External ophthalmoplegia is present when the motility of the globe is restricted but the autonomic (parasympathetic) innervation of the eye is preserved. Oculomotor nerve palsies account for about 30% of all palsies affecting the muscles of eye movement (abducens nerve palsies are more common, accounting for 40-50% of cases). Ptosis is more common with lesions of the (peripheral) nerve itself, rarer with lesions of its nuclear complex within the brainstem. Once the nerve emerges from the brainstem, the pupillomotor fibers lie in the outer portion of the nerve, directly beneath the epineurium, and are thus more vulnerable than the other fibers of the nerve to compression by trauma, tumors, or aneurysms. For the same reason, the pupillomotor fibers are less commonly damaged by vascular lesions, such as those caused by diabetes. The more common causes of isolated oculomotor nerve palsy are aneurysms (approx. 30%), tumors (approx. 15%), and vascular lesions (including diabetes, approx. 15-20%).
Trochlear Nerve Palsy
Trochlear nerve palsy paralyzes the superior oblique muscle. The affected eye deviates upward and slightly inward, i.e., medially, toward the side of the normal eye (Fig. 4.19). The deviation is most evident, and the diplopia most extreme, when the patient looks downward and inward. Another way of bringing out the upward-and-inward deviation of the affected eye and the resulting diplopia is by having the patient tilt the head to the affected side while fixating on an object with the normal eye (Bielschowsky test). The more common causes of trochlear nerve palsy are trauma (30-60% of cases), vascular lesions, and tumors.
The affected eye is deviated inward on primary (straight-ahead) gaze and cannot be abducted, because the lateral rectus muscle is paralyzed. The inward squint is also referred to as convergent strabismus. When looking toward the nose, the paretic eye rotates upward and inward because of the predominant action of the inferior oblique muscle. Abducens palsy is usually an isolated finding and is most commonly caused by tumors or vascular lesions. Among all of the cranial nerves, the abducens nerve has the longest course within the subarachnoid space; thus, abducens palsies can be caused by meningitis and by subarachnoid hemorrhage, as well as by elevated intracranial pressure (intracranial hypertension). Unilateral abducens palsy may accompany generalized intracranial hypertension and is not necessarily a lateralizing sign. Abducens palsy is also occasionally produced by the temporary disturbance of intracranial pressure after a lumbar puncture.
Conjugate Eye Movements
Positioning and stabilizing the image of an object exactly on the fovea of both eyes at the same time requires precisely coordinated activity of the eye muscles. The agonist and antagonist muscles of the two eyes are always simultaneously innervated (Hering’s law), and each contraction of an agonist occurs in conjunction with relaxation of the corresponding antagonist (Sherrington’s law). Conjugate movements of both eyes in thesamedirection are called versive movements (from the Latin for “turning”), while movements of the two eyes in opposite directions are vergence movements (either convergence or divergence). Movements of a single eye are called either duction or torsion (rotatory movement).
Horizontal and Vertical Gaze
Conjugate horizontal gaze.The central relay nucleus of the oculomotor system is found in the paramedian pontine reticular formation (PPRF or “pontine gaze center”), which lies adjacent to the nucleus of the abducens nerve. The PPRF is the site of origin of all of the neural connections participating in conjugate horizontal gaze, in particular the fibers that connect the ipsilateral abducens nucleus to the portion of the contralateral oculomotor nucleus innervating the medial rectus muscle. These fibers run in the medial longitudinal fasciculus (MLF), a white-matter tract that ascends and descends the brainstem on both sides near the midline. The MLF, which extends from the midbrain all the way to the cervical spinal cord, serves to interconnect all of the individual nuclei innervating the eye muscles (Fig. 4.21). It also conveys impulses to and from the cervical spinal cord (anterior and posterior cervical musculature), the vestibular nuclei, the basal ganglia, and the cerebral cortex.
Disturbances of conjugate horizontal gaze.If the medial longitudinal fasciculus is damaged on the left side (for example), then the patient’s left medial rectus muscle is no longer activated on attempted conjugate gaze to the right, and the left eye stays behind, i.e., it comes no further medially than the midline. At the same time, monocular nystagmus is seen in the right eye, whose movement to the right (abduction) is subserved by the right abducens nerve. This combination of findings is called internuclear ophthalmoplegia
(INO, Fig. 4.22). It is important to realize that INO involves neither a nuclear nor a peripheral palsy of the nerves to the eye muscles: in the patient just described, the left medial rectus muscle will contract normally on convergence of the two eyes. As mentioned, the MLF lies near the midline; the two medial longitudinal fasciculi in fact lie very near each other, and damage to them is usually bilateral. The above findings of internuclear ophthalmoplegia are thus usually seen on attempted gaze in either direction: the adducting eye comes no further medially than the midline, while the abducting (leading) eye manifests nystagmus. All other eye movements are intact, and the pupillary reflexes are intact. Multiple sclerosis is the most common cause of internuclear ophthalmoplegia. Others include encephalitis and (in older patients) vascular disturbances.
Conjugate vertical gaze.The vertical gaze center lies in the rostrodorsal portion of the midbrain reticular formation (Fig. 4.21) and consists of a number of specialized nuclei: the prestitial nucleus in the rear wall of the third ventricle for upward gaze; the nucleus of the posterior commissure for downward gaze; and the interstitial nucleus of Cajal and the nucleus of Darkschewitsch for conjugate rotatory movements.
Other conjugate gaze centers.Vertical gaze movements can also be generated from neurons lying at the anterior border of the superior colliculi. Disturbances affecting this area cause paresis of upward gaze (Parinaud syndrome). Impulses originating in the occipital lobes also travel to the contralateral pontine gaze centers (para-abducens nucleus) to initiate conjugate lateral gaze movements. Experimental stimulation of occipital areas 18 and 19 has been found to provoke conjugate gaze movements that are most often lateral, though sometimes upward or downward (lateral gaze movements are certainly the most important type in human beings, as they are far more frequent than the other two types) (Fig. 4.21). Voluntary eye movements are initiated by neurons of the frontal eye field in Brodmann area 8 (and perhaps also parts of areas 6 and 9), anterior to the precentral gyrus (Fig. 4.21). The most common result of stimulation or irritation in this area, e. g., during an epileptic seizure, is a conjugate lateral gaze movement to the opposite side (Fig. 4.24).
This eye movement is occasionally accompanied by turning of the head to the opposite side. The pathway from the frontal eye field to the brainstem nuclei subserving eye movements has not yet been fully traced. It is currently thought that fibers of this pathway run in the internal capsule and the cerebral peduncle together with the corticonuclear tract, but then do not terminate directly in the nuclei subserving eye movement, reaching them instead through a number of “way stations” including the superior colliculi, interneurons of the reticular formation, and the medial longitudinal fasciculus (Fig. 4.21). All voluntary movements are under the influence of reflex arcs, not only visual, but also auditory, vestibular, and proprioceptive (from the cervical and nuchal musculature to the spinotectal tract and medial longitudinal fasciculus).
Lesions of the gaze centers. Destruction of area 8on one side results in a preponderance of impulses coming from the corresponding area of the opposite hemisphere, producing conjugate gaze toward the side of the lesion (i.e., dйviation conjuguйe looking toward the focus). The gaze deviation is occasionally accompanied by turning of the head to the side of the lesion. The patient cannot voluntarily look to the other side, but can do so in reflex fashion, as when visually pursuing an object that is slowly moved into the contralateral visual field. (The opposite is found in lesions of the occipital lobe, as discussed below.) Gaze deviation due to a lesion of the frontal eye field generally resolves after a brief period. In contrast to a destructive lesion, stimulation or irritation of area 8 (as in an epileptic seizure) produces conjugate gaze away from the side of the focus. The situation is different with pontine lesions because the corticopontine pathways are crossed (Fig. 4.24). Stimulation or irritation of the pontine gaze center produces ipsilateral gaze deviation, while a destructive lesion causes contralateral gaze deviation. Gaze deviation of pontine origin rarely resolves completely.
Convergence and Accommodation
These reflexes are evoked by watching an object as it moves closer to the observer in the visual field. The so-called near response actually consists of three processes that occur simultaneously:
Convergence: the medial rectus muscles of the two eyes are activated so that the optical axis of each continues to point directly to the object under observation. This keeps the image of the object on the fovea of each eye.
Accommodation: contraction of the ciliary muscle slackens the suspending apparatus of the lens. Because it is intrinsically elastic, the lens then takes on a more spherical shape, and thus a higher refractive power. This process keeps the retinal image of an object in focus as it is moved closer to the eye. Conversely, when the object is moved farther away or the individual’s gaze is redirected onto a more distant point, relaxation of the ciliary muscle allows the suspending apparatus to pull the lens back into a flatter shape, lowering its refractive power and once again bringing the visual image into sharp focus (Fig. 4.25).
Pupillary constriction: the pupil constricts to keep the retinal image of the near object as sharp as possible. (A camera shutter functions similarly: the closer the object to be photographed, the narrower the aperture must be to keep it in focus.)
All three of these processes can be brought about voluntarily by fixating on a near object and also occur as reflexes when a distant object moves closer to the observer.
Anatomical substrate of convergence and accommodation(Fig. 4.25). The afferent impulses travel from the retina to the visual cortex, and the efferent impulses from the visual cortex to the pretectal area and then to the parasympathetic nucleus of Perlia, which lies medial and ventral to the Edinger-Westphal nucleus (accessory autonomic nucleus). From the nucleus of Perlia on either side, impulses travel to the nuclear area of the medial rectus muscle (for ocular convergence) and to the EdingerWestphal nucleus, from which they proceed to the ciliary ganglion and muscle (for accommodation) and to the papillary sphincter (for pupilloconstriction) (Fig. 4.26 on page 8). The neural pathways to the ciliary muscle and the pupillary sphincter are presumably distinct, because the accommodation and light reflexes can be differentially affected in various conditions. In neurosyphilis, for example, one can find the phenomenon of the Argyll Robertson pupil: the light reflex is absent, but convergence and accommodation are preserved.
Regulation of the Pupillary Light Reflex
The width of the pupil varies in relation to the incident light: bright light induces pupillary constriction, and darkness induces pupillary dilation. The pupillary light reflex serves to modulate the amount of light falling on the retina, both to protect the photoreceptors from potentially damaging, excessive illumination, and to keep the visual images of objects in the best possible focus on the retina, in analogous fashion to a camera shutter. This reflex is entirely involuntary; the cerebral cortex is not involved in the reflex loop.
Afferent arm of the pupillary light reflex(Fig. 4.26 see p.8). The afferent fibers accompany the visual fibers in the optic nerve and tract nearly to the lateral geniculate body, but, instead of entering the latter, they turn off in the direction of the superior colliculi and terminate in the nuclei of the pretectal area. Interneurons located here project further to the parasympathetic EdingerWestphal nuclei (accessory autonomic nuclei) on both sides (Fig. 4.26). This bilateral innervation of the Edinger-Westphal nuclei is the anatomical basis of the consensual light response: illumination of one eye induces constriction not just of that pupil, but of the contralateral pupil as well.
Lesions of the afferent pathway. Lesions of the optic radiation, visual cortex, or superior colliculi have no effect on the pupillary light reflex. A lesion of the pretectal area, however, abolishes the reflex. This indicates that the former structures do not participate in the reflex arc, and that the afferent arm of the reflex arc must traverse the pretectal area, though the precise anatomical localization of this pathway is not yet fully clear. Similarly, optic nerve lesions, which interrupt the afferent arm of the reflex arc at a different site, impair the pupillary response to illumination of the eye on the side of the lesion: neither the ipsilateral nor the contralateral pupil will constrict normally. Illumination of the other eye is followed by normal constriction of both pupils. These findings imply the presence of an afferent pupillary defect.