occurs at the upper eyelid crease, located approximately 6–7 mm above the eyelid margin. The superior eyelid crease is formed by collateral insertion of the levator aponeurosis to the skin of the eyelid. Closure of the eyelids is marked by an increase in activity of the orbicularis muscle and inhibition of the levator palpebrae superioris muscle. The balance of tonic orbicularis and active levator activity determines the amount of eyelid opening. For discussion of eyelid abnormalities encountered in neuro-ophthalmic practice, see Chapter 11. For further discussion of eyelid anatomy, with illustrations, see BCSC Section 7, Orbit, Eyelids, and Lacrimal System.
Ocular Autonomic Pathways
Branches of the parasympathetic system play a role in lacrimal function, and pupil size is controlled by a balance between the innervation of the sympathetic fibers to the iris dilator muscles and of the parasympathetic fibers to the sphincter muscles. The accessory retractor muscles, including the Müller muscle in the upper eyelid, receive sympathetic innervation.
Sympathetic Pathways
Sympathetic activity originates in the posterolateral region of the hypothalamus. Activity in the hypothalamus is influenced by signals in the frontal, sensorimotor, and occipital cortex and in the limbic system (cingulate gyrus). The course of sympathetic fibers destined for the orbit is divided into first-, second-, and third-order segments (Fig 1-39). Axons destined for the dilator muscles of the pupil and Müller muscle descend as the first-order segment, along with other sympathetic fibers, superficially in the anteromedial column through the brainstem to the spinal cord. Within the cervical spinal cord, the sympathetic fibers continue in the intermediolateral column. From levels C8 to T2, the sympathetic fibers destined for the orbit synapse in the ciliospinal center of Budge-Waller.
Figure 1-39 Anatomy of the sympathetic pathway showing first-order central neuron, second-order intermediate neuron, and third-order neuron pathways. Note the proximity of the pulmonary apex to the sympathetic chain. Note also the intimate relationship of the sympathetic fibers to CN VI within the cavernous sinus. (Illustration b y Christine Gralapp.)
The postsynaptic second-order fibers leave the spinal cord through the ventral rami of the cervical (C8) and upper thoracic (T1 and T2) levels before joining the paravertebral sympathetic plexus. Ascending rostrally, the sympathetic chain passes in the anterior loop of the ansa subclavia proximate to the innominate artery on the right and the subclavian artery on the left just above the lung apex. These fibers pass through the inferior and middle cervical ganglia to terminate in the superior cervical ganglion, at the level of the angle of the jaw (C2) and the carotid artery bifurcation.
The postganglionic third-order fibers continue in the wall of the bifurcated carotid. Sympathetic fibers innervating the sweat glands of the lower face follow the ECA.
The sympathetic fibers destined for the pupil continue along the ICA to enter the cranium through the carotid canal. Some sympathetic fibers leave the carotid artery as it exits the petrous bone and, along with the greater superficial petrosal nerve, form the vidian nerve. These sympathetic fibers parallel the parasympathetic fibers to the lacrimal gland. Within the cavernous sinus, sympathetic fibers destined for the dilator muscles leave the carotid in conjunction with CN VI for a few millimeters. Further anteriorly in the cavernous sinus, the sympathetic fibers join the nasociliary branch of V1. In the orbital apex, the fibers then pass through the ciliary ganglion (without synapsing). Along with the nasociliary branch, the sympathetic fibers reach the globe and travel with the long ciliary nerves to the dilator muscles of the pupil. The dilator muscle lies just superficial to the posterior pigment epithelium of the iris, which continues peripherally as the nonpigmented superficial layer of the ciliary body. The myoepithelial cells measure approximately 12.5 μm in thickness, with an apical epithelial portion and a basilar muscular portion that is oriented radially toward the pupillary opening. The muscular processes terminate peripheral to the sphincter muscle. Peripherally at the iris root, these cells are continuous with the pigmented epithelium of the ciliary body.
The fibers destined for the Müller muscle travel along the OphA and its subsequent frontal and lacrimal branches. The Müller muscle originates near the origin of the levator aponeurosis and inserts 10–12 mm inferiorly on the superior border of the tarsus. The superior orbital sympathetic fibers also innervate the sweat glands of the forehead. Thus, disruption of these sympathetic fibers is responsible for the mild ptosis and the frontal anhidrosis associated with distal Horner syndrome.
Parasympathetic Pathways
Parasympathetic activity originates in various areas within the brainstem. The fibers that control the pupil sphincter muscles originate in the Edinger-Westphal (EW) nuclei of the CN III nuclear complex within the midbrain. The main input to the EW nuclei is from the pretectal nuclei, both directly and via the posterior commissure. The pretectal nuclei, in turn, receive input directly from the afferent visual pathways via the pupillary tract, which leaves the optic tract in the brachium of the superior colliculus just anterior to the LGN (Fig 1-40). The cortex (especially the frontal lobes), the hypothalamus, and the reticular activating system provide tonic inhibitory signals to the EW nucleus. During sleep, the pupil becomes smaller through loss of this inhibitory activity. In addition, the EW nucleus receives inputs from the more ventral and rostral midbrain, probably representing input
related to bitemporal image disparity and serving as a stimulus for convergence and the near reflex.
Figure 1-40 Pathway of the pupillary reaction to light. (Illustration b y Christine Gralapp.)
The parasympathetic fibers and the CN III fascicles leave the CN III nucleus and exit in the interpeduncular fossa. Within the subarachnoid space, the parasympathetic fibers tend to run on the medial superficial surface of CN III. When CN III bifurcates in the anterior cavernous sinus, the parasympathetic fibers travel with the inferior division. In the orbital apex, these fibers synapse in the ciliary ganglion (as opposed to the oculosympathetic and nasociliary fibers, which travel through the ganglion without synapse). The postsynaptic fibers then travel with the branch destined for the inferior oblique muscle to join the posterior ciliary nerves to reach the anterior segment and the iris sphincter muscles. The sphincter muscle measures approximately 0.8 mm in diameter and 0.15 mm in thickness. It travels circumferentially around the pupillary margin just anterior to the posterior
pigmented epithelium and central to the termination of the dilator muscle cells. The muscle itself is made up of units composed of groups of 5–8 muscle cells.
Parasympathetic innervation to the lacrimal gland originates in the superior salivatory (salivary) nucleus located in the caudal pons posterolateral to the motor nucleus of CN VII. This nucleus receives sensory input from the trigeminal nerve and additional afferent fibers from the hypothalamus. Efferent parasympathetic fibers for lacrimal, mucous, and salivary secretion leaving the nucleus join other parasympathetic efferent fibers coming from the salivatory nucleus and run with afferent gustatory fibers from the anterior two-thirds of the tongue in the nervus intermedius. The gustatory fibers synapse in the nucleus of the tractus solitarius parallel to the fascicles of CN VII in the nervus intermedius (Fig 1-38B). This nerve joins with CN VII to exit the brainstem on its ventral surface of the pontomedullary junction. With the other fascicles of CN VII, the parasympathetic fibers of the nervus intermedius run laterally to the internal auditory meatus. Within the petrous bone and fallopian canal, the parasympathetic fibers exit at the geniculate ganglion and then travel superficially over the petrous bone with the greater superficial petrosal nerve. This course parallels that of the ICA. In the area where the ICA turns to rise into the cavernous sinus, the fibers join the vidian nerve. It then travels through the sphenoid bone parallel to and beneath the foramen rotundum to enter the pterygomaxillary space. The fibers synapse in the sphenopalatine ganglion. The postganglionic fibers travel superiorly through the inferior orbital fissure and then with the lacrimal nerve to reach the lacrimal gland. The parasympathetic fibers are responsible for reflex tearing.
Loewenfeld IE. The Pupil: Anatomy, Physiology, and Clinical Applications. 2nd ed. New York: Butterworth-Heinemann; 1999.