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Show Journal of Neuro- Ophthalmology 20( 2): 130- 134, 2000. © 2000 Lippincott Williams & Wilkins, Inc., Philadelphia Bilateral Ptosis With Pupil Sparing Because of a Discrete Midbrain Lesion: Magnetic Resonance Imaging Evidence of Topographic Arrangement Within the Oculomotor Nerve Naokatsu Saeki, MD, Akira Yamaura, MD, and Kenro Sunami, MD The topographic arrangement within the midbrain oculomotor nerve is not adequately elucidated in humans. Two patients with a partial oculomotor palsy because of a localized infarction or hematoma were treated. Both patients had bilateral ptosis, impaired adduction, and supraduction. One patient had impaired infraduction and pupillary involvement on one side. Results of computed tomography and magnetic resonance imaging revealed discrete lesions at the dorsal midbrain tegmentum that spared the rostral midbrain. The authors' cases elucidate that pupillary components take the most rostral course. This report provides indirect magnetic resonance imaging evidence to prove the course of pupillary fibers. Based on the different neuro- ophthalmologic findings in the authors' cases ( sparing or affecting pupillary component and infraduction), the nerves of the inferior rectus and inferior oblique for infraduction pass more rostrally than those of medial rectus, superior rectus, and levator palpebrae. The nuclear and fascicular arrangement within the midbrain oculomotor nerve is speculated to be pupillary, extraocular, and eyelid elevation in the rostro- caudal order, based on the neuro- ophthalmologic impairment and magnetic resonance imaging findings in the authors' patients and in previous animal experiments. Knowing the fascicular and nuclear arrangement within the midbrain in detail will offer diagnostic clues for differentiation of causes for partial oculomotor palsy. Key Words: Infarct- Midbrain- Oculomotor nerve- Ptosis- Pupil- sparing. Partial lesions of oculomotor nucleus and fascicles were described in previous reports based on autopsied cases and computerized imaging ( l ^ t ) . However, those cases often had lesions that were too large to achieve minute ocular and anatomic correlations. In this respect, evidence of the oculomotor nuclear and fascicular arrangement with localized and discrete lesions in humans Manuscript received November 24, 1998; accepted December 15, 1999. From the Department of Neurological Surgery ( NS, AY, KS), Chiba University, School of Medicine, Chiba, Japan; and the Department of Neurosurgery ( KS), Kawatetsu Chiba Hospital, Chiba, Japan. Address correspondence and reprint requests to Naokatsu Saeki, MD, Department of Neurological Surgery, Chiba University, School of Medicine, 1- 8- 1 Inohana, Chuoh- ku Chiba- shi, Chiba, Japan 260. has been inadequate. The recent advent of magnetic resonance imaging ( MRI) has provided further detailed correlations between neurologic signs and neuroanatomy ( 5- 15). This paper reports two cases of partial oculomotor palsies and bilateral midbrain ptosis associated with pupillary sparing. Magnetic resonance imaging and neurologic findings have provided clues to elucidate the nuclear and fascicular arrangement within the human midbrain oculomotor complex. CASE REPORTS Case 1 A 63- year- old woman with a 7- year history of untreated hypertension had an episode of subarachnoid hemorrhage because of a ruptured aneurysm of the right middle cerebral artery. The aneurysm was clipped in the neck on the day of admission. There was no neurologic deficit after the procedure. Two months later, the patient underwent another procedure to clip the unruptured left middle cerebral artery aneurysm. The anesthetic and operative procedure was uneventful. No remarkable change of vital signs was noted during the procedure. After emergence from anesthesia after the second operation, the patient was arousable but could not open her eyes. A neurologic examination the next day revealed that she was alert and without limb paresis. Neuro- ophthalmologic findings included bilateral ptosis and extraocular motion ( EOM) impairment. She had normal abduction OU, but she could not elevate or adduct her eyes normally. Depression of her eyes was less involved ( Fig. 1). The Bell phenomenon was absent. The pupils were normal in size and reacted briskly. She had trunkal and limb ataxia associated with dysarthria. Results of preoperative MRI showed a pontine lacunar infarct, which had been asymptomatic. The left vertebral angiography revealed diffuse sclerotic change, but no stenotic or occlusive change. Results of a computed tomography scan did not demonstrate a responsible lesion. Results of MRI showed a high- intensity lesion in the midbrain tegmentum ( Fig. 2). 130 BILATERAL PTOSIS WITH PUPIL SPARING 131 FIG. 1. Extraocular motion in case 1. Bilateral ptosis and marked limitation of medial and upward motion were noted. Downward motion was involved to a lesser degree. The pupillary component was spared. A: Bilateral ptosis. B: Right supraduction. C: Supraduction. D: Left supraduction. E: Right lateral gaze. F: Mid- position. G: Left lateral gaze. H: Right infraduction. I: Infraduction. J: Left infraduction. The patient was diagnosed with a midbrain infarct, based on her history of hypertension, angiographic change, and the old lacunar infarct in the pons; the midbrain infarct occurred speculatively at the perianesthetic period because of occlusion of the paramedian branch of the basilar artery. The patient was placed on rehabilitation and recovered gradually from her ocular and cerebellar impairment. Results of MRI showed a more localized lesion 1 month later. Five months later, the patient was discharged with slightly impaired upward gaze and eye opening, as well as persisting ataxia; she could, however, lead an independent life. Results of MRI 8 months later showed a more localized lesion at the dorsal midbrain on the right side ( Fig. 3). Case 2 An 83- year- old man who had been healthy and lived an independent life was found in a stuporous state at home and transferred to our hospital. On admission, the neurologic examination showed slight disorientation, slight right hemiparesis, bilateral ptosis, and impaired EOM, except for abduction. The pupillary size was 4 mm OS and 2.5 mm OD. Pupillary reaction was initially absent bilaterally. Five days later, the patient became alert, and right hemiparesis disappeared. Pupillary size was 3 mm OS and 1 mm OD. The pupillary reaction was noted on the right side ( Fig. 4). Both eyes demonstrated lack of adduction, supraduction, and infraduction. Results of a computed tomography scan on the day of admission showed a hematoma, 12 mm in diameter, at the dorsal tegmentum of the upper brainstem ( Fig. 5). Results of MRI 3 weeks later showed a slightly high-intensity lesion at the lower midbrain and upper pons ( Fig. 5). The patient started walking 1 week after admission. However, 1 month later, a fall led to a fatal cerebral contusion. FIG. 2. T2- weighted image of case 2 taken 4 days after onset. A: The coronal slice shows the high intensity lesion around the middle of the midbrain. B: The axial slice shows the high intensity in the tegmentum of the midbrain. C: The lesion affected both the ventral and dorsal areas. The lesion was 4 mm in rostro- caudal direction and 6 mm in anteroposterior direction. J Neuro- Ophlhalmol, Vol. 20, No. 2, 2000 132 N. SAEK1 ET Ah. FIG. 3. Magnetic resonance imaging of case 1 taken 8 months later. The lesion was more localized to the left dorsal tegmentum in the midbrain, corresponding to the nuclear area. DISCUSSION Two cases with a pupil- sparing type of oculomotor palsy are presented ( bilateral in case 1 and unilateral in case 2). The etiology was an infarct in case 1 and a hematoma in case 2. Common features were bilateral complete ptosis and EOM impairment in the distribution of the oculomotor nerve. The degree of EOM impairment in each case was different. In case 1, infraduction of the eyes was relatively spared, compared with supraduction and adduction. In case 2, all eye motions in the distribution of the oculomotor nerve were completely impaired. Results of MRI in the acute stage demonstrated the nuclear and fascicular lesions at the ventral and dorsal midbrain. Although no further MRI evidence was provided in case 2, the later MRIs in case 1 showed a more localized dorsal lesion. Because a localized lesion at the central caudal nucleus can produce bilateral ptosis, the main lesion in cases 1 and 2 speculatively were located at the caudal subnucleus and/ or the bilateral fascicular lesions close to the subnucleus ( 11- 13). There have been numerous isolated case reports using necropsy materials and computerized imaging correlating isolated midbrain vascular lesions affecting the oculomotor nucleus and fascicles ( 1- 4). In most reports, however, the lesion was part of a larger one, involving the pons or thalamus, and the oculomotor palsy was not partial. Detailed correlations of a discrete small lesion with the anatomy has been realized with the advent of MRI; there have been several single case reports of isolated midbrain vascular lesions producing ptosis with pupil sparing ( 6- 13). The evidence presented in these reports often had only a one- directional MRI slice ( commonly axial). Photographic demonstration of ocular impairment was usually incomplete ( 11,13). The insufficient clinical data seem to be because of subtle and transient oculomotor signs; radiologically, they became undetectable even with superconductive MRI ( 11,13). Therefore, the nuclear and fascicular topography within the oculomotor nerve based on small and discrete lesions in humans has not been adequately analyzed or elucidated. Axons from various subnuclei leave the nucleus, spreading in a widely divergent pattern, as they course anteriorly through red nucleus and converge at the exit of the interpeduncular fossa. The maximum span of divergent fibers ( 10 mm in rostro- caudal direction close to the nucleus and 6 mm in its transverse or axial plane at the level of red nucleus) is supposed to be wide enough to produce a selective involvement of upper, middle, or lower portions in rostro- caudal direction and a medial or lateral portion ( 4,8,14,15). In our patients, MRI results identified the lesion in case 1 to be an infarct ( 4 mm in the rostro- caudal direction and 6 mm in the anteroposterior direction). In case 2, in the acute stage, a hematoma of 12 mm in diameter was detected radiologically. FIG. 4. Extraocular motion in case 2. Bilateral ptosis and marked limitation of extraocular motions, except for bilateral abduction, were noted. The pupillary component was spared. A: Bilateral ptosis. B: Supraduction. C: Right lateral gaze. D: Mid-position. E: Left lateral gaze. F: Infraduction. J Neuro- Ophlhalmol Vol. 20, No. 2, 2000 BILATERAL PTOSIS WITH PUPIL SPARING 133 FIG. 5. A: A computed tomography scan on admission shows a hematoma at the dorsal midbrain tegmentum, 12 mm in diameter. B: T1- weighted axial image shows the high intensity lesion as seen in the computed tomography scan. C: T1 - weighted mid- sagittal slice shows a high intensity lesion at the midline dorsal tegmentum, sparing the upper third of the midbrain. These two cases enhance an already- theorized arrangement of the oculomotor complex for the nucleus and fascicle. The most rostral part of the midbrain was spared, as seen in the MRI results of both cases. In case 1, there was pupillary sparing, and in case 2, both pupils were initially involved and one recovered; this supports the current evidence that pupillary components pass through the most rostral course. Schwarz et al. ( 16) and Saeki et al. ( 14) reported MRI evidence in humans and provided anatomic discussion. In case 1, infraduction of eyes was less impaired than supraduction and adduction. In case 2, all eye motions were completely impaired, as was the pupillary component on one side. Based on the above evidence, one may speculate that infraduction takes a more rostral course than does supraduction and adduction ( 8). Results of MRI did not provide further details enabling more meticulous anatomic correlation to determine the exact arrangement of the subnucleus of the oculomotor nerve. Castro et al. ( 7), by reviewing previous reports of partial oculomotor lesions, proposed a two- dimensional model in which the fibers for inferior oculomotor, nerve superior collicolus inferior collioulus oculomotor nucleus ( lateral somatic cells - caudal central nucl.' visceral nucl. FIG. 6. In a sagittal section at the midbrain, the scheme shows fascicular divisions of fibers for visceral nucleus ( pupillary function), lateral somatic cells ( extraocular motions), and caudal central nucleus ( eye elevation), in rostro- caudal order, based on reports of MRI and neuro- ophthalmologic findings with partial oculomotor palsy. The arrangement is speculatively analogous to the hypothesis for nuclear arrangement proposed by Warwick ( 17). The dotted area demonstrates the lesion in our patients. rectus, medial rectus, levator palpebrae, superior rectus, and inferior oblique muscles lie medial to lateral. The rostro- caudal organization of the nucleus and fascicle has been less clearly determined. Ksiazek et al. ( 10) have proposed a three- dimensional model based on clinical and experimental evidence. Their scheme includes medial- to- lateral organization as described above, as well as a rostro- caudal dimension in which the pupil is most rostral, followed by fibers for the inferior rectus, inferior oblique, medial rectus, superior rectus, and levator palpebrae ( 10). The evidence of fascicular arrangement obtained from our cases corresponds to the proposal of Ksiazek et al. ( 10), even though the arrangement of each ocular muscle within the oculomotor nucleus and fascicle were difficult to determine from our data. Based on our data and review of previous human cases, we speculate that the nuclear and fascicular arrangement is pupil, EOM ( inferior oblique and inferior rectus more rostral than superior rectus and medial rectus), and levator palpebrae, in rostro- caudal direction. The scheme is presented to show the nuclear and fascicular arrangement of the oculomotor nerve in the midbrain ( Fig. 6) ( 17). Knowing the fascicular and nuclear arrangement within the midbrain in detail will offer diagnostic clues to differentiate causes for patients with a partial oculomotor palsy. REFERENCES 1. Biller J, Shapiro R, Evans LS, Haag JR, Fine M. Oculomotor nuclear complex infarction: clinical and radiological correlation. Arch Neurol 1984; 41: 985- 7. 2. Bogousslavsky J, Maeder P, Regli F, Meuli R. Pure midbrain infarction: clinical syndrome, MRI, and etiologic patterns. Neurology 1994; 44: 2032- 40. 3. Gowdon JH, Winkler GF, Wray Shirley. Midbrain ptosis: a case with clinicopathologic correlation. Arch Neurol 1974; 30: 179- 81. 4. Nadeau SE, Trobe JD. Pupil sparing in oculomotor nerve palsy: a brief review. Ann Neurol 1983; 13: 143- 8. 5. Abdollah A, Francis GS. Intraaxial divisional oculomotor nerve paresis suggests intraaxial fascicular organization. Ann Neurol 1990; 28: 589- 90. 6. Breen LA, Hopf HC, Farris BK, Gutmann L. Pupil- sparing oculomotor palsy due to midbrain infarction. Arch Neurol 199 f ; 48: 105- 6. Castro O, Johnson LN, Mamourian AC. Isolated inferior oblique paresis from brain- stem infarction: perspective on oculomotor fascicular organization in the ventral midbrain tegmentum. Arch Neurol 1990; 47: 235- 7. 7 J Neuro- Ophthalmol, Vol. 20, No. 2, 2000 134 N. SAEKI ETAL. 1 8. Hriso E, Masdeu JC, Miller A. Monocular elevation weakness and ptosis: an oculomotor fascicular syndrome? J Clin Neuroophthal-mol 1991; 11: 111- 3. 9. Hopf H, Gutmann L. Diabetic 3rd nerve palsy: evidence for a mesencephalic lesion. Neurology 1990; 40: 1041- 5. 10. Ksiazek SM, Slamovits TL, Rosen CE, Burde RM, Parisi F. Fascicular arrangement in partial oculomotor paresis. Am J Ophthalmol 1994; 118: 97- 103. 11. Liu GT, Carrazana EJ, Charness ME. Unilateral oculomotor palsy and bilateral ptosis from paramedian midbrain infarction. Arch Neurol 1991; 48: 983- 6. 12. Miller NR. Walsh and Hoyl's clinical neurophthalmology. Vol. 2. 4th ed. Baltimore: Williams & Wilkins, 1985. 13. Pratt DV, Orengo- Nania S, Horowitz BA, Oram O. Magnetic resonance imaging findings in a patient with nuclear oculomotor palsy. Arch Ophthalmol 1995; 113: 141- 2. 14. Saeki N, Murai H, Sunami K. Midbrain tegmental lesions affecting or sparing the pupillary fibres. J Neurol Neurosurg Psychiatry 1996; 61: 401- 2. 15. Saeki N. Unilateral upward gaze palsy and ptosis due to localized midbrain infarct: MRI evidence of divisional palsy. J Clin Neuro-sci 2000. In press. 16. Schwartz TH, Lycette CH, Yoon SS, and Kargman DE. Clinico-radiographic evidence for oculomotor fascicular anatomy ( letter). J Neurol Neurosurg Psychiatry 1995; 59: 338. 17. Warwick R. Representation of extra- ocular muscles in oculomotor nuclei of monkey. J Comp Neurol 1953; 98: 449- 95. J Neuro- Ophthalmol, Vol. 20, No. 2, 2000 |
