Ординатура / Офтальмология / Английские материалы / Neuro-Ophthalmology_Kidd, Newman, Biousse_2008

lower bank of the calcarine cortex, for example, produce contralateral congruous superior visual field defects, respecting both the horizontal and vertical meridians (Fig. 1-4, visual fields #7 and #8).

Bilateral occipital lobe lesions may produce cortical blindness. Such patients may deny that they are blind and may confabulate or “make-up” descriptions of what they see (Anton’s syndrome). Bilateral macular-sparing homonymous hemianopsias may cause a clinical picture of apparent “constriction” of the visual fields. This may be misinterpreted as functional, or nonphysiologic, visual loss because the pupillary responses in such patients are normal. Careful documentation of a vertical “step-off,” or a difference in size of the areas of macular sparing between the two eyes, should lead the examiner to suspect a bilateral occipital lobe process.

Retrochiasmal visual field defects are often accompanied by other neurologic signs and symptoms, such as hemiparesis, hemisensory disturbance, aphasia, or neglect. Lesions involving the occipito-temporal area may produce palinopsia (persistent perception of an image after gaze has been shifted away from it). Patients may also perceive motion without being able to see details in the affected hemifield (Riddoch’s phenomenon). Complex visual hallucinations may also occur in the blind hemifield, either as release phenomena or as manifestations of partial seizure activity.

The Ocular Motor System

Disorders of the ocular motor system may occur secondarily to lesions in any of several locations, from the orbit to the cavernous sinus, subarachnoid space, brainstem, and involving supranuclear or vestibulo-ocular pathways. This section emphasizes the anatomic features that are important to the recognition and localization of eye movement disorders.

ANATOMY OF THE ORBIT AND EXTRAOCULAR MUSCLES

There are six muscles that are responsible for eye movements; these are arranged about the eye as shown in Figure 1–6.10 The superior and inferior rectus muscles elevate and depress the eye, respectively, performing these functions best when the eye is abducted. The superior and inferior oblique muscles, however, work using a sling/pulley mechanism, with insertions of the muscles being located toward the posterior portion of the globe. The oblique muscles serve as rotators of the eye about the vertical axis as the eye is viewed (clockwise or counterclockwise torsion) but also serve to elevate or depress the eye in adduction. The superior oblique primarily intorts the eye (rotates the superior aspect of the globe toward the nasal bridge about the vertical axis, clockwise in the case of the right eye as viewed by the examiner); this muscle also depresses the eye in adduction. The inferior oblique, in contrast, extorts the eye but also serves as an elevator in adduction. In the primary position of gaze, the superior and inferior oblique and rectus muscles all perform a combination of vertical and torsional actions. Adduction is performed by the medial rectus, whereas abduction is subserved by the lateral rectus muscle.

The superior rectus, inferior rectus, inferior oblique, and medial rectus are innervated by the third cranial nerve (oculomotor nerve), whereas the superior

Pons

Inferior oblique

Trigeminal

ganglion

Figure 1–6 Innervation of the muscles of the globe. The oculomotor (III), trochlear (IV), and abducens (VI) nerves enter the orbit through the orbital fissure. The trochlear nerve supplies the superior oblique, the abducens nerve supplies the lateral rectus, and the oculomotor nerve supplies the remaining five muscles. (From Moore KL: Clinically Oriented Anatomy, 4th ed. Baltimore, Lippincott and Wilkins, 1999, p 911.)

oblique and lateral rectus are supplied by the fourth (trochlear) and sixth (abducens) nerves, respectively (Fig. 1–6). The tendon origins of the four rectus muscles form the annulus of Zinn, a sheath through which the optic nerve, third nerve, and sixth nerve pass at the orbital apex.

ANATOMIC CONSIDERATIONS OF THE THIRD, FOURTH, AND SIXTH CRANIAL NERVES

Third Nerve

Originating in the dorsal midbrain as a cluster of subnuclei, the third nerve (oculomotor nerve) innervates the superior rectus, inferior rectus, inferior oblique, and medial rectus muscles. The pupillary sphincter and levator palpebrae (major eyelid elevator muscle) are also supplied by the third nerve. After traversing ventrally through the midbrain as the third nerve fascicle, the nerve itself exits the midbrain near the medial aspect of the cerebral peduncle. The nerve then enters the subarachnoid space (Fig. 1–6), where it travels medial to the posterior communicating artery and enters the cavernous sinus. Within the cavernous sinus, the third nerve travels within the lateral wall, superior to the fourth nerve (Fig. 1–7).11 Entering the orbit (Fig. 1–6), the nerve passes through the annulus of Zinn and then divides into a superior division (innervates levator, superior rectus) and inferior division (innervates pupillary sphincter, medial

Figure 1–8 Photographs of a patient with partial, pupil-involving right third nerve palsy. (From Balcer LJ, Galetta SL, Bagley LJ, et al: Localization of traumatic oculomotor nerve palsy to the midbrain exit site by magnetic resonance imaging. Am J Ophthalmol 1996;122:437.)

third nerve palsies may occur in the absence of pupillary dilation (pupil-sparing third nerve palsy), especially in older patients with diabetes or hypertension. Galetta and colleagues have presented a discussion of the recommendations for neuroimaging in adult patients with acute, isolated third nerve palsies.13,14 Table 1–1 summarizes their recommendations for evaluation based on the presence or absence of pupillary involvement and the complete versus incomplete extent of the ophthalmoparesis.

In addition to compression by aneurysms, the third nerve within the subarachnoid space is also vulnerable to compression by uncal herniation because of supratentorial space-occupying lesions or edema. Such patients usually have altered mental status and may also have hemiparesis or other neurologic signs. At the level of the anterior cavernous sinus or superior orbital fissure, the third nerve divides into a superior and inferior division. Superior-division third nerve palsies, affecting the levator palpebrae and superior rectus only, may thus occur secondary to lesions within the cavernous sinus, orbital apex, or superior orbital fissure. Although there is an anatomic separation of the third nerve at the level

CT, computed tomography; MRI, magnetic resonance imaging.

From Galetta SL, Liu GT, Volpe NJ: Diagnostic tests in neuro-ophthalmology. Neurol Clin 1996;14:201. Modified from Trobe JD: Third nerve palsy and the pupil. Footnotes to the rule. Arch Ophthalmol 1988;106:601.

of the anterior cavernous sinus, divisional third nerve palsies may occur in the setting of more proximal lesions.

Lesions of the third nerve nucleus are rare but may be manifested by the following findings: (1) unilateral third nerve palsy with contralateral superior rectus weakness and (2) bilateral partial ptosis.15 These findings are present because a single, central caudal nucleus is shared between the right and left third nerve nuclear complexes, and each superior rectus subnucleus innervates the contralateral superior rectus muscle.

The presence of other neurologic signs and symptoms may also be helpful in localizing third nerve palsies to the brainstem, subarachnoid space, cavernous sinus, or orbital apex. For example, a hemiparesis contralateral to the side of the third nerve palsy would suggest a lesion in the anterior midbrain involving the third nerve fascicle and cerebral peduncle (Weber’s syndrome).16 Similarly, a lesion affecting the third nerve fascicle and red nucleus would produce a third nerve palsy and contralateral ataxia (Claude’s syndrome). The presence of other cranial neuropathies, particularly those involving contralateral or nonadjacent cranial nerves, would suggest a subarachnoid space process, such as an inflammatory, carcinomatous, or infectious meningitis. Cavernous sinus syndromes (see later section) may be characterized by dysfunction of the third nerve (superior division, inferior division, or both) along with the ipsilateral fourth, fifth (V1 and V2 divisions), and sixth nerves and the oculosympathetics (Fig. 1–7). Lesions located more distally at the orbital apex (Fig. 1–6) may also involve the third, fourth, and sixth nerves, as well as the ophthalmic (V1) division of the fifth nerve, oculosympathetics, and optic nerve. Proptosis or other orbital signs may be present.

Fourth Nerve

Crossed innervation is also a unique characteristic of the superior oblique muscle, which is supplied by the contralateral fourth (trochlear) nerve nucleus in the midbrain. Exiting posteriorly, the fourth nerve crosses over to the contralateral side of the midbrain, then travels ventrally within the subarachnoid space. The fourth nerve subsequently follows a course similar to that of the third nerve, traveling within the lateral wall of the cavernous sinus (Fig. 1–7) to the orbital apex (Fig. 1–6). However, unlike the third nerve, which travels through the annulus of Zinn, the fourth nerve enters the superior orbit outside of the annulus to innervate the superior oblique muscle.

The fourth (trochlear) nerve is unique in its dorsal exit from the midbrain (Fig. 1–6), posterior crossover within the subarachnoid space, and innervation of the superior oblique muscle contralateral to its nucleus. Because of these anatomic features and the resultant long course from midbrain to muscle, the fourth nerve is particularly vulnerable to injury in the setting of head trauma. Unilateral or bilateral fourth nerve palsies are indeed common in this setting.

Lesions of the fourth nerve at any location from its nucleus to the orbit are manifested by weakness of the superior oblique muscle. This results in a tendency for the affected eye to rest higher than the other (a hypertropia). Patients note vertical double vision and, on questioning, may admit to a relative tilt of one image. Superior oblique weakness is particularly notable when the patient is asked to look downward with the affected eye in adduction (Fig. 1–9).17 Difficulty reading at near is thus a common complaint. The vertical diplopia generally

Figure 1–9 Photograph of patient with a left fourth nerve palsy. Because of weakness of the left superior oblique muscle, the patient has difficulty depressing the left eye in adduction.

becomes more pronounced when the patient looks in the direction contralateral to the side of the affected superior oblique (away from the side of the hypertropia) and when the head is tilted toward the side of the hypertropia. Thus, patients with fourth nerve palsies often manifest a head tilt away from the side of the affected superior oblique muscle.

As is the case for third nerve palsies, the presence of other neurologic symptoms, cranial neuropathies, or oculosympathetic paresis (Horner’s syndrome) may be useful in localizing fourth nerve palsies to the midbrain, subarachnoid space, cavernous sinus, or orbital apex. For instance, the presence of an ipsilateral Horner’s syndrome and contralateral superior oblique weakness strongly suggests a nuclear fourth nerve lesion secondary to a midbrain process. However, fourth nerve palsies (as well as third and sixth nerve palsies) may also occur in isolation as manifestations of intrinsic brainstem processes, including stroke, hemorrhage, or neoplasm.

Sixth Nerve

The sixth cranial nerve (abducens nerve) has its nucleus at the medial dorsal pontomedullary junction, near the genu of the seventh (facial) nerve. This area within the dorsal pons is termed the facial colliculus. From the sixth nerve nucleus, motor neuron axons traverse anteriorly within the sixth nerve fascicle, whereas interneurons cross over to ascend within the contralateral medial longitudinal fasciculus (MLF) to the medial rectus subnucleus of the third nerve (Fig. 1–11).

After exiting the pons, the sixth nerve ascends along the ventral aspect of the brainstem (Fig. 1–6), passes through Dorello’s canal beneath the petroclinoid (Gruber’s) ligament, and enters the cavernous sinus. Unlike the third and fourth nerves, which travel within the lateral wall of the cavernous sinus, the sixth nerve is freely situated within the cavernous sinus, lateral to the internal carotid artery (Fig. 1–7). Because the sixth nerve lies in close proximity to the cavernous carotid artery, it may be involved early in the setting of an expanding cavernous carotid artery aneurysm and may be associated with a Horner’s syndrome. The sixth nerve enters the orbit through the superior orbital fissure and annulus of Zinn (Fig. 1–6) to innervate the ipsilateral lateral rectus muscle. Lesions of the sixth nerve nucleus produce an ipsilateral horizontal conjugate gaze palsy, or inability to move both eyes toward the side of the affected sixth nerve nucleus. Because the genu of the seventh (facial) nerve passes posteriorly around the sixth nerve nucleus in the facial colliculus, lesions in this area may result in an ipsilateral peripheral seventh nerve palsy in addition to the conjugate gaze palsy (facial colliculus syndrome). In the setting of a sixth nerve nuclear lesion,

the inability to move the eyes past the midline horizontally cannot be overcome by the oculocephalic (Doll’s head) maneuver or caloric testing. Lesions involving the paramedian pontine reticular formation (PPRF) (Fig. 1–10) but sparing the sixth nerve nucleus also produce an ipsilateral horizontal conjugate gaze palsy.18 Gaze palsies that occur in this rare setting, however, can be overcome by the oculocephalic maneuver, although the patient cannot move the eyes voluntarily past the midline. In this manner, lesions of the PPRF that spare the sixth nerve nucleus may be distinguished from those affecting the sixth nerve nucleus.

Because the sixth nerve lies freely within the cavernous sinus, rather than residing within the lateral wall (Fig. 1–7), it may be particularly susceptible to compression in this location by tumor or aneurysm. Unilateral or bilateral sixth

VN

Figure 1–10 Summary of eye movement control. The center figure shows the supranuclear connections from the frontal eye fields (FEF) and the parieto-occipital-temporal junction region (POT) to the superior colliculus (SC), rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF), and the paramedian pontine reticular formation (PPRF). The FEF and SC are involved in the production of saccades, whereas the POT is thought to be important in the production of pursuit. The schematic drawing on the left shows the brainstem pathways for horizontal gaze. Axons from the cell bodies located in the PPRF travel to the ipsilateral sixth nerve (abducens) nucleus (VI) where they synapse with abducens motoneurons whose axons travel to the ipsilateral lateral rectus muscle (LR) and with abducens internuclear neurons whose axons cross the midline and travel in the medial longitudinal fasciculus (MLF) to the portion(s) of the third nerve (oculomotor) nucleus (III) concerned with medial rectus (MR) function (in the contralateral eye). The schematic drawing on the right shows the brainstem pathways for vertical gaze. Important structures include the riMLF, PPRF, the interstitial nucleus of Cajal (INC), and the posterior commissure (PC). Note that axons from cell bodies located in the vestibular nuclei (VN) travel directly to the sixth nerve nuclei and, mostly via the MLF, to the third (III) and fourth (IV) nerve nuclei. (From Miller NR: Neural control of eye movements. In Miller NR (ed): Walsh and Hoyt’s Clinical Neuro-Ophthal- mology, 4th ed. Baltimore, Williams & Wilkins, 1985, p 627.)

nerve palsies also occur as false localizing signs of supratentorial mass lesions, edema, hemorrhage, or other causes of increased intracranial pressure. Within the subarachnoid space, the nerve is particularly vulnerable to downward pressure on the brainstem as it ascends the ventral aspect of the pons, passes beneath the petroclinoid ligament, and travels over the edge of the tentorium (Fig. 1–6). This appears to be the mechanism of sixth nerve palsies resulting from increased intracranial pressure.

ORBITAL APEX AND CAVERNOUS SINUS SYNDROMES

Lesions at the superior orbital fissure and orbital apex (Fig. 1–6) are characterized by combinations of third, fourth, and sixth nerve palsies, as well as facial sensory loss in the V1 (ophthalmic) distribution, optic neuropathy, and oculosympathetic paresis. This syndrome is often difficult to distinguish from the cavernous sinus syndrome, which may involve a combination of cranial nerves three, four, six, the V1 and V2 distributions of the fifth nerve, and oculosympathetic paresis (Horner’s syndrome) (Fig. 1–7). Visual loss may also be present if the optic nerve or chiasm is involved, but lesions affecting the cavernous sinus in isolation, unlike orbital apex syndromes, do not produce optic neuropathy.

ANATOMY OF THE SUPRANUCLEAR, INTERNUCLEAR, AND

VESTIBULO-OCULAR GAZE PATHWAYS

The initiation of conjugate eye movements is controlled by pathways and centers above the third, fourth, and sixth nerve nuclei (supranuclear pathways) and by interconnections among these nuclei (internuclear pathways). Inputs from the vestibular system (vestibulo-ocular pathways) also play an important role in the maintenance of eye position with head movement. Pursuit eye movements are initiated and maintained through cortical and cerebellar inputs.

SACCADE SYSTEM

Saccadic eye movements (fast conjugate eye movements to a fixed target) are initiated in the frontal eye fields (Fig. 1–10). The supplementary eye fields and parietal eye fields also play a role in saccade generation. The frontal eye fields send inputs to saccade-generating neurons within the superior colliculus, the contralateral PPRF, and rostral interstitial nucleus of the medial longitudinal fasciculus (riMLF) (Fig. 1–10). The horizontal saccade pathway (Fig. 1–10, left) involves axons that travel from cell bodies in the PPRF to the ipsilateral sixth nerve nucleus. From a synapse in the sixth nerve nucleus, axons of abducens motor neurons travel to the ipsilateral lateral rectus muscle, whereas axons of abducens internuclear neurons cross over and ascend in the contralateral MLF to the medial rectus subnucleus of the third nerve. It is this internuclear connection between the PPRF and contralateral third nerve nucleus via the MLF that is responsible for conjugate horizontal gaze. Each frontal eye field, therefore, generates a conjugate movement of the eyes toward the contralateral side of the body. Brainstem pathways for vertical saccades involve the riMLF, the PPRF, the posterior commissure (PC), and the interstitial nucleus of Cajal (INC) (Fig. 1–10, right).

VESTIBULO-OCULAR SYSTEM

Conjugate gaze in both the vertical and horizontal planes is stabilized through inputs from the vestibular nuclei. From each vestibular nuclear complex, axons subserving horizontal gaze-holding connect to the contralateral sixth nerve nucleus; motor neurons from this nucleus innervate the lateral rectus, whereas interneurons cross back over to ascend in the MLF to the third nerve nucleus (Fig. 1–10, left). Stimulatory input from each vestibular nucleus, therefore, produces conjugate horizontal gaze toward the contralateral side of the body. Inputs from the vestibular nuclei also influence vertical gaze-holding through inputs to the contralateral fourth nerve nucleus, third nerve nucleus, INC, and riMLF (Fig. 1–10, right). The maintenance of ocular alignment in the vertical plane is controlled by the existence of balanced inputs from the vestibular nuclei to the fourth nerve nucleus (innervates contralateral superior oblique muscle), the superior rectus subnucleus (innervates contralateral superior rectus), and the inferior oblique and inferior rectus subnuclei (innervate ipsilateral inferior oblique and inferior rectus) (Fig. 1–11).19 An imbalance between these inputs to the various subnuclei results in skew deviation.

PURSUIT SYSTEM

Smooth pursuit eye movements (conjugate maintenance of fixation of the eyes while following a moving target) are generated in higher cortical centers, especially the parieto-occipital-temporal (POT) junction (Fig. 1–10). Inputs are sent from each POT to the superior colliculi (SC), from which control of horizontal and vertical pursuit eye movements is mediated. Unlike the saccadic system, in which each hemisphere (frontal eye fields and other centers) produces conjugate horizontal eye movements toward the contralateral direction, the pursuit system is designed such that each hemisphere controls conjugate pursuit eye movements to the ipsilateral visual space.20

The Pupillary Pathways

ANATOMY OF THE PUPILLARY PATHWAYS

Constriction of the Pupil—Parasympathetic Pathway

Pupillary constriction to light and near stimuli is mediated via parasympathetic nerve fibers that travel along the third cranial nerve. The pupillary light reflex pathway (Fig. 1–12) is a four-neuron pathway consisting of three synapses.21 Light information from retinal ganglion cells travels through the optic nerves, chiasm (with decussation of the fibers from nasal retina), and tracts, synapsing in the pretectal nuclei of the dorsal midbrain. Note (Fig. 1–12) that both pretectal nuclei receive inputs from both eyes. In turn, each pretectal nucleus sends axons to both Edinger-Westphal nuclei. It is this duality of pathways that provides the anatomic basis for the consensual response of the pupils to light (i.e., the fact that both pupils, if normally innervated, constrict equally in response to a light stimulus in either eye). Parasympathetic fibers for pupillary constriction travel along the third nerve to the ipsilateral ciliary ganglion within the orbit (Fig. 1–12).

SR

SO

IO

IR

III

IV

VN

SCC

Figure 1–11 The main excitatory vestibulo-ocular connections from the vertical semicircular canals. The dashed line indicates the midline of the brainstem. The arrows indicate directions of eye movement when individual extraocular muscles are stimulated. Filled circles receive the anterior canal projection; open circles receive the posterior canal projection. Lesions occurring within these vestibulo-ocular pathways result in skew deviation. III, third nerve (oculomotor) subnuclei; IV, fourth nerve (trochlear) nucleus; IO, inferior oblique muscle; IR, inferior rectus muscle; SCC, semicircular canals; SO, superior oblique muscle; SR, superior rectus muscle; VN, vestibular nuclei. (From Zee DS: The organization of the brainstem ocular motor subnuclei. Ann Neurol 1978;4:384.)

Distal to this synapse, the pupillary sphincter muscle (and ciliary muscle for lens accommodation) is innervated by the postganglionic parasympathetic fibers.

The constriction of the pupils to near stimuli is also accomplished through the parasympathetic pathways. However, the near reflex pathway, thought to originate in higher cortical centers, bypasses the pretectal nuclei in the dorsal midbrain. Near inputs thus descend directly to the area of the Edinger-Westphal nuclei. This distinction between the light and near pathways forms the basis for some forms of pupillary light-near dissociation (pupils that react to near but not to light), in which the dorsal midbrain and pretectal nuclei are involved.

Dilation of the Pupil—Oculosympathetic Pathway

Dilation of the pupil is mediated through sympathetic pathways, which originate in the hypothalamus (Fig. 1–13).22 In this three-neuron pathway, the first-order