Monocular Single Saccadic Pulses

Clinical Correspondence Monocular Single Saccadic Pulses Eun Hye Oh, MD, Seo-Young Choi, MD, Kwang-Dong Choi, MD, Jae-Hwan Choi, MD A 40-year-old man experienced diplopia, gait disturbance, dysarthria, and dysphagia for 2 months. He had no associated headache or ocular pain, and denied any preceding illnesses. Ocular motor examination revealed a conjugate gaze palsy to the left and adduction paresis in the left eye with abducting nystagmus in the right eye during rightward gaze, findings consistent with one-and-a half syndrome. Fixation with the right eye was continuously interrupted by spontaneous abducting eye movements (see Supplemental Digital Content, Video, http://links.lww. com/WNO/A359). He also showed gaze-evoked nystagmus during vertical gaze. Other findings included dysarthria, decreased soft palate elevation on the left side, and truncal ataxia. Brain MRI showed widespread gadoliniumenhancing hyperintensities in the dorsal pons and medulla, particularly on the left side, extending to the cerebellum (Fig. 1). Laboratory evaluation including autoimmune antibody screening, cerebrospinal fluid analysis, and paraneoplastic antibody tests were normal. Eye movement recording with video-oculography (SLMED, Seoul, Korea) showed spontaneous bursts of abducting saccades in the right eye followed by a slow return toward the initial position, consistent with single saccadic pulse (SSP) (see Supplemental Digital Content, Video, http://links.lww.com/WNO/A359) (Fig. 2A, B). The SSPs occurred irregularly at a frequency of 1-3 Hz and up to 6° in amplitude. Without visual fixation, SSPs were markedly reduced. During a rightward saccade, the right eye had normal saccadic velocity followed by abducting nystagmus, but the left eye showed a marked slow movement with a small range of adduction (Fig. 2C). Department of Neurology (EHO, J-HC), Pusan National University School of Medicine, Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Yangsan, Gyeongsangnam-do, Korea; and Department of Neurology (S-YC, K-DC), Pusan National University Hospital, Pusan National University School of Medicine and Biomedical Research Institute, Busan, Korea. The authors report no conflicts of interest. Supplemental digital content is available for this article. Direct URL citations appear in the printed text and are provided in the HTML and PDF versions of this article on the journal's Web site (www. jneuro-ophthalmology.com). Address correspondence to Jae-Hwan Choi, MD, Department of Neurology, Pusan National University School of Medicine, Research Institute for Convergence of Biomedical Science and Technology, Pusan National University Yangsan Hospital, Kumo-ro 20, Beomo-ri, Mulgum-eup, Yangsan, Gyeongnam 626-770, Korea; E-mail: [e-mail] Oh et al: J Neuro-Ophthalmol 2019; 39: 237-239 The patient was thought to have brainstem encephalitis and was treated with intravenous dexamethasone 15 mg/day for 3 days, followed by 60 mg of oral prednisolone/day and tapered over 1 month. Within 3 days, there was improvement in the left gaze palsy and adduction of the left eye. However, the SSPs were still observed in the right eye despite the improvement of adduction paresis in the left eye. The SSPs resolved 7 days later. Saccadic pulses are brief saccadic intrusions that consist of an initial saccade away from fixation followed by a return movement to the initial position without an intersaccadic interval (1). They may be SSPs or double saccadic pulses (DSPs) according to the nature of the returning eye movement (i.e., slow return vs saccade, respectively). Our patient developed saccadic pulses associated with the one-and-a-half syndrome from dorsal pontomedullary lesions. The pulse consisted of spontaneous bursts of abducting saccades followed by a slow return toward the initial position, consistent with SSPs. The movements were distinguished from DSPs or ocular flutter, which are composed of conjugate salvos of back-to-back saccades (1,2). Saccades are produced by burst-tonic firing patterns of ocular motor neurons. For horizontal saccades, burst neurons within the paramedian pontine reticular formation generate a pulse discharge to move the eye rapidly against orbital viscous forces. Subsequently, the neural integrator network including the nucleus prepositus hypoglossi and the medial vestibular nucleus yields a step discharge to sustain the eyes at a new position (1). If the step signal is lacking, the eyes return to the previous position in a decreasing velocity waveform. Omnipause neurons that lie in the paramedian caudal pons tonically inhibit the burst neurons to prevent unwanted spontaneous saccades. In our patient, spontaneous bursts of abducting saccades and a slow return with a decreasing velocity, suggest simultaneous dysfunction of omnipause neurons and neural integrator system. Because brain MRI showed widespread hyperintensities in the dorsal pons and medulla particularly on the left side, the structures for a horizontal gaze and the neural integrator may have been damaged. However, the lesions seem to spare the omnipause neurons that are located in the midline of caudal pons (1). We postulated that the SSPs in our patient may be due to damage to the inhibitory projection from the omnipause neurons to burst neurons rather than only the omnipause neurons. An intriguing finding in our patient was that SSPs occurred only in the right eye during disease course. Previously, monocular saccadic intrusions have been reported in patients with bilateral internuclear ophthalmoplegia (INO) (3,4). These 237 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Clinical Correspondence FIG. 1. Brain MRI. A. Contiguous axial fluid-attenuated inversion recovery image images show hyperintensities in the medulla and pons, particularly on the left side, extending into the cerebellum. B. Contiguous postcontrast T1 axial scans reveal enhancement in the dorsomedial pons (arrow). FIG. 2. Eye movement recordings. Velocity (A) and eye position (B) traces demonstrate bursts of abducting saccades of the right eye followed by a slow return toward the initial eye position. C. During a rightward saccade, the right eye demonstrates normal saccadic velocity followed by abducting nystagmus. The left eye shows a slow movement with a small range of adduction. RH, horizontal position of the right eye; LH, horizontal position of the left eye. 238 Oh et al: J Neuro-Ophthalmol 2019; 39: 237-239 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Clinical Correspondence patients have impaired fixation with sporadic bursts of monocular abducting saccades in each eye, and the adduction paresis due to the involvement of medial longitudinal fasciculus (MLF) might prevent conjugate adducting saccades of the fellow eye. Thus, the SSPs in bilateral INO are not actually monocular, but rather markedly disconjugate (4). However, the SSPs in our patient still occurred monocularly in the right eye during the resolution of horizontal gaze palsy. Also, one patient in a previous report showed monocular SSPs despite partially impaired adduction of the fellow eye (3). These findings indicate that true monocular saccadic intrusions can occur in brainstem lesions associated with bilateral INO. The underlying mechanism remains unclear, but it may be ascribed to the predominant loss or low-pass filtering of the high-frequency saccadic pulse command within the damaged MLF, leading to the absence of adducting saccades in the fellow eye (5,6). Indeed, INO due to demyelinating diseases can show a discrepancy between the involvement of saccades and other movements because demyelinating fibers cannot carry the high-frequency discharges required during the saccadic pulse but can sustain lower-frequency discharges that occur with slow movements Oh et al: J Neuro-Ophthalmol 2019; 39: 237-239 (1,5). Initially, our patient also showed a slow eye movement with a small amplitude in the left eye during a rightward saccade. The adduction paresis of the left eye improved after treatment, but the capacity to convey the high-frequency pulse discharges within the MLF may not be fully restored. This partial improvement might contribute to the maintenance of monocular SSPs during the recovery phase in our patient. The pathophysiology of monocular saccadic intrusion requires further investigation in other disorders. REFERENCES 1. Leigh RJ, Zee DS. The Neurology of Eye Movements. 5th edition. New York, NY: Oxford University Press, 2015. 2. Manta A, Ugradar S, Theodorou M. Ocular flutter after mild head trauma. J Neuroophthalmol. 2018;38:476-478. 3. Herishanu YO, Sharpe JA. Saccadic intrusions in internuclear ophthalmoplegia. Ann Neurol. 1983;14:67-72. 4. Otero-Millan J, Benavides DR, Zee DS, Kheradmand A, Bilateral INO. Unusual patterns of saccadic intrusions. Neurology. 2015;85:1428-1429. 5. Serra A, Liao K, Matta M, Leigh RJ. Diagnosing disconjugate eye movements: phase-plane analysis of horizontal saccades. 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