Vertical Head Thrusting in Acquired Supranuclear Vertical Ophthalmoplegia

Patients with congenital ocular motor apraxia (OMA) typically show head thrusts while attempting to shift gaze. In congenital OMA, this compensatory head motion mostly occurs in the horizontal plane. Two patients with acquired palsy of voluntary vertical gaze and continuous upward gaze deviation, one from aortic surgery and the other from multiple infarctions involving the mesodiencephalic junction, showed intermittent downward head thrusting to redirect the eyes straight ahead or downward. The head thrusting behavior improved markedly after surgical correction of the upward gaze deviation in one patient. Vertical head thrusting may be a characteristic sign of acquired vertical gaze palsy when combined with vertical gaze deviation.

Original Contribution Vertical Head Thrusting in Acquired Supranuclear Vertical Ophthalmoplegia Yeon-Hee Lee, MD, Seong-Hae Jeong, MD, Hyo-Jung Kim, PhD, Jeong-Min Hwang, MD, PhD, Woohyuk Lee, MD, Ji-Soo Kim, MD, PhD Abstract: Patients with congenital ocular motor apraxia (OMA) typically show head thrusts while attempting to shift gaze. In congenital OMA, this compensatory head motion mostly occurs in the horizontal plane. Two patients with acquired palsy of voluntary vertical gaze and continuous upward gaze deviation, one from aortic surgery and the other from multiple infarctions involving the mesodiencephalic junction, showed intermittent downward head thrusting to redirect the eyes straight ahead or downward. The head thrusting behavior improved markedly after surgical correction of the upward gaze deviation in one patient. Vertical head thrusting may be a characteristic sign of acquired vertical gaze palsy when combined with vertical gaze deviation. Journal of Neuro-Ophthalmology 2017;37:386-389 doi: 10.1097/WNO.0000000000000506 © 2017 by North American Neuro-Ophthalmology Society H ead thrusting during an attempt to shift a gaze is characteristic of congenital ocular motor apraxia (OMA) (1). In congenital OMA, this compensatory head motion changes the direction of gaze in the presence of voluntary gaze palsy and mostly occurs in the horizontal plane (1). Vertical head thrusting is rare in congenital OMA (2-5). In an acquired form of vertical ophthalmoplegia, Departments of Ophthalmology (Y-HL, WL) and Neurology (S-HJ), Chungnam National University College of Medicine, Daejeon, Korea; Research Administration Team, Seoul National University Bundang Hospital (H-JK), Seongnam, Korea; and Departments of Ophthalmology (J-MH) and Neurology (J-SK), Seoul National University College of Medicine, Seoul National University Bundang Hospital, Seongnam, 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 full text and PDF versions of this article on the journal's Web site (www. jneuro-ophthalmology.com). Address correspondence to Ji-Soo Kim, MD, PhD, Department of Neurology, Seoul National University College of Medicine, Seoul National University Bundang Hospital, 173-82 Gumi-ro, Bundang-gu, Seongnam-si, Gyeonggi-do 13620, Korea; E-mail: [e-mail] 386 we were able to find 2 reports (6,7) with this behavior when we searched the PubMed, PubMed Central, and MEDLINE databases in April 2016 using the following terms: head thrust, vertical oculomotor apraxia, OMA, vertical gaze palsy, vertical ophthalmoplegia, saccadic palsy, and saccades palsy. We describe 2 patients who showed vertical head thrusting to redirect the eyes straight ahead or downward in the presence of continuous upward eye deviation due to acquired supranuclear vertical ophthalmoplegia. CASE REPORTS Patient 1 A 31-year-old man underwent surgery for traumatic aortic dissection. He did not have any neurologic symptoms or signs before surgery. Postoperatively, the patient showed altered mental status and anxiety. Five days after surgery, the medical staff noted abnormal eye stability, and 7 days later, he began to report difficulty directing gaze downward and showed upward eye deviation with a chin-down posture. Brain MRI revealed multifocal microhemorrhages in the subcortical portions of left superior frontal gyrus, right thalamus, pons, and left inferior cerebellar hemisphere. A few weeks later, he began to thrust his head downward repeatedly. Approximately 3 years after surgery, neuro-ophthalmic examination showed slow horizontal saccades and absence of spontaneous and volitional vertical saccades. Smooth pursuit appeared normal in both horizontal directions but impaired vertically (see Supplemental Digital Content, Videos 1 and 2, http://links.lww.com/WNO/A223 and http://links.lww.com/WNO/A224). Optokinetic (OKN) stimulation evoked normal responses horizontally. However, vertical OKN produced deviation of the eyes in the direction of stimulation but without corrective saccades. Passive head rotation while fixating on a stationary target Lee et al: J Neuro-Ophthalmol 2017; 37: 386-389 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution induced full ranges of eye movements in both horizontal and vertical directions (see Supplemental Digital Content, Videos 1 and 2, http://links.lww.com/WNO/A223 and http://links.lww.com/WNO/A224). Bell phenomenon was normal in both eyes. The patient showed continuous upward deviation of the eyes and intermittent downward thrusting of the head to redirect the eyes straight ahead or downward (see Supplemental Digital Content, Video 3, http://links.lww.com/WNO/A225). He tended to tilt his head backward after each vertical head thrust and tried to keep the eyes in downgaze during attempted fixation. This seemed to be a strategy to extend the duration of fixation after each vertical head thrust. Other neurologic findings included dysarthria and ataxia. The head thrusting behavior had improved markedly 8 years later. Patient 2 A 61-year-old man was referred for management of vertical ophthalmoplegia and strabismus because of top of the basilar syndrome which occurred 2 years previously. He had a history of hypertension, hypertrophic cardiomyopathy, paroxysmal atrial flutter, and chronic kidney disease. Initially, he showed complete bilateral ptosis and upward and outward deviation of the eyes on manual opening of the eyelids, which had improved over the following year but had been stationary since then. Examination showed bilateral partial ptosis, decreased pupillary reaction to light in both eyes, and upward and outward deviation of both eyes, more so in the left eye (Fig. 1). He could not voluntarily move his eyes downward but limited ranges of vertical eye movements were elicited during vertical head oscillation (see Supplemental Digital Content, Video 4, http://links. lww.com/WNO/A226). Adduction was limited in both eyes, and the right eye showed complete abduction palsy. The patient would intermittently thrust his head downward, which moved his eyes temporarily into primary gaze, but his eyes would then spontaneously deviate upward (see Supplemental Digital Content, Video 4, http://links.lww. com/WNO/A226). The remainder of the neurologic examination was unremarkable except for left hemiparesis. Brain MRI demonstrated multiple infarctions, involving both medial thalami, midbrain tegmentum, right superior cerebellar peduncle (Fig. 2). There also were infarctions involving the left occipital lobe and both cerebellar hemispheres. MRA revealed occlusion of the left distal vertebral artery and atherosclerotic change at the right proximal internal carotid artery. After surgical correction of the ocular deviation with recession of both superior and inferior recti, the patient had a left exotropia of 20-prism diopters and a left hypertropia of 10-prism diopters. Also, he reported improved gaze control. DISCUSSION Our patients with acquired vertical ophthalmoplegia and upward gaze deviation showed intermittent downward head thrusting to redirect the eyes straight ahead or downward. Head thrusting is a characteristic sign of congenital OMA (1). Even although mostly horizontal, a few cases of vertical head thrusts have also been described in congenital OMA associated with perinatal hypoxia in the presence of normal horizontal eye motion (2-5). Patients with congenital OMA use head thrusting to shift their gaze toward a new point of interest (1). The patients thrust their head in the direction of the intended target and then move their head back to face the target after obtaining fixation of the target. In contrast, our patients adopted downward head thrusting to maintain the gaze straight ahead in the setting of constant upward gaze deviation. This type of vertical head thrusts has not been described in patients with acquired palsy of voluntary vertical saccades or smooth pursuit in the presence of preserved vestibulo-ocular reflex. FIG. 1. Patient 2. There is bilateral ptosis, upward and outward deviation of the eyes, more severe in the left eye, complete vertical ophthalmoplegia, bilateral adduction palsy, and abduction limitation of the right eye. Lee et al: J Neuro-Ophthalmol 2017; 37: 386-389 387 Copyright © North American Neuro-Ophthalmology Society. Unauthorized reproduction of this article is prohibited. Original Contribution FIG. 2. Patient 2. Axial diffusion-weighted imaging shows acute infarctions involving the dorsal pons (A), midbrain tegmentum (B), and both medial thalami (C). Our first patient had a syndrome of saccadic palsy after cardiac and aortic surgeries (8,9). This syndrome is characterized by palsy of both voluntary and reflexive saccades. However, other eye movements including smooth pursuit, vergence, and the vestibulo-ocular reflex are mostly spared (9). It may include horizontal head thrusts to improve the range and speed of a gaze shift. In one report, one of the 3 patients with acquired OMA after aortic surgery showed head thrusts in both horizontal and vertical directions during refixation (7). The pathophysiology of acquired OMA after aortic or cardiac surgery remains to be elucidated. Neuroimaging studies have failed to detect any relevant abnormalities (10), and autopsy findings are suggestive of damage to the excitatory burst or omnipause neurons in the brainstem (11,12). One report documented severe loss or fragmentation of the perineuronal nets surrounding the intact excitatory burst neurons and omnipause neurons in a patient who developed permanent selective saccadic palsy after cardiac surgery (9). Our second patient developed both horizontal and vertical ophthalmoplegia and upward deviation of the eyes from multiple infarctions involving bilateral medial thalami, mesodiencephalic junction, and cerebellum. The mesodiencephalic junction contains the rostral interstitial nucleus of the medial longitudinal fasciculus, the interstitial nucleus of Cajal, the mesencephalic reticular formation, and the posterior commissure, which are involved in the premotor neuron control of eye movements (13). These structures are primarily supplied by the paramedian thalamic- mesencephalic arteries. In previous reports, patients with vertical head thrusts from vertical ophthalmoplegia showed bilateral involvement of the mesodiencephalic junction due to congenital or acquired lesions (4-6). Given the complete palsy of saccades (Patient 1) and voluntary eye movements (Patient 2) in both upward and downward directions, the continuous upward deviation of the eyes seems unusual in our patients. Previously, upward gaze deviation has been described in comatose 388 patients after resuscitation and has been ascribed to diffuse cerebrocerebellar damage, sparing the brainstem (14). All patients with postresuscitation vertical gaze deviation showed cerebellar lesions on diffusion-weighted MRI (8). The upward deviation was explained by loss of inhibitory inputs from the cerebellum to the brainstem anterior semicircular canal projections for the upward vestibulo-ocular reflex, which would lead to an upward bias in a static eye position. STATEMENT OF AUTHORSHIP Category 1: a. Conception and design: Ji-Soo Kim; b. Acquisition of data: Yeon-Hee Lee, Jeong-Min Hwang, Woohyuk Lee, and SeongHae Jeong; c. Analysis and interpretation of data: Yeon-Hee Lee. Category 2: a. Drafting the manuscript: Yeon-Hee Lee and SeongHae Jeong; b. Revising it for intellectual content: Hyo-Jung Kim, JiSoo Kim, and Yeon-Hee Lee. Category 3: a. Final approval of the completed manuscript: Ji-Soo Kim. REFERENCES 1. Cogan DG. A type of congenital ocular motor apraxia presenting jerky head movements. Am J Ophthalmol. 1953;36:433-441. 2. Ro A, Gummeson B, Orton RB, Cadera W. 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