Ocular motor nerves

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23 Ocular motor nerves

Study Guidelines

General

Because of the immense diagnostic and therapeutic importance of ocular innervation, and because of its inherent complexity, neuro-ophthalmology has become a branch of medicine in its own right.

It is especially important to appreciate the way in which premotor centers are able to operate bilaterally in order to keep the gaze on target, even when the head is moving.

Particular

1 In addition to nerves III, IV, and VI, the sympathetic supply to the eye is reviewed here because it counterbalances the parasympathetic innervation contained in nerve III.

2 The nerve supply to the six muscles that move the eyeball is straightforward. However, nerve III also supplies the elevator of the upper eyelid.

3 The autonomic supply to the eye is straightforward. For the sympathetic, think of someone being startled awake at night. For the parasympathetic, think of someone eyeing food on a fork.

The Nerves

The ocular motor nerves comprise the oculomotor (III cranial), trochlear (IV cranial), and abducens (VI cranial) nerves. They provide the motor nerve supply to the four recti and two oblique muscles controlling movements of the eyeball on each side (Figure 23.1). The oculomotor nerve contains two additional sets of neurons: one to supply the levator of the upper eyelid, the other to control the sphincter of the pupil and the ciliary muscle.

Figure 23.1 Extrinsic ocular muscles.

The nuclei serving the extraocular muscles (extrinsic muscles of the eye) belong to the somatic efferent cell column of the brainstem, in line with the nucleus of the hypoglossal nerve. The oculomotor nucleus has an additional, parasympathetic nucleus which belongs to the general visceral efferent cell column.

Oculomotor nerve

The nucleus of the third nerve is at the level of the superior colliculus. It is partly embedded in the peri-aqueductal gray matter (Figure 23.2A). It is composed of five individual nuclei for the supply of striated muscles, and one parasympathetic nucleus.

Figure 23.2A–C Transverse sections of the brainstem showing the origins of the ocular motor nerves.

The nerve passes through the tegmentum of the midbrain and emerges into the interpeduncular cistern. It crosses the apex of the petrous temporal bone, pierces the dural roof of the cavernous sinus, runs in the lateral wall of the sinus, and breaks into upper and lower divisions within the superior orbital fissure. The upper division supplies the superior rectus and the levator palpebrae superioris; the lower division supplies the inferior and medial recti and the inferior oblique.

The parasympathetic fibers originate in the Edinger–Westphal nucleus. They accompany the main nerve as far as the orbit, then leave the branch to the inferior oblique and synapse in the ciliary ganglion. Postganglionic fibers emerge from the ganglion in the short ciliary nerves, which pierce the lamina cribrosa (’sieve-like layer’) of the sclera and supply the ciliaris and sphincter pupillae muscles.

Trochlear nerve

The nucleus of the fourth nerve is at the level of the inferior colliculus. The nerve itself is unique in two respects (Figure 23.2B): it is the only nerve to emerge from the back of the brainstem; and it decussates with its opposite number.

The IV nerve winds around the crus of the midbrain and travels through the cavernous sinus in company with the III nerve (Figure 23.3). It passes through the superior orbital fissure and supplies the superior oblique muscle.

Figure 23.3 (A) Middle cranial fossa with cavernous sinuses removed. (B) Coronal section in the plane of the hypophysis with the cavernous sinuses in place. III, Oculomotor nerve; IV, trochlear nerve; VI, abducens nerve; Vi, Vii, Viii, ophthalmic, maxillary, mandibular divisions of trigeminal nerve.

The nucleus of the sixth nerve, in the floor of the fourth ventricle, is at the level of the facial colliculus, in the lower pons (Figure 23.2C). The nerve descends, to emerge at the lower border of the pons, and runs up the pontine subarachnoid cistern beside the basilar artery. It angles over the apex of the petrous temporal bone and passes through the cavernous sinus beside the internal carotid artery (Figure 23.3). It enters the orbit through the superior orbital fissure and supplies the lateral rectus muscle, which abducts the eye.

Nerve Endings

Motor endings

All of the ocular motor units are small, containing 5 to 10 muscle fibers apiece (compared with 1000 or more in the tibialis anterior).

Type A fibers produce the fast twitches required for saccadic movements. Type B are slow-twitch and may be used for smooth pursuit. Type C show only local contractions beneath the individual plates. Type C fibers may be involved in keeping the visual axes of the two eyes parallel with one another. Since the visual axes diverge following administration of muscle relaxants, keeping them parallel must require continuous muscle action, even during sleep.

Sensory endings

In addition to neuromuscular spindles of standard type, numerous palisade endings exist in the form of nerve spirals around individual muscle fibers.

The extraocular muscle proprioceptors are the peripheral terminals of neurons in the mesencephalic nucleus of the trigeminal nerve. In monkeys, some of the central processes of these neurons reach as far caudally as the accessory cuneate nucleus in the medulla oblongata. This nucleus also receives proprioceptive terminals from the neck muscles, and it projects both to the ipsilateral cerebellum and to the contralateral superior colliculus. The conjunction of ocular and cervical proprioceptive information presumably assists in the coordination of simultaneous movements of the eyes and head.

Pupillary Light Reflex (Figure 23.4)

Constriction of the pupils in response to light involves four sets of neurons, as follows:

1 The afferent limb commences in the ganglionic layer of the retina, which gives rise to the optic nerve. Fibers leaving the chiasma enter both optic tracts and terminate in the pretectal nuclei, situated just rostral to the superior colliculus on each side (Figure 17.19).

2 Each pretectal nucleus is linked by internuncial neurons to both Edinger–Westphal (parasympathetic) nuclei; the contralateral nucleus is reached by way of the posterior commissure.

3 Preganglionic parasympathetic fibers enter the oculomotor nerve, leave the branch to the inferior oblique, and synapse in the ciliary ganglion.

4 Postganglionic fibers run in the short ciliary nerves and enter the iris to supply the sphincter (constrictor) pupillae.

Figure 23.4 Pupillary light reflex. For numbers, see text.

Accommodation

The near response

When the eyes view an object close up, the ciliary muscle contracts reflexly, thereby relaxing the suspensory ligament of the lens (Figure 23.5). Since the lens at rest is somewhat compressed (flattened) by tension exerted on the lens capsule by the suspensory ligament, the lens bulges passively when the ciliary muscle contracts. The thicker lens has the greater refractive power required to bring close-up objects into focus on the retina. The response of the lens is one of accommodation.

Figure 23.5 Intrinsic muscles of the eye.

The accommodation reflex, as understood clinically, involves two additional features. The sphincter pupillae contracts in order to eliminate passage of light through the peripheral, thinner part of the lens. At the same time, the visual axes of the two eyes converge, as a result of increased tone in the medial rectus muscles. The convergence is known clinically as vergence.

The three features described are also known as the near response.

Pathway for the accommodation reflex

In order to execute the near response, a stereoscopic analysis of the object is carried out at the level of the visual association cortex. The afferent limb of the reflex passes from the retina to the occipital lobe via the lateral geniculate body. The efferent limb passes from the occipital lobe to the midbrain, where some fibers activate the Edinger–Westphal nucleus and others activate vergence (convergence) cells in the reticular formation. The vergence cells activate the nuclear groups serving the medial recti, with the effect of fixating the object onto the fovea centralis of each eye. The (con)vergence response is called the fixation reflex.

The far response

Just as the state of the pupil depends upon the balance of sympathetic and parasympathetic activity, so does the state of the lens. At rest, both are in midposition. The resting focal length of the lens averages 1 meter (with considerable variation between individuals). This is because the ciliary muscle is tonically active. In order to bring a distant object into focus, the ciliary muscle must be inhibited, so that the suspensory ligament becomes taut and the lens flat. The sphincter of the pupil is inhibited as well.

The sympathetic system innervates all of the intrinsic muscles. It has a dual mode of action. It causes contraction of the dilator pupillae by way of alpha receptors on the muscle fibers; and it causes relaxation of the ciliary muscle and pupillary sphincter, by way of beta receptors. This dual effect constitutes the far response, and it is used to focus the eyes upon objects at a distance. (Note: The unqualified use of alpha and beta receptors signifies α¹ and β², respectively.)

In stressed individuals, heightened sympathetic activity may interfere with the normal process of accommodation. For example, students taking an important written test may have difficulty in bringing the questions into proper focus.

Notes on the Sympathetic Pathway to the Eye

The great length of the sympathetic pathway to the eye is indicated in Figure 23.6.

1 Central fibers descending from the hypothalamus cross to the other side in the midbrain. In the pons and medulla, they are joined by ipsilateral fibers descending from the reticular formation.

2 Preganglionic fibers emerge in the first thoracic ventral nerve root, and run up in the sympathetic chain to the superior cervical ganglion.

3 Postganglionic fibers run along the external and internal carotid arteries and their branches.

Figure 23.6 Three neuron pathways from the hypothalamus to the eye. Arrows indicate directions of impulse conduction. SCG, superior cervical ganglion. For numbers, see text.

The external carotid sympathetic fibers accompany all of the branches of the external carotid artery. Those accompanying the facial artery supply the arterioles of the cheek and lips and are particularly responsive to emotional states. Those accompanying the maxillary artery supply the cavernous tissue covering the nasal conchae (turbinate bones).

Two sets of sympathetic fibers accompany the internal carotid artery. One set leaves it to join the ophthalmic division of the V nerve in the cavernous sinus, then leaves this in the long and short ciliary nerves to supply the vessels and smooth muscles of the eyeball. The second set forms a plexus around the internal carotid artery and its branches including the ophthalmic artery. The ophthalmic artery gives off supratrochlear and supraorbital branches which carry sympathetic fibers to the skin of the forehead and scalp.

Interruption of the postganglionic fibers at the jugular foramen (see jugular foramen syndrome, Ch. 18), or in the cavernous sinus, produces anhidrosis (loss of sweating) on the forehead and scalp.

Ocular Palsies

The effects of paralysis of the motor nerves to the eye are described in Clinical Panel 23.1.

Clinical Panel 23.1 Ocular palsies

One or more of the three ocular motor nerves may be paralyzed by disease within the brainstem (e.g. multiple sclerosis, vascular occlusion), in the subarachnoid space (e.g. meningitis, aneurysm in the circle of Willis, distortion by an expanding intracranial lesion), or in the cavernous sinus (e.g. thrombosis of the sinus, aneurysm of the internal carotid artery there).

Oculomotor nerve

Complete III nerve palsy

Characteristic signs of complete third nerve paralysis are shown in Figure CP 23.1.1A. They are:

1 complete ptosis of the eyelid (unopposed orbicularis oculi)

2 a fully dilated, non-reactive pupil (unopposed dilator pupillae)

3 a fully abducted eye (unopposed lateral rectus), which is also depressed (unopposed superior oblique).

Partial III nerve palsy

The pupils are always monitored when cases of head injury come to medical attention. Rapidly increasing intracranial pressure, resulting from an acute extradural or subdural hematoma (Ch. 4), often compresses the third nerve against the crest of the petrous temporal bone. The parasympathetic fibers are superficially placed and are the first to suffer, and the pupil dilates progressively on the affected side. Pupillary dilatation is an urgent indication for surgical decompression of the brain.

Trochlear nerve

The IV nerve is rarely paralyzed alone. The cardinal symptom is diplopia (double vision) on looking down, e.g. when going down stairs. This happens because the superior oblique normally assists the inferior rectus in pulling the eye downward, especially when the eye is in a medial position.

Abducens nerve

The effect of a complete VI nerve paralysis is shown in Figure CP 23.1.1B. The eye is fully adducted by the unopposed pull of the medial rectus.

The abducens has the longest course in the subarachnoid space of any cranial nerve. It also bends sharply over the crest of the petrous temporal bone. A space-occupying lesion affecting either cerebral hemisphere may cause compression and paralysis of one abducens nerve.

’Spontaneous’ paralysis of the VI nerve may be caused by an arterial aneurysm at the base of the brain or by hardening (atherosclerosis) of the internal carotid artery in the cavernous sinus.

Internuclear ophthalmoplegia (Figure CP 23.1.2)

Interruption of the linkage between the abducens nucleus and the contralateral oculomotor nucleus gives rise to the condition known as internuclear ophthalmoplegia. As an example, a lesion of the VI–III connection shown in Figure 23.7 would leave a saccade to the right unaffected, whereas on attempting a saccade to the left, the paralyzed right medial rectus would create a divergent strabismus with accompanying diplopia. Integrity of the nucleus serving the right medial rectus is shown by its normal behavior during the vergence component of the near response.

Below the age of 40, the chief cause of internuclear ophthalmoplegia is a plaque of demyelination associated with multiple sclerosis. Above the age of 60, the chief cause is a patch of tissue necrosis associated with occlusion of a pontine branch of the basilar artery.

Ocular sympathetic supply

Any one of the three sequential sets of neurons depicted in Figure 23.6 may be interrupted by local pathology.

1 The central set may be interrupted by a vascular lesion of the pons or medulla oblongata. The usual picture is one of Horner’s syndrome (ptosis and miosis, as described in Ch. 13) and cranial nerve involvement on one side, together with motor weakness and/or sensory loss in the limbs on the contralateral side. The Horner’s syndrome is associated with anhidrosis – absence of sweating – in the face and scalp on the same side, together with congestion of the nose (engorged turbinates).

2 The preganglionic set is most often interrupted by stony, cancerous deep cervical lymph nodes in the lower part of the neck. Horner’s syndrome is associated with anhidrosis of the face and scalp (and nasal congestion) on the same side.

3 The postganglionic set accompanying the external carotid artery is rarely damaged directly. The set accompanying the internal carotid artery may be interrupted as part of a jugular foramen syndrome (Ch. 18), or by pathology in the cavernous sinus. Horner’s syndrome is accompanied by anhidrosis of the forehead and anterior scalp (territory of the supraorbital and supratrochlear arteries).

Figure CP 23.1.1 (A) Complete left III nerve paralysis. The closed eyelid has been raised by the examiner’s finger. (B) Complete left VI nerve paralysis.

Figure CP 23.1.2 Internuclear ophthalmoplegia (simulation).

Control of Eye Movements

The eyes normally move as a pair. This conjugate movement is of three fundamentally different kinds, as follows:

1 Scanning. The eyes flick from one visual target to another, in high-speed movements called saccades.

2 Tracking. In tracking, or smooth pursuit, the eyes follow an object of interest across the visual field.

3 Compensation. The gaze can be held on an object of interest during movements of the head. This is the vestibulo-ocular reflex, which depends upon displacement of endolymph in the kinetic labyrinth (Ch. 19).

Scanning

Four separate gaze centers in the brainstem pick out motor neurons appropriate to the direction of movement: leftward, rightward, upward, or downward. The centers are small nodes in the reticular formation. They contain burst cells, which discharge at 1000Hz (impulses/s) and entrain the appropriate motor neurons momentarily at this rate.

The paired centers (left and right) for horizontal saccades are in the paramedian pontine reticular formation (PPRF) (Figure 17.15). Each pulls the eyes to its own side (Figure 23.7). The midbrain contains a bilateral center for upward saccades located in the rostral end of the medial longitudinal fasciculus (MLF), at the level of the pretectal nucleus. It is called the rostral interstitial nucleus (riMLF). At the same level but a little ventral to this is a bilateral center for downward gaze (Figure 17.19).

Figure 23.7 Pathways involved in a voluntary ocular saccade to the left. (1) A projection from the right frontal eye field activates left paramedian pontine reticular formation (PPRF).

(2) Some PPRF neurons activate adjacent abducens neurons. (3) Other PPRF neurons send heavily myelinated (fast) internuclear fibers along the medial longitudinal bundle to activate oculomotor neurons serving the right medial rectus. Simultaneous contraction of the respective rectus muscles yields a saccade to the left.

Automatic scanning movements are activated by the superior colliculus, on receipt of visual information from the retina through the medial root of the optic tract. Examples of automatic scanning include the sideward glance toward an object attracting attention in the peripheral visual field, and the saccadic movements used in reading. The tectoreticular projections concerned cross the midline before engaging the gaze centers. Saccadic accuracy is controlled by the midregion (vermis) of the cerebellum, which receives afferents from the superior colliculi and projects to the vestibular nucleus.

Voluntary scanning movements are initiated in the frontal eye fields, located at the junction of motor and premotor cortex (Ch. 29). From each frontal eye field, a projection descends in the anterior limb of the internal capsule. Most of the fibers cross over before terminating in the gaze centers.

As explained in Chapter 29, the ipsilateral superior colliculus is activated at the same time, to reinforce the excitation of the appropriate gaze center.

The projection from the frontal eye field is interrupted in about one-third of patients who suffer a stroke involving the internal capsule. The result is paralysis of contraversive horizontal gaze. ‘Contraversive’ refers to an inability to make a voluntary saccade away from the side of the lesion. The gaze paralysis vanishes within a week, even if the hemiplegia remains profound – presumably because of takeover by uncrossed fibers.

The best-known afferents to the frontal eye field come from the parietal cortex, from cells concerned with visual attention. In monkeys, some cells in the posterior parietal cortex become active when an object of interest is seen. These cells project to the frontal eye field and are thought to facilitate eye movement in the direction of the object. In humans, neglect of the contralateral visual field is a well-known feature of damage to the posterior parietal lobe, especially on the right side (Ch. 32).

Tracking

The neural mechanisms for tracking must be complex because of the following basic requirements: (a) intact visual pathways to monitor the position of the object throughout the movement; (b) neurons to signal the rate of movement of the object (velocity detectors); (c) neurons to coordinate movements of the eyes and head (neural integrator); and (d) a system to monitor smooth execution of the tracking movement. Monkey and cat experiments indicate the following:

• Object position information is forwarded from the visual cortex to the posterior parietal cortex, and from there to the reticular formation of the pons.

• Velocity detectors are present in the upper part of the pons, apparently receiving information direct from the retina via the medial root of the optic tract.

• Head movement is signaled by the dynamic labyrinth, and is integrated with spatial and velocity information in the nucleus prepositus hypoglossi – a node of the reticular formation which is in fact closer to the abducens nucleus than to the hypoglossal nucleus. The nucleus prepositus projects to the PPRF, which controls conjugate eye movements. The pathway to the neck muscles (for turning the head) may involve the superior colliculus.

• Smooth execution of tracking movements is monitored by the flocculus of the cerebellum, which has two-way connections to the vestibular nucleus and pontine reticular formation.

The dynamic labyrinth and cerebellum cooperate to keep the eyes on target during movement of the head, as described in Chapter 19.

Core Information

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Ocular motor nerves

The Nerves

Oculomotor nerve

Trochlear nerve

Abducens nerve

Nerve Endings

Motor endings

Sensory endings

Pupillary Light Reflex (Figure 23.4)

Accommodation

The near response

Pathway for the accommodation reflex

The far response

Notes on the Sympathetic Pathway to the Eye

Ocular Palsies

Oculomotor nerve

Complete III nerve palsy

Partial III nerve palsy

Trochlear nerve

Abducens nerve

Internuclear ophthalmoplegia (Figure CP 23.1.2)

Ocular sympathetic supply

Control of Eye Movements

Scanning

Tracking

Oculomotor nerve

Trochlear nerve

Abducens nerve

Sympathetic

Parasympathetic

Reflex pathways

Oculomotor controls

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Ocular motor nerves

Pupillary Light Reflex (Figure 23.4)

Internuclear ophthalmoplegia (Figure CP 23.1.2)

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