Expanding the Spectrum of Ocular Dipping With Ping-Pong Gaze

Photo and Video Essay Expanding the Spectrum of Ocular Dipping With Ping-Pong Gaze Julie C. Gudenkauf, MD, Arens Taga, MD, Jiaying Zhang, MD, Daniel Gold, DO FIG. 1. A. Computed tomography of head (sagittal view) showing diffuse intraventricular hemorrhage and hydrocephalus. B– D. Images of the brain MRI from left to right: diffusion weighted imaging (DWI), fluid attenuated inversion recovery (FLAIR), and susceptibility weighted imaging (SWI). DWI shows multifocal ischemic infarcts, which are believed to be in the setting of infectious vasculopathy. A 51-year-old man was initially admitted for a hypertensive left thalamic intracerebral hemorrhage (ICH) later complicated by intraventricular hemorrhage (IVH) (Fig. 1) and hydrocephalus requiring extraventricular drain (EVD) placement. He subsequently developed iatrogenic bacterial meningitis (Gram stain and culture negative) and, in this setting, numerous bihemispheric punctate ischemic strokes with minimal infratentorial involvement (Fig. 1). Notably, the brainstem was spared on neuroimaging, and brainstem reflexes were intact including normal horizontal and vertical vestibulo-ocular reflexes (VOR). After extensive workup, these strokes were felt to be because of an infectious vasculopathy from his meningitis. His initial neurologic examination after the ICH with IVH was characterized by persistent unresponsiveness with decerebrate posturing. Approximately 2 weeks into the clinical course, and 3 days after the multifocal strokes were identified on MRI, he developed slow conjugate downward movements resembling ocular dipping and slow horizontal roving eye movements, consistent with the smooth pursuit subtype of ping-pong gaze (Video 1). These eye movements were not provoked by examination maneuvers including noxious stimulation or passive limb movements. The remainder of his cranial nerve examination was unremarkable. Diagnostic work-up included continuous electroencephalogram (EEG) monitoring that was negative for seizures and showed bihemispheric and relatively symmetric slowing, intracranial pressure (ICP) monitoring was without significant fluctuations, and infectious and toxic–metabolic laboratory studies that were unremarkable. INTERPRETATION OF FINDINGS © 2024 by North American Neuro-Ophthalmology Society The clinical finding of slow, conjugate downward movements followed by rapid return to midposition has been previously described in the literature as inverse bobbing or ocular dipping (OD).1 The movements in OD contrast with ocular bobbing (OB), which consists of an initial downward movement of the eyes followed by a slow return to midposition. OD has been reported in the setting of anoxic brain injury,1 with only isolated reports of cases in status epilepticus, prion disease, encephalopathy because of hemiplegic migraine, Wernicke encephalopathy, and anti-N-methyl-D-aspartate (NMDA) receptor encephalitis.2,3 Slow, conjugate, horizontal roving eye movements that alternate every few seconds are known as ping-pong gaze (PPG).4 Two subtypes have been recognized, based on their resemblance to normal smooth pursuit or saccadic eye movements.4,5 The “smooth pursuit” subtype, which is the most Gudenkauf et al: J Neuro-Ophthalmol 2024; 44: e501-e502 e501 Department of Neurology, Johns Hopkins University, Baltimore, Maryland. The authors report no conflicts of interest. J. C. Gudenkauf and A. Taga contributed equally to the work. Please follow this link to view Video 1: https://journals.lww.com/ jneuro-ophthalmology/fulltext/9900/expanding_the_spectrum_of_ ocular_dipping_with.531.aspx Address correspondence to Daniel Gold, DO, Department of Neurology, Johns Hopkins University, 600 N. Wolfe Street, Baltimore, MD 21287; E-mail: [e-mail] doi: 10.1097/WNO.0000000000002063 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Photo and Video Essay common, consists of slow, horizontal, conjugate, smooth movements. The “saccadic” subtype is characterized by superimposed small saccadic movements. PPG has been reported in the setting of supratentorial lesions, mainly infarctions or hemorrhages, affecting the bilateral hemispheres, the bilateral basal ganglia, the bilateral cerebral peduncles, or the ventral pons.4,5 The exact mechanism and localizing value of OD remains unclear, in contrast to OB, which is classically associated with pontine dysfunction affecting horizontal gaze centers. The observation that the horizontal VOR remains intact in patients with OD, and that OD frequency and intensity are influenced by arousal patterns, suggests at least some degree of intact pontine function in these patients.1,2 Furthermore, the co-occurrence of pingpong gaze in our patient suggests sparing of pontine horizontal gaze centers. One hypothesis1 is that OD could be because of the release of the vertical gaze centers at the thalamo-mesencephalic junction (including the rostral interstitial nucleus of medial longitudinal fasciculus and the interstitial nucleus of Cajal) from inhibitory supratentorial control. Given the time course and the appearance of these abnormalities after multifocal ischemic strokes, we hypothesize that these vertical gaze connections were compromised by bihemispheric lesions. This seems more likely than direct injury to brainstem vertical gaze centers, especially given preserved cranial nerve reflexes on serial examinations, including vertical VOR and pupillary reflex. The quick upward phase after the downward dipping movement was lacking in our patient, presumably because of at least some degree of dorsal midbrain compression related to the hydrocephalus and IVH. Similarly, a proposed pathophysiologic mechanism of PPG is the disconnection of supratentorial gaze centers from a relatively intact brainstem, with release of the paramedian pontine reticular formation from inhibitory supranuclear control.4 The saccadic appearance may indicate less extensive lesions, with sparing of the corticobulbar pathways controlling the saccadic eye movements.5 e502 The prognostic significance of ocular dipping and pingpong gaze remains to be understood, with reports of both positive and negative patient outcomes.3,4 In our patient, over the course of his prolonged hospitalization of 3 months, the movements persisted. The patient has not experienced any significant improvement in his overall neurological status. In conclusion, our case extends the spectrum of potential causes of ocular dipping to include multifocal supratentorial lesions, in addition to the previously described more diffuse and symmetric bihemispheric processes. The co-occurrence of OD and PPG in our patient suggests that the disconnection of supratentorial gaze centers from a relatively intact brainstem may be a common mechanism for both abnormalities. STATEMENT OF AUTHORSHIP Conception and design: J. C. Gudenkauf1, A. Taga, J. Zhang, D. Gold; Acquisition of data: J. C. Gudenkauf1, A. Taga, J. Zhang, D. Gold; Analysis and interpretation of data: J. C. Gudenkauf1, A. Taga, J. Zhang, D. Gold. Drafting the manuscript: J. C. Gudenkauf1, A. Taga, J. Zhang, D. Gold; Revising the manuscript for intellectual content: J. C. Gudenkauf1, A. Taga, J. Zhang, D. Gold. Final approval of the completed manuscript: J. C. Gudenkauf1, A. Taga, J. Zhang, D. Gold. REFERENCES 1. Jeanneret V, Beach PA, Kase CS. Ocular dipping in anoxic brain injury. JAMA Neurol. 2019;76:1252. 2. Sierra-Hidalgo F, Llamas S, Gonzalo JF, Sánchez Sánchez C. Ocular dipping in Creutzfeldt-Jakob disease. J Clin Neurol. 2014;10:162–165. 3. Gray IN, Cristancho AG, Licht DJ, Liu GT. Ocular dipping in a patient with hemiplegic migraine. J Pediatr Ophthalmol Strabismus. 2018;55:e4–e6. 4. Yang SL, Han X, Guo CN, Zhu XY, Dong Q, Wang Y. A closer look at ping-pong gaze: an observational study and literature review. J Neurol. 2018;265:2825–2833. 5. Sotiriou K, Artemiadis AK, Papanastasiou I. Ping-pong gaze in a patient with bilateral hemispheric ischemic stroke: case report and video. J Stroke Cerebrovasc Dis. 2015;24:e67–e68. Gudenkauf et al: J Neuro-Ophthalmol 2024; 44: e501-e502 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited.