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Show ORIGINAL CONTRIBUTION Unilateral Midbrain Infarction Causing Upward and Downward Gaze Palsy Murat Alemdar, MD, Senol Kamaci, MD, and Faik Budak, MD Abstract: We report on a 47- year- old- woman who developed sudden complete loss of vertical saccades, smooth pursuit, and vestibular eye movements bilaterally. MRI revealed a unilateral midbrain infarct involving the rostral interstitial nucleus of the medial longitudinal fasciculus ( riMLF) and the interstitial nucleus of Cajal ( INC) and spared the posterior commissure ( PC). The lesion is presumed to have interrupted the pathways involved in vertical gaze just before they decussate, inducing an anatomically unilateral but functionally bilateral lesion. Previous reports of bidirectional vertical gaze palsy have shown lesions involving the PC or both riMLFs. This case is the first to show that a unilateral lesion of the riMLF and the INC that spares the PC may cause complete bidirectional vertical gaze palsy. (/ Neuro- Ophthalmol 2006; 26: 173- 176) The posterior commissure ( PC), interstitial nucleus of Cajal ( INC), and rostral interstitial nucleus of the medial longitudinal fasciculus ( riMLF), neural structures of the reticular formation of the midbrain, are involved in the mediation of vertical gaze. Vertical gaze deficits after a unilateral midbrain lesion have been identified in prior reports ( 1,2). This single case reveals for the first time that a unilateral lesion that involves the riMLF and INC but spares the PC can paralyze upward and downward saccades, smooth pursuit, and the vestibulo- ocular reflex. We report on a 47- year- old woman who developed sudden vertical gaze palsy consisting of bilateral complete loss of upward and downward saccades, smooth pursuit, and vestibular eye movements. Brain MRI studies revealed a unilateral ischemic midbrain infarct sparing the PC but involving the riMLF and INC. Department of Neurology, Faculty of Medicine, University of Kocaeli, Kocaeli, Turkey. Address correspondence to Murat Alemdar, MD, Kocaeli University Tip Fak., Noroloji A. D., Umuttepe, Izmit, 41380, Kocaeli, Turkey; Email: drmuratalemdar@ yahoo. com CASE REPORT A 47- year- old woman developed sudden diplopia worse when looking up or down. She had no associated nausea, vomiting, vertigo, or weakness. Neurologic examination revealed complete upward and downward gaze palsy on voluntary saccadic and pursuit eye movements ( Fig. 1). Vertical oculocephalic maneuver did not elicit any upward or downward response. Bilateral caloric stimulation to test for the vestibular response was also impaired. Bell phenomenon, horizontal eye movements, and convergence were preserved. Motor and sensory examinations were completely normal. Brain MRI on the third day after symptom onset revealed acute infarction of the right upper midbrain in the region containing the riMLF, INC, red nucleus, and substantia nigra pars compacta but sparing the PC ( Fig. 2). Magnetic resonance angiography did not show stenosis of the vertebral or basilar arteries. Pericranial and transcranial Doppler studies were unremarkable. Transthoracic echocardiography detected mitral stenosis and an enlarged left atrium. Transesophageal echocardiography did not reveal any thrombus or septal defect. She was treated with antiplatelet medication. Neuro- ophthalmologic examination 6 months after symptom onset revealed only a slight improvement in downward saccadic and pursuit movements. DISCUSSION Our patient had an impairment of all types of upward or downward eye movements: saccadic, pursuit, and vestibular. MRI showed a high- intensity area limited to the medial side of the right midbrain region involving the riMLF and INC but not the PC. The diffusion- weighted images confirmed the area of acute infarction as sparing the PC. Cases of vertical gaze palsies in association with a unilateral upper midbrain lesion without PC involvement have seldom been reported ( 3,4). They differ from our case in that vestibulo- ocular eye movements were preserved. Our report confirms that a unilateral midbrain lesion can J Neuro- Ophthalmol, Vol. 26, No. 3, 2006 173 J Neuro- Ophthalmol, Vol. 26, No. 3, 2006 Alemdar et al FIG. 1. Position of the patient's eyes in ( a) straight ahead gaze, ( b) left gaze, ( c) right gaze, ( d) attempted upgaze, and ( e) attempted downgaze. paralyze not only upward and downward saccades and smooth pursuit, but also the vestibulo- ocular reflex. Vertical saccades are generated by burst neurons lying in the riMLF, a wing- shaped nucleus lying dorso-medial to red nucleus, rostral to the oculomotor nucleus, and ventral to the periaqueductal gray matter ( 5) ( Fig. 3). Combined upward and downward gaze palsies have been attributed to bilateral infarctions involving both riMLFs resulting from occlusion of a single posterior thalamosub-thalamic paramedian artery ( 5- 7). However, two reports confirmed by neuroimaging- neuropathologic correlation ( 1,4) have provided evidence that a unilateral lesion in the midbrain can paralyze both upward and downward gaze. The projections from the riMLF to oculomotor neurons innervating elevator muscles ( superior rectus and inferior oblique) appear to be bilateral with collaterals probably crossing within the oculomotor nuclear complex. Projections to motoneurons supplying the depressor muscles ( inferior rectus and superior oblique), however, appear to be ipsilateral. Thus, riMLF lesions cause conjugate saccadic palsies that are usually either complete or selectively downward, whereas bilateral riMLF lesions abolish all vertical and torsional saccades. Other types of eye movements are preserved ( 8,9). Downward gaze is mediated by fibers that travel ventrally to the ipsilateral inferior rectus subnucleus and contralateral superior oblique nucleus. Although a unilateral midbrain lesion would not be expected to affect bilateral vertical eye movements, at least not the upward gaze component ( 10), such a phenomenon has been reported ( 1,2,4). There are also reports of lesions producing bidirectional vertical gaze palsy that completely spare the midbrain but involve the thalamus ( 5). Therefore, although this scheme of vertical eye motility is useful clinically, it is still speculative. Ranalli et al ( 1) first reported a patient with paralysis of upward saccades, decreased amplitude and velocity of downward saccades and vertical smooth pursuit, and decreased gain and amplitude of the vestibulo- ocular response. In that case, neuropathologic examination demonstrated that the right riMLF, part of the INC, and the nucleus of the PC were involved but the PC tract was spared. They hypothesized that downgaze fibers might partly decussate in the vertical commissure and traverse the region of the opposite riMLF ( 1). Recent experimental studies have confirmed this view and shown that bilateral lesions of the INC not only impair gaze- holding ability, but also greatly reduce the range of vertical eye movements ( 11). Bogousslavsky et al ( 4) have described a patient with combined upgaze and downgaze palsy in association with an upper midbrain infarct limited to the right riMLF They suggested that a unilateral riMLF lesion may have disrupted bilateral upgaze excitatory and inhibitory inputs and unilateral downgaze excitatory inputs. Paralysis of vertical saccades in our case may also be explained by complete loss of burst cells in the right riMLF and interruption of crossing fibers from the left riMLF as they traverse the right midbrain tegmentum. 174 © 2006 Lippincott Williams & Wilkins Vertical Gaze Palsy J Neuro- Ophthalmol, Vol. 26, No. 3, 2006 FIG. 2. ( a) T2 axial and ( b) diffusion MRI of the midbrain. The arrows indicate the ischemic lesion at caudal ( left) and rostral ( right) midbrain levels. Vertical pursuit signals are known to traverse the rostral midbrain before innervating ocular motor nuclei. Neuronal firing related to vertical pursuit pathways has been recorded in or near the INC in monkeys ( 12). The INC also contains neurons that contribute to neural integration of vertical eye movements. It contains burst- tonic neurons that show a discharge pattern similar to that of vertical oculomotor neurons and receives strong anatomic connections from the vestibular nucleus. The INC is important for holding the eyes in eccentric gaze after a vertical saccade and coordinating eye- head movements in the roll plane. Bilateral destructive INC lesions are known to limit FIG. 3. Histologic cross- sections at caudal ( left) and rostral ( right) midbrain levels showing structures involved in the mediation of vertical gaze. PC, posterior commissure; PUL, pulvinar nucleus of the thalamus; SC, superior colliculus; PG, periaqueductal gray; RN, red nucleus; SN, substantia nigra; 3rd nuc, third cranial nerve nucleus; Int Caps, internal capsule; riMLF, rostral interstitial nucleus of the medial longitudinal fasciculus; INC, interstitial nucleus of Cajal. 175 J Neuro- Ophthalmol, Vol. 26, No. 3, 2006 Alemdar et al the range of vertical gaze ( 10). The main projections from the INC to ocular motoneurons ( in oculomotor and trochlear nuclei) and the contralateral INC are through the PC ( 13). Therefore, a lesion of the PC may be functionally a bilateral lesion and affect inputs to motoneurons on both sides. REFERENCES 1. Ranalli PJ, Sharpe JA, Fletcher WA. Palsy of upward and downward saccadic, pursuit, and vestibular movements with a unilateral midbrain lesion: pathophysiologic correlations. Neurology 1988; 38: 114- 22. 2. Hommel M, Bogousslavsky J. 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