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Show · t 1992 Raven Press, Ltd., New York Levator- Sparing Nuclear Oculomotor Palsy Clinical and Magnetic Resonance Imaging Findings J. Shepard Bryan, M. D. and Latif M. Hamed, M. D. Two patients with diplopia presented with unilateral oc · ulomotor palsy, defective elevation of the contralateral eye, and sparing of the levator palpebrae muscle. In each case, magnetic resonance imaging disclosed an infarction of the oculomotor nuclear complex in the meso encephalon. This clinical neuroradiological correlation is consistent with Warwick's scheme pertaining to the neuroanatomy of the oculomotor nuclear complex and demonstrates the utility of MRl in diagnosing ocular motility disorders of brainstem origin. Key Words: Levator palpebrae muscle- Magnetic resonance imaging- Unilateral oculomotor palsy. . From the Department of Ophthalmology, University of FlorIda College of Medicine, Gainesville, Florida, USA. This work was supported in part by an unrestricted grant trom Research to Prevent Blindness, Inc. Address correspLlndence and reprint requests to Dr. L M. Hamed. Department of Ophthalmology, JH~ IHSC. BLl~ 100284, G. lln' · ' · ' lll" Ff "'~ hlIJ- II~,~- l. l S.'" - 26 The oculomotor nucleus complex represents a specialized functional organization of axonal cell bodies located within the rostral midbrain at the level of the superior colliculus, Warwick's primate research provides the basis of the current understanding of the functional anatomy of the oculomotor nucleus ( 1). It is assumed that the oculomotor nuclear complex in nonhuman primates closely resembles that of man. However, only a limited number of cases in humans with clinicopathologic or clinicoradiologic verification of nuclear oculomotor palsies have been described in the literature. The following case reports support Warwick's conceptualization of the oculomotor nuclear complex in humans and are, to our knowledge, the first such cases in the English literature with clinical neuroradiologic correlation utilizing magnetic resonance imaging. CASE STUDIES Case 1 A 74- year- old man presented to a local emergency room with a history of sudden onset nausea, dizziness, and weakness followed 30 minutes later by unresponsiveness. His medical history was remarkable for hypertension, atherosclerotic vascular disease, noninsulin- dependent diabetes mellitus, and dementia. The patient had suffered an occipital infarction and had undergone right carotid endarterectomy 3 months prior to presentation. An examination upon admission in September 1989 revealed that the patient was unresponsive, with a systemic blood pressure of 154170 mm Hg. The left pupil was dilated, measuring 8 mm in diameter, and did not react to light. The right pupil reacted briskly to light. Oculocephalic reflexes of the left eye demonstrated normal abduction but a NUCLEAR OCULOMOTOR SYNDROME 27 complete adduction deficit. The right eye showed full horizontal motility. The patient had a flaccid right hemiplegia and a positive right Babinski reflex. Computed tomography ( CT) of the head showed only an old occipital infarction. The patient was placed on heparin anticoagulation therapy. He became responsive, and the hemiparesis resolved within several days. He was discharged on Coumadin with a diagnosis of a residual third nerve palsy. The Coumadin was subsequently discontinued, and daily aspirin therapy was begun for stroke prophylaxis. The patient was referred for evaluation of persistent diplopia. A neuro- ophthalmologic examination in December 1990 demonstrated visual acuity of 20/ 25 00 and 20/ 30 OS. There were 40 prism diopters ( PO) of left exotropia with 12 PO of left hypertropia in the primary position. Testing of ocular ductions showed deficient adduction and depression of the left eye. Elevation was decreased bilaterally, more notably in the right eye ( Fig. 1). The pupils measured 3.0 mm on the right and 3.5 mm on the left. The right pupil reacted briskly to light; the left reacted sluggishly. No afferent defect was present. An external examination revealed no blepharoptosis. Magnetic resonance imaging ( MRI) with gadolinium ethylenediaminetetraacetate ( EDTA) enhancement disclosed a lesion involving the left oculomotor nucleus in the rostral brainstem ( Fig. 2). Careful review of the MRI with a neuroradiologist revealed no rostral or caudal extension of the localized midbrain lesion. Case 2 A 49- year- old man presented to a local emergency room in November 1988 with complaints of dizziness, headache, and ataxia, followed 4 hours later by onset of binocular vertical diplopia. There was no associated loss of consciousness. His medical history was remarkable for poorly controlled systemic hypertension. Systemic blood pressure upon admission was 2201138 mm Hg. Computed tomography of the head demonstrated an intracranial hemorrhage in the right basal ganglia with possible brainstem extension. Cerebral angiography revealed no aneurysm. The patient gradually improved in the hos- FIG. 1. Ocular versions in the diagnostic positions of gaze show the typical features of levator- sparing left oculomotor nuclear palsy. Notice the bilaterally deficient elevation, more pronounced on the right side. I Cli" Neuro- ophthalmol. Vol. 12, No. I, 1992 28 f. S. BRYAN AND L. M. HAMED FIG. 2. Magnetic resonance imaging with gadolinium EDTA enhancement demonstrates a focal lesion involving the left oculomotor nucleus. pita!. His blood pressure was initially managed with intravenous nipride followed by oral procardia, hydrochlorothiazide, and capoten. The patient was referred for evaluation of persistent diplopia. In April 1991, a neuro- ophthalmologic examination revealed a visual acuity of 20/ 25 00 and 20/ 20 as. There were 25 prism diopters of right exotropia and 45 prism diopters of right hypertropia in the primary position. The right eye showed poor adduction and depression with a mild decrease in elevation. Ductions of the left eye were full except for deficient elevation. The pupils measured 4 mm on the right and 2 mm on the left. Pupillary light reaction was sluggish 00 and brisk as. No afferent pupillary defect was present. There was no blepharoptosis. The remainder of the ocular examination was normal. T2- weighted MRI demonstrated a lesion involving the right oculomotor nucleus complex consistent with a previous hemorrhagic infarction ( Fig. 3). No rostral or caudal extension of the lesion was noted. DISCUSSION Since the 1800s, many researchers have speculated on the functional organization of the oculomotor nucleus. However, Warwick's treatise is widely considered to be the classic work on this FIG. 3. T2- weighted magnetic resonance imagery shows a focal lesion at the level of the right oculomotor nucleus complex. subject ( 1). Warwick examined primate oculomotor nuclei for evidence of retrograde degeneration after extirpation of different oculomotor- innervated extraocular muscles. Results demonstrated that within the oculomotor nucleus complex, the inferior rectus, inferior oblique, medial rectus, superior rectus, and levator palpebrae muscles are each subserved by a specific compact group of cell bodies in the form of a subnucleus. These subnuclei exist as discrete narrow columns of cell bodies with a rostrocaudal and dorsoventral orientation within the brainstem. This functional organization of the oculomotor nucleus in nonhuman primates has been confirmed by more recent investigations ( 2,3). These studies involved examination of the oculomotor subnuclei for the presence of horseradish peroxidase from retrograde transport after injection of the marker into the various oculomotor- innervated extraocular muscles. Studies demonstrate that innervation of the extraocular muscles supplied by the oculomotor subnuclei is ipsilateral except for the superior rectus and levator palpebrae muscles. Both levator palpebrae muscles are subserved by a single, centrally located subnucleus known as the central caudal nucleus. The superior rectus muscle receives innervation from a contralaterally located subnucleus. Because of this unique pattern of innervation, a unilateral oculomotor nucleus lesion causes bilateral eye movement dysfunction. Similarly, blepharoptosis resulting from a lesion of the oculomotor nucleus is always bilateral ( 4). NUCLEAR OCULOMOTOR SYNDROME 29 The presence in humans of a central caudal nucleus supplying both levator palpebrae muscles is supported by clinicopathologic and clinicoradiologic correlation. Because of its location at the far caudal and dorsal extent of the oculomotor nuclear complex, selective involvement of the levator subnucleus is possible, leading to isolated bilateral ptosis ( 5,6). More commonly, bilateral ptosis occurs in combination with an oculomotor paralysis ( 6- 13). Rarely, a nuclear oculomotor nerve paralysis can occur without ptosis by sparing of the levator subnucleus ( 14,15). This was the case in both of our patients. Nerve fibers originating in the contralateral superior rectus subnucleus have been shown to pass through the ipsilateral oculomotor nuclear complex to exit in the nerve fascicle ( 16). Thus, a nuclear third nerve lesion is expected to cause bilateral supraduction deficits in addition to ipsilateral dysfunction of the medial rectus, inferior rectus, and inferior oblique muscles. Such bilateral paresis of elevation has been termed a pseudo- Parinaud's syndrome ( 17). There are very few case reports to support Warwick's concept of crossed innervation of the superior rectus in humans ( 8,9,13,15,18-- 20). Our two cases with clinical radiologic correlation by MRl provide further evidence that Warwick's scheme can be applied to humans. Clinically, the presence of ipsilateral exotropia and contralateral hypotropia is particularly revealing of a nuclear third nerve palsy in both cases and highlights the contralateral innervation pattern of the superior rectus subnucleus ( 17). It is interesting that in both patients, the central caudal nucleus is spared because of its unique and relatively isolated location within the oculomotor nucleus complex. Magnetic resonance imaging demonstrates the lesions within the mesencephalon, involving the oculomotor nucleus complex. Careful review of the scans with a neuroradiologist confirms the localized nature of these lesions with no extension in adjacent sections taken rostrally or caudally. The presentation of patient 1 initially pointed to a lesion of the left oculomotor fascicle ( 21), but the patient was left ultimately with a nuclear third nerve palsy. Upon admission, a Weber's syndrome was diagnosed, consisting of a pupil involving oculomotor palsy and contralateral hemiplegia. Initial complaints of dizziness presumably resulted from involvement of the red nucleus or cerebellum. Ischemia to the rostral medial reticular formation may account for the somnolence and decreased responsiveness. The patient's rostral brainstem stroke was most likely caused by occlusion of the distal basilar artery and its small pene-trating branches that supply the mesencephalon on the left side. Such occlusion occurs most frequently as a result of embolic disease ( 22). There was reversible ischemia to some affected areas of the mesencephalon, including the oculomotor nerve fascicle, but the infarction of the left oculomotor nucleus complex was permanent. Presumably, embolic occlusion of the proximal portion of the distal basilar artery and its penetrating branches was transient and reversible, making the patient's hemiparesis and somnolence temporary. Propagation of the embolus however, caused permanent occlusion of the distal extent of a paramedian penetrating artery with terminal arborizations around the left oculomotor nuclear complex. Patient 2 suffered a hemorrhagic infarction of the oculomotor nucleus complex. A mesencephalic hematoma resulting in nuclear oculomotor paralysis has been reported only once in the literature ( 20). The oculomotor palsy in that patient improved with resolution of the midbrain hematoma over 1 week. Our patient suffered a permanent infarction of the oculomotor nerve nucleus. The Edinger- Westphal subnuclei are located dorsal and rostral to the motor subunits of the oculomotor nucleus complex. In Warwick's scheme, these subnuclei are connected across the midline. As a result, pupil involvement might be expected to be bilateral if associated with a nuclear third nerve palsy. Nevertheless, ipsilateral pupillary abnormalities can occur in oculomotor nucleus injury ( 14,15). This was the case in both of our patients. The ipsilateral pupils were slightly larger and sluggishly reactive to light compared to the contralateral side. Presumably, the midline connection of the Edinger- Westphal subnuclei was not involved by the ischemic injury. The cases presented are the first known reports in the English literature of nuclear third nerve palsies with clinical and neuroradiologic correlation by MRI. One case has been reported in the French literature ( 23). Clinical radiologic correlations of brainstem oculomotor fascicular lesions by MRI ( 24- 26) or CT ( 27,28) have been reported. Magnetic resonance imaging of the posterior fossa is clearly superior to CT scan and is particularly useful in the neuro- ophthalmological evaluation of oculomotor abnormalities of brainstem origin ( 26,29). In summary, these case reports help to verify Warwick's concept of crossed innervation of the superior rectus muscle in man. Each patient's unilateral oculomotor nuclear complex infarction caused bilateral supraduction deficits. In both cases, ptosis was absent from sparing of the centrally located levator subnucleus. The infarctions I Clill Neuro- ophtlwlmol, Vol. 12, No. 1, 1992 30 f. S. BRYAN AND L. M. HAMED 22. 24. 29 26. nolence due to stroke: a case report. Ann Acad Med 1990; 19: 382- 4 14. Keane J, Zaias B, Itabashi H. Levator- sparing oculomotor nerve palsy caused by a solitary midbrain metastasis. Arch NeuroI1984; 41: 21Q- 12. 15. 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