Ipsilateral
Intermediate / Inferior Oblique / Ipsilateral
Ventral / Medial Rectus / Ipsilateral
Edinger-Westphal (parasymp) / Pupillary and Ciliary muscles / Bilateral
Central Caudal / Levator Palpebrae Superioris / Bilateral
Medial / Superior Rectus / Contralateral

Diplopia – double vision can be caused in several areas:

1.  mechanical problems such as orbital fracture with muscle entrapment

2.  disorders of extraocular muscles such as thyroid disease or orbital myositis

3.  neuromuscular junction disorders such as myasthenia gravis

4.  Disorders of CN III, IV, VI

-ask patient to close one eye and see if double vision goes away, suggests diplopia was caused by eye movement abnormality

-monocular diplopia or polyopia can be caused by ophthalmological disease, but not eye movement abnormalities

-dysconjugate gaze – when extraocular muscle is not working, causes diplopia

-image farther toward direction of gaze is always seen by abnormal eye; when looking at object to the right, if one eye does not move to the right then it will form a second image that is displaced to the right

-Red glass test – transparent red glass is held over one eye (usually right) and a small white light is held directly in front of patient; image is seen in right eye as red, left eye as white

-patient is asked to follow light as it is moved to 9 positions and report locations of red and white images. Normally, the white and red images are fused in all positions

-Exotropia – abnormal lateral deviation of one eye

-Esotropia – abnormal medial deviation of one eye

-Hypertropia – vertical deviation is described only with respect to the eye that is higher

-shine a flashlight directly in front of the patient on both eyes simultaneously and then examine position of reflection of light on each cornea; normally symmetrical

-Cover-uncover test – when eye is covered while looking in direction of weak muscle, it may drift slightly back toward neutral position; this mild weakness present only with an eye covered is called a phoria in contrast to a tropia

-congenital eye muscle weakness in young children is called strabismus that causes suppression of one of the images, resulting in amblyopia (decreased vision in one eye)

Oculumotor Palsy (CN III) – causes paralysis of all extraocular muscles EXCEPT for lateral rectus and superior oblique

-remaining movements are some abduction and some depression and intorsion

-due to decreased tone in all muscles except LR and SO, eye lies in down and out position at rest

-paralysis of levator palpebrae superioris = eye to be closed unless eyelid is raised with finger

-red glass testing reveals diagonal diplopia most severe when looking UP and MEDIALLY with affected eye

-causes of CN III palsy include diabetic neuropathy and head trauma that damages the nerve, compression of nerve by intracranial aneurysms arising from posterior communicating artery with internal carotid artery

-herniation of medial temporal lobe over edge of tentorium cerebelli can compress CN III

-Ophthalmoplegic migraine is condition seen that causes reversible CN III palsy

-Aneurysms classically cause painful oculomotor palsy that involves the pupil

-Complete oculomotor palsy that spares the pupil is usually caused by diabetes

-in Partial oculomotor palso that spares the pupil – caused by partial compression of CN III by aneurysm

-Lesion of superior division results in weakness of superior rectus and levator palpebrae sup.

Trochlear Palsy (CN IV) – trochlear nerve produces depression and intorsion of the eye, and so in CN IV palsy there is vertical diplopia, and may cause hypertropia

-can improve diplopia by looking up (chin tuck) and tilting head AWAY from affected eye to compensate for hypertropia and extorsion

-vertical diplopia is most pronounced when eye is looking downward and toward nose

-Diagnosis involves FOUR basic steps

1. Affected eye has hypertropia
2. Vertical diplopia worsens when affected eye looks nasally
3. Vertical diplopia improves with head tilt away from affected eye
4. Vertical diplopia worsens with downgaze

-another test is to have patient look at horizontal line; patient with CN IV palsy will see 2 lines

-relationship between compensatory head movement and eye abnormalities is because head movement is ALWAYS in direction of action normally served by affected muscle

-for example, right CN IV palsy causes head held down and tilted to the left, normal action of right trochlear nerve is depression and intorsion of eye

-CN IV is most common injured nerve because it has a long course and thin, making it susceptible to shear

-other causes of vertical diplopia include disorders of extraocular muscles, myasthenia gravis, lesions of superior division of CN III affecting superior rector, and skew deviation

-Skew deviation is defined as vertical disparity in position of eyes of supranuclear region

-vertical disparity is constant in all positions of gaze, and is caused by lesions of cerebellum, brainstem, or inner ear

Abducens Palsy (CN VI) – lesions of CN VI causes horizontal diplopia with potential esotropia

-patients report diplopia is better when they are viewing near objects and worse when viewing far objects; affected eye does not ABDUCT normally

-mild CN VI palsy can cause incomplete burial of sclera on lateral gaze

-diplopia worsens when patient tries to abduct the affected eye

-some patients turn head toward affected eye to compensate for diplopia

-caused by injury from downward traction caused by elevated intracranial pressure; therefore CN VI palsy is early sign of supratentorial/infratentorial tumors, hydrocephalus, and other lesion

-in elevated intracranial pressure, CN VI pals is either uni or bilateral

-pontine infarcts or other disorders affecting the exiting abducens fascicles in pons cause weakness of ipsilateral eye abduction resembling a peripheral abducens nerve lesion

Gaze Palsy – movements of BOTH eyes in one direction are decreased

Pupils and Other Ocular Autonomic Pathways – pupils controlled by both parasympathetic and sympathetic pathways

-light entering 1 eye activates retinal ganglion cells, which project to both optic tracts because of fibers crossing in optic chiasm

-fibers in extrageniculate pathway continue in brachium of superior colliculus past lateral geniculate nucleus to reach pretectal area rostral to midbrain

-After synapsing, axons continue bilaterally to the Edinger-Westphal nuclei which contain preganglionic parasympathetic neurons; some crossing fibers travel in posterior commissure

-preganglionic parasympathetics travel bilaterally from Edinger-Westphal nuclei via CN III to reach ciliary ganglia in orbit and parasympathetics continue to pupillary constrictors to cause pupils to become smaller

-light shone in one eye causes direct response in same eye and consensual response in other because information crosses bilaterally at multiple levels

-Bilateral pupillary constriction also occurs through another circuit during an accommodation response, which occurs when visual object moves from far to near; with three components:

1. pupillary constriction

2. accommodation of lens ciliary muscle

3. convergence of eyes

-accommodation response is activated by visual signals relayed to visual cortex; from there, pretectal nuclei are again activated causing bilateral pupillary constriction mediated by parasympathetic fibers

-contraction of ciliary muscle of lens is parasympathetically mediated by same pathway

-ciliary muscle acts as a sphincter, so when it contracts it causes suspensory ligament of the lens to relax and produce a rounder, more convex shape

-the Sympathetic pathway – in pupillary dilation is: descending sympathetic pathway from hypothalamus travels in lateral brainstem and cervical cord to reach thoracic spinal levels T1 and T2

-descending sympathetic pathway activates preganglionic sympathetic neurons in the intermediolateral cell column of upper thoracic cord

-axons of these exit spinal cord via ventral roots of T1/2 and skirt apex of lung before joining the paravertebral sympathetic chain via white rami communicantes

-axons synapse in superior cervical ganglion à carotid plexus along walls of internal carotid artery, reaching pupillary dilator muscle

-sympathetic pathway also controls smooth muscle of the superior tarsal muscle which elevates upper lid, causing wide-eyed stare in conditions of increased sympathetic outflow

Pupillary Abnormalities – can cause anisocoria (pupillary asymmetry)

1.  CN III Lesion – lesions of efferent parasympathetic pathway from Edinger-Westphal nucleus to the pupillary constrictor muscle can cause impaired pupillary constriction resulting in a unilateral dilated pupil, decreased response to light

2.  Horner’s Syndrome – consists of ptosis, miosis, and anhidrosis

1. Ptosis – upper eyelid drooping (caused by loss of innervation to mullers smooth muscle in upper eyelid
2. Miosis – decreased pupillary size caused by loss of sympathetic innervation to pupillary dilator muscle resulting in impaired dilation
3. Anhidrosis – decreased sweating of ipsilateral face and neck, caused by loss of sympathetic innervation

-pupils still have constricting response to light, but there is a dilation lag relative to normal pupil when light is removed

-lesion commonly in sympathetic pathway in lateral brainstem, spinal cord, roots 1-3, sympathetic chain, carotid plexus, cavernous sinus, orbit

3.  Afferent Pupillary Defect (Marcus Gunn Pupil) – direct response to light in affected eye is decreased or absent, while consensual response of affected eye to light in opposite eye is normal; caused by decreased sensitivity of affected eye to light resulting from CN II lesions, retina, or eye

1. Swinging flashlight test – flashlight is moved back and forth between eyes every 2-3 seconds; afferent pupillary defect becomes obvious when flashlight is moved from normal to affected eye, and affected pupil dilates in response to light.

4.  Benign Anisocoria – slight pupillary asymmetry is seen in 20% of population and is normal

5.  Pharmacological Miosis and Mydriasis

1. Opiates cause bilateral pinpoint pupils, barbiturate overdose can also cause small pupils bilaterally
2. Anticholinergic agents can cause dilated pupils

6.  Light-Near Dissociation – pupils constrict much less in response to light than to accommodation; classic example is Argyll Robertson pupil associated with neurosyphilis, in which pupils are small and irregular, seen in diabetes and Adie’s myotonic pupil

7.  Adie’s Myotonic Pupil – degeneration of ciliary ganglion or postganglionic parasympathetic neurons resulting in mid-dilated pupil reacting poorly to light; pupillary constriction can be elicited with accommodation response

8.  Midbrain Corectopia – lesions of midbrain can cause pupil to assume irregular, off-center shape

Ptosis – eye opening is caused by levator palpebrae superior (CN III) with Muller’s smooth muscle in upper eyelid (sympathetics) and frontalis muscle (CN VII) has a small role

-eye CLOSURE is performed by the orbicularis oculi muscle CN VII

-ptosis – drooping of eyelid with causes such as Horner syndrome, CN III palsy, myasthenia gravis, redundant skin fold

-in ptosis, upper eyelid comes down farther over iris in affected eye

-in facial weakness, palpebral fissure is widened mainly because of sagging of lower lid in affected eye

Cavernous Sinus and Orbital Apex – CN III, IV, and VI all pass through and lesions can produce syndromes that affect eye movements

Cavernous sinus is a collection of venous sinusoids on either side of pituitary that receives venous blood from eye and superficialcortex and ultimately drains via several pathways into internal jugular vein

-cavernous sinus surrounds carotid siphon and nerves CN VI (closest to carotid), CN III, CN IV, and CN V1 which run in sequence with lateral wall of cavernous sinus

-maxillary nerve CN V2 skirts lower portion of cavernous sinus and runs through a short distance before exiting via the foramen rotundum

-Sympathetic fibers traveling in the carotid plexus to pupillary dilator muscle traverse cavernous sinus as well

-optic nerve lies above cavernous sinus and enters orbital apex through optic canal

-orbital apex is where all nerves, arteries, and veins of orbit converge before communicating with intracranial cavity via optic canal and superior orbital fissure

Cavernous Sinus Syndrome (CN III, IV, VI, V1) and Orbital Apex Syndrome (CN II, III, IV, VI, V1) – lesions of cavernous sinus or orbital apex can affect all or some of the nerves traversing them