Chapter 14 Autonomic Innervation of Ocular Structures
Autonomic Pathway
Ocular structures supplied by the sympathetic system are the iris dilator, ciliary muscle, smooth muscle of the lids, lacrimal gland, and choroidal and conjunctival blood vessels.1–5 Ocular structures supplied by the parasympathetic system are the iris sphincter, ciliary muscle, lacrimal gland, and blood vessels.
Sympathetic Pathway to Ocular Structures
Sympathetic fibers are controlled by the hypothalamus through a pathway that terminates in the lateral column of the cervical spinal cord. The fiber from the preganglionic neuron leaves the spinal cord in one of the first three thoracic nerves via the ventral root and enters the sympathetic ganglion chain located adjacent to the vertebrae (Figure 14-1). These preganglionic fibers then ascend in the sympathetic chain to a synapse in the superior cervical ganglion, located near the second and third vertebrae.6,7
FIGURE 14-1 Sympathetic innervation to iris dilator, Müller muscle, blood vessels, and lacrimal gland.
Some of these sympathetic fibers travel with the ophthalmic division of the trigeminal nerve from the cavernous sinus into the orbit.8 Once in the orbit the sympathetic fibers follow the nasociliary nerve and then travel with the long ciliary nerves to innervate the iris dilator and the ciliary muscle8–12 (see Figure 14-1).
Other fibers from the carotid plexus follow this same route to the nasociliary nerve and then branch to the ciliary ganglion as the sympathetic root; these fibers pass through the ganglion without synapsing. They enter the globe as the short ciliary nerves to innervate the choroidal blood vessels. Alternately, the sympathetic root to the ciliary ganglion may emanate directly from the internal carotid plexus.12,13 A sympathetic nerve network accompanies the ophthalmic artery and its branches could have a role in the control of blood flow to ocular structures.14 The pathway to the conjunctival vasculature may be through either the long or the short ciliary nerves.
Other fibers from the carotid plexus join the oculomotor nerve and travel with it into the orbit to innervate the smooth muscle of the upper eyelid. These fibers follow the same path as the superior division of the oculomotor nerve as it supplies the levator muscle8 (see Figure 14-1). An alternate route to Müller’s muscle from the infratrochlear or lacrimal nerve has been suggested.14
Sympathetic stimulation activates the iris dilator, causing pupillary dilation and thereby increasing retinal illumination. It also causes vasoconstriction of the choroidal and conjunctival vessels and widening of the palpebral fissure by stimulating the smooth muscle of the eyelids. The sympathetic nerves also exhibit a small inhibitory effect on the ciliary muscle.1–3,5,15–18
Parasympathetic Pathway to Ocular Structures
The preganglionic neuron in the parasympathetic pathway to the intrinsic ocular muscles is located in the midbrain in the parasympathetic accessory third-nerve nucleus, also called the Edinger-Westphal nucleus. The preganglionic fibers leave the nucleus with the motor fibers of the oculomotor nerve and follow the inferior division of that nerve into the orbit.19 The parasympathetic fibers leave the inferior division and enter the ciliary ganglion as the parasympathetic root13,20–22 (Figure 14-2).
The ciliary ganglion is a small, somewhat flat structure, 2 mm long and 1 mm high, located within the muscle cone between the lateral rectus muscle and the optic nerve, approximately 1 cm anterior to the optic canal.9,13,23 Three roots are located at the posterior edge of the ganglion: the parasympathetic root, mentioned previously; the sensory root, which carries sensory fibers from the globe and joins with the nasociliary nerve; and the sympathetic root, which supplies the blood vessels. Only the parasympathetic fibers synapse in the ciliary ganglion; the sensory and sympathetic fibers pass through without synapsing (see Figure 14-2).
The short ciliary nerves, located at the anterior edge of the ciliary ganglion, carry sensory, sympathetic, and parasympathetic fibers. The postganglionic parasympathetic fibers, which are myelinated,20 exit the ganglion in the short ciliary nerves, enter the globe, and travel to the anterior segment of the eye to innervate the sphincter and ciliary muscles. Most of the fibers innervate the ciliary body; only approximately 3% supply the iris sphincter.20,21 The two groups of neurons likely share some characteristics and differ in others, but specifics have not been identified.24
Clinical Comment: Inhibition of Ciliary Muscle
Parasympathetic activation causes contraction of the ciliary muscle in accommodation. Many investigators, using pharmacologic,25,26 electrophysiologic,27 and anatomic20,28,29 evidence, have demonstrated the presence of both sympathetic receptors and fibers in animals and humans.30,31 The sympathetic effect on the ciliary muscle appears to be a small, slow inhibition that is a function of the level of parasympathetic activity.1–5
Autonomic Innervation to Lacrimal Gland
The efferent autonomic pathway to the lacrimal gland follows a complex route. Fibers controlling the parasympathetic innervation originate in the pons in an area within the nucleus for cranial nerve VII designated as the lacrimal nucleus. These preganglionic fibers exit the pons with the motor fibers of the facial nerve, enter the internal auditory canal, and pass through the geniculate ganglion of the facial nerve without synapsing. They leave the ganglion as the greater petrosal nerve, which exits the petrous portion of the temporal bone.32 The greater petrosal nerve is joined by the deep petrosal nerve, composed of sympathetic postganglionic fibers from the carotid plexus. The greater petrosal and the deep petrosal nerves together form the vidian nerve (nerve of the pterygoid canal) (see Figures 14-1 and 14-2).
The vidian nerve enters the pterygopalatine ganglion, where the parasympathetic fibers synapse. The pterygopalatine ganglion (also called the sphenopalatine ganglion) lies in the upper portion of the pterygopalatine fossa (see Figure 12-5). It is a parasympathetic ganglion because it contains parasympathetic cell bodies and synapses; sympathetic fibers pass through without synapsing.
The autonomic fibers (all of which are now postganglionic) leave the ganglion, join with the maxillary branch of the trigeminal nerve, pass into the zygomatic nerve, and then form a communicating branch to the lacrimal nerve (see Figures 14-1 and 14-2). An alternate pathway bypasses the zygomatic nerve and travels from the ganglion directly to the gland.33 The parasympathetic fibers that innervate the lacrimal gland are of the secretomotor type and thus cause increased secretion. The sympathetic fibers innervate the blood vessels of the gland and might indirectly cause decreased production of lacrimal gland secretion by restricting blood flow.14 Parasympathetic stimulation causes increased lacrimation. Figure 14-3 provides a flow chart of the common autonomic nerve pathways to orbital structures. Sympathetic fibers from the zygomatic nerve also branch into the lower eyelid to innervate Müller’s muscle of the lower lid.34
FIGURE 14-3 Flow chart of autonomic nervous system. A, Sympathetic innervation. B, Parasympathetic innervation.
Parasympathetic innervation to the choroidal blood vessels is believed to emanate directly from the sphenopalatine ganglion through a network of fine nerves, the rami oculares.35 Parasympathetic activation presumably causes vasodilation, which might raise intraocular pressure.33,36
Irritation of any branch of the trigeminal nerve activates a reflex afferent pathway, precipitating increased lacrimation.7,37
Clinical Comment: Corneal Reflex
Corneal touch initiates the three-part corneal reflex: lacrimation, miosis, and a protective blink (Figure 14-4). The pain sensation elicited by the touch travels to the trigeminal ganglion and then into the pons as the trigeminal nerve. Communication from the trigeminal nucleus to the Edinger-Westphal nucleus causes activation of the sphincter muscle. Communication to the facial nerve nucleus activates the motor pathway to the orbicularis muscle, causing the blink, and communication to the lacrimal nucleus and the parasympathetic pathway to the lacrimal gland stimulates increased lacrimation.
Pharmacologic Responses of Intrinsic Muscles
Neurotransmitters
When an action potential reaches the terminal end of an axon, a neurotransmitter is released that activates either the next fiber in the pathway or the target structure, the effector. In the sympathetic pathway the neurotransmitter released by the preganglionic fiber is acetylcholine, and the neurotransmitter released by the postganglionic fiber is norepinephrine. In the parasympathetic system both preganglionic and postganglionic fibers secrete acetylcholine (Figure 14-5). Fibers that release acetylcholine are called cholinergic, and fibers that release norepinephrine are called adrenergic.
FIGURE 14-5 Autonomic neurotransmitters at their sites of action. CNS, Central nervous system.
(From Bartlett JD, Jaanus SD: Clinical ocular pharmacology, ed 2, Boston, 1989, Butterworth-Heinemann.)
Drugs: Agonists and Antagonists
Ophthalmic Agonist Agents
Epinephrine and phenylephrine are direct-acting adrenergic agonists that bind to sites on the dilator muscle, causing contraction38 (Figure 14-6). Hydroxyamphetamine and cocaine are indirect-acting adrenergic agonists. Hydroxyamphetamine causes the release of norepinephrine from the nerve ending, thus indirectly initiating muscle contraction. Cocaine prevents the reuptake of norepinephrine by the nerve ending; thus norepinephrine remains at the neuromuscular junction and can continue to activate the dilator.38
Pilocarpine is a direct-acting cholinergic agonist that directly stimulates the sites on the iris sphincter and ciliary muscle, causing contraction38 (Figure 14-7). Physostigmine is an indirect-acting cholinergic agonist that inhibits acetylcholinesterase.38 Therefore, acetylcholine is not broken down but remains in the junction, and the sphincter and ciliary muscle contraction continues in a spasm.
