Chapter Summary
Notes on the sympathetic pathway to the eye
Study guidelines
General
Because of the immense diagnostic and therapeutic importance of ocular innervation, and because of its inherent complexity, neuroophthalmology has become a branch of medicine in its own right.
It is especially important to describe the way in which premotor centres are able to operate bilaterally to keep the gaze on target, even when the head is moving.
Particular
- 1.
Describe the action of the III, IV, and VI nerves on the movement of the eye; identify which extraocular muscles work together to keep both eyes in their cardinal position of gaze.
- 2.
Indicate the nerve supply to the six muscles that move the eyeball and describe how the III nerve elevates the upper eyelid.
- 3.
Contrast the effects of the sympathetic and parasympathetic autonomic supply to the eye; explain the changes and anatomic pathways that are responsible for the pupillary changes noted in a dark room, in a well lit room, and when focusing on an object held close to one’s nose.
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.
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 that 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 periaqueductal grey matter ( Figure 23.2A ). It is composed of five individual subnuclei for the supply of striated muscles (ipsilateral subnuclei innervate the inferior rectus, inferior oblique, and medial rectus, but 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, 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 fibres 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 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 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 dorsum of the brainstem and the only nerve to fully decussate.
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.
Abducens 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 fibres apiece (compared with 1000 or more in the tibialis anterior). These motor units can be divided into three groups, but two groups are most relevant: motor neurons that form single ‘en plaque’ endings and innervate muscle fibres that respond by generating a fast twitch and those that form multiple small ‘en grappe’ endings along the length of nontwitch muscle fibres that respond by a slow tonic contraction. The twitch muscle fibres are likely involved with saccadic or rapid eye movements, while the role of the nontwitch fibres is gaze holding (e.g. fixation, smooth pursuit).
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 nontwitch muscle fibres, but then turn back towards either distal muscle zone forming a spiral of nerve endings (assuming a fencepost or palisade appearance) around their tips. This unique nerve ending type, the palisade ending , is believed to provide proprioceptive information by assessing muscle tension; the cell bodies of these nerves lie around the periphery of the cranial motor nuclei. (The motor neuron cell bodies that provide the innervation of these nontwitch muscle fibres [en grappe] are most likely in a similar peripheral location around the nuclei. If these motor neurons function in the same role as γ motor neurons, then they would function with the palisade ending neurons in a similar manner to a muscle spindle and would 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. This nucleus 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.
Pupillary light reflex ( Figure 23.4 )
Constriction of the pupils in response to light optimises visual acuity and protects the retina from overexposure to bright light. It involves four sets of neurons:
- 1.
The afferent limb commences in melanopsin-containing retinal ganglion cells, with inputs from photoreceptors (rods and cones), and travels within the optic nerve.
- 2.
Fibres leaving the chiasm enter both optic tracts and terminate in the pretectal nuclei , situated just rostral to the superior colliculus on each side ( Figure 17.19 ).
- 3.
Each pretectal nucleus is linked by interneurons to both Edinger–Westphal (parasympathetic) nuclei; the contralateral nucleus is reached by way of the posterior commissure (PC) .
- 4.
Preganglionic parasympathetic fibres enter the oculomotor nerve, leave the branch to the inferior oblique, and synapse in the ciliary ganglion.
- 5.
Postganglionic fibres run in the short ciliary nerves and enter the iris to supply the sphincter (constrictor) pupillae. The normal response is consensual; that is, both pupils constrict when the light is applied to one eye only.
Accommodation
The near response
When the eyes view an object close up, the ciliary muscle contracts by reflex, thereby relaxing the suspensory ligament of the lens ( Figure 23.5 ). Because the lens at rest is somewhat flattened or stretched by tension exerted on the lens capsule by the suspensory ligaments, 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. This response of the lens is termed accommodation .
