Ocular Motor Nerves

Oculomotor Nerve

The nucleus of the third nerve is at the level of the superior colliculus of the midbrain. It is partly embedded in the periaqueductal grey matter ( Fig. 23.2A ). It is composed of five individual subnuclei, which supply striated muscles (ipsilateral subnuclei innervate the inferior rectus, inferior oblique, and medial rectus, and the contralateral superior rectus muscle; the levator palpebrae superioris is innervated by a single midline nucleus) and one parasympathetic nucleus.

The nerve passes through the tegmentum of the midbrain and emerges into the interpeduncular fossa. It crosses the apex of the petrous temporal bone, pierces the dural roof of the cavernous sinus ( Fig. 23.3 ), runs in the lateral wall of the sinus, and divides into an upper and a lower division 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 fibres originate in the Edinger–Westphal nucleus . They accompany the main nerve into the orbit and then leave the branch to the inferior oblique to synapse in the ciliary ganglion . Postganglionic fibres emerge from the ganglion in the short ciliary nerves , which pierce the lamina cribrosa (‘sieve-like layer’) of the sclera and supply the ciliary and sphincter (constrictor) pupillae muscles.

Trochlear Nerve

The nucleus of the fourth nerve is at the level of the inferior colliculus of the midbrain. The nerve itself is unique in two respects ( Fig. 23.2B ): it is the only nerve to emerge from the dorsum of the brainstem and the only nerve to fully decussate.

The CN IV winds around the crus of the midbrain and travels in the wall of the cavernous sinus accompanied by CN III ( Fig. 23.3 ). It passes through the superior orbital fissure and supplies the superior oblique muscle.

Abducens Nerve

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

Motor Endings

All the ocular motor units are small, containing 5 to 10 muscle fibres (compared with 1000 or more in the tibialis anterior muscle). These motor units can be divided into three groups, of which two are most relevant: motor neurons that form single ‘en plaque’ endings that innervate muscle fibres and respond with a fast twitch and those that form multiple small ‘en grappe’ endings on muscle fibres that respond with a slow tonic contraction. The fast twitch muscle fibres are likely involved with saccadic or rapid eye movements, while the slow twitch fibres are involved in gaze holding (e.g. fixation, smooth pursuit). As extraocular muscles execute multiple functions it is likely to occur through unique groupings of motor units that allow independent activation to produce a repertoire of actions.

Sensory Endings

Neuromuscular spindles and Golgi tendon organs are not prominent in the extraocular muscles of humans. However, other assumed sensory axons approach the central portion of slow twitch muscle fibres, but then turn back towards the distal muscle zone forming a spiral of nerve endings around their tips. This unique nerve ending type, the palisade ending , is believed to provide such proprioceptive information and contribute to the monitoring of eye position.

The cell bodies of these palisade ending nerves and the cell bodies of the motor neurons that innervate the slow twitch muscle fibres are most likely found around the periphery of the cranial motor nuclei. If these motor neurons function in the same role as γ motor neurons, then the palisade ending neurons would function in a similar manner to a muscle spindle and provide proprioceptive information rather than contribute to eye movement.

There are other sensory afferents from extraocular muscles (some may provide proprioceptive information, others nociception or vasodilatation), which travel through the ophthalmic nerve to the trigeminal ganglion. The trigeminal ganglion also receives proprioceptive terminals from the neck muscles and 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.