Kim, Eui-Jung MD; Oh, Sun-Young MD; Choi, Ha-Cheol MD; Shin, Byoung-Soo MD; Seo, Man-Wook MD; Choi, Jong-Bum MD
Departments of Neurology (E-JK, S-YO, H-CC, B-SS, M-WS) and Chest Surgery (J-BC), School of Medicine, Chonbuk National University, Jeonju, South Korea.
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 Sun-Young Oh, MD, PhD, Department of Neurology, Chonbuk National University Hospital, Gumam-dong, Jeonju, South Korea; E-mail: email@example.com
We report a patient who showed a selective deficit of voluntary saccades and quick phases of nystagmus after cardiac surgery. Voluntary saccades in the horizontal plane were very slow, while vertical saccades, vestibular and optokinetic nystagmus, were absent. However, smooth pursuit, the vestibulo-ocular reflex, and the ability to hold steady eccentric gaze were preserved.
To maintain optimal visual acuity, we use voluntary saccades to move the eyes rapidly from one point of visual fixation to the next (1). Loss of voluntary saccades may occur with brainstem strokes, although other types of eye movements are usually affected. Cases of selective saccadic palsy as a complication of cardiac surgery have been previously described (2-4). However, the pathogenesis of the disorder is unclear, and few reports have clearly defined the nature of the ocular motor deficit. Here, we report a patient with selective saccadic palsy after a cardiac operation and characterize and quantify the defect of the ocular motor disorder.
A 43-year-old man with chest pain underwent repair of an aortic dissection. The procedure was complicated by massive bleeding. On awakening from anesthesia, the patient had difficulty shifting his gaze and complained of vertical diplopia in primary position, which worsened in downward gaze. He also had difficulty walking because of an inability to alter his direction of gaze voluntarily.
On neurologic examination, the patient was alert and fully oriented. He had no dysarthria or dysphagia. He showed mild dysmetria of upper extremities and truncal ataxia with a tendency to fall.
Abnormalities on neuro-ophthalmic examination were limited to his eye movements. The patient had a right hypertropia, worse on looking down and to his left. Three-dimensional recording of eye motion with oculography (SMI, Teltow, Germany) was performed (see Video, Supplemental Digital Content 1, http://links.lww.com/WNO/A8). Horizontal and vertical saccades were profoundly slowed and hypometric. Optokinetic responses were absent. However, smooth pursuit, vergence, horizontal and vertical VOR, and the ability to hold the eye in an eccentric position were preserved. Eye movements and the ability to hold steady gaze were evaluated during attempted fixation of visual targets located centrally or eccentrically (±30° horizontally and ±20° vertically). There was no spontaneous or gaze-evoked nystagmus. Horizontal saccades were generated by a target moving pseudorandomly on a light bar with a range of ±16.7°. The range of target amplitude was 5°-30°. The patient had slowed and hypometric voluntary horizontal saccades (Fig. 1). Vertical saccades were completely paralyzed. Quick phases of nystagmus (reflexive saccades) were also reduced or absent during optokinetic nystagmus. Smooth pursuit (Fig. 1) and vergence eye movement were preserved. The vestibulo-ocular reflex (VOR), evaluated during passive or active head rotations, was normal in the horizontal and vertical planes while optokinetic stimuli elicited no horizontal or vertical movements (see Video, Supplemental Digital Content 1, http://links.lww.com/WNO/A8).
Bithermal caloric tests showed bilateral weak responses (less than 4° per second) (Fig. 2). Sinusoidal harmonic accelerations (peak velocity: 50° per second; frequency range: 0.02-0.32 Hz) showed decreased gains of the VOR and visual-enhanced VOR.
No brainstem abnormalities were detected on MRI (Fig. 3). Somatosensory and brainstem auditory-evoked potentials and audiogram were normal.
During 2 years of follow-up, our patient experienced no improvement in either his saccadic palsy or his truncal ataxia with gait instability.
Our patient showed abnormalities of saccades and quick phases of nystagmus including slowing, hypometria, and limited range. In contrast, smooth pursuit, VOR, vergence, and the ability to hold the eye in an eccentric position were preserved. Review of several anatomic structures within the brainstem may help explain this dichotomy. Premotor burst neurons and omnipause neurons lie within the reticular formation of the brainstem. Excitatory burst neurons generating horizontal saccades are located in the paramedian pontine reticular formation (PPRF), at the level of the abducens nuclei, and extend rostrally (1,5). Experimental bilateral lesions in the PPRF selectively abolish horizontal saccades, leaving other eye movements intact (6). Excitatory burst neurons for vertical and torsional saccades and quick phases are located in the rostral interstitial nuclei of the median longitudinal fasciculus (riMLF) (1,7). Bilateral lesions of riMLF abolish vertical and torsional rapid eye movements (8). However, it would be difficult to conceive a process causing selective impairment of burst neurons for horizontal and vertical saccades located in the pons and midbrain.
The omnipause neurons (OPNs) are another important component of the brainstem saccade generator and lie close to the midline in the raphe interpositus nucleus (1,9). OPNs are glycinergic and project to burst neurons in both the pontomedullary reticular formation, which directly controls horizontal fast eye movements, and the riMLF, which contains vertical eye movement-related burst neurons. OPNs are tonically active and make inhibitory connections with burst neurons directly controlling motoneurons for vertical and horizontal eye movements but pause before saccades in any direction. Chemical lesions of OPNs cause saccades to become slow (10). Recently, it has been proposed that OPNs also have a neuromodulatory function, to increase the responsiveness of saccade-related neurons when they receive a trigger signal (11-13). Therefore, the effect of OPNs on burst neurons may be 2-fold: inhibition when no saccade is planned, but enhancement of glutaminergic mechanisms when a saccade is triggered. So, a possible explanation of selective saccadic palsy in our patient is that OPNs might be damaged, in which case, both horizontal and vertical saccades would be expected to be slow.
The small vertical deviation in our patient suggests that structures adjacent to the brainstem reticular formation concerned with saccade generation may also have been affected. Yet, the pathogenesis of our patient's mild dysmetria and gait instability remains unclear. These findings could be explained by cerebellar damage as would decreased saccadic acceleration and deceleration and saccadic hypometria (14). However, MRI failed to demonstrate any abnormalities of the cerebellum.
It is likely that ischemia to the brainstem reticular formation was responsible for saccadic palsy in our patient. Hypotension, intraoperative hypothermia, or microemboli are all potential contributing factors (2). Over a 2-year period, our patient showed no clinical improvement. This is consistent with other reports that patients with this ocular motor disorder may remain permanently visually disabled after cardiac surgery (2,3).
1. Leigh RJ,
Zee DS. The Neurology of Eye Movements. New York, NY: Oxford University Press, 2006.
2. Solomon D,
Ramat S, Tomsak RL, Reich SG, Shin RK, Zee DS, Leigh RJ. Saccadic palsy after cardiac surgery: characteristics and pathogenesis. Ann Neurol. 2008;63:355-365.
3. Eggers SDZ,
Moster ML, Cranmer K. Selective saccadic palsy after cardiac surgery. Neurology. 2008;70: 318-320.
4. Hanson MR,
Hamid MA, Tomsak RL, Chou SS, Leigh J. Selective saccadic palsy caused by pontine lesions: clinical, physiological, and pathological correlations. Ann Neurol. 1986;20:209-217.
5. Horn AKE,
Büttner-Ennever JA, Suzuki Y, Henn V. Histological identification of premotor neurons for horizontal saccades in monkey and man by parvalbumin immunostaining. J Comp Neurol. 2004;359:350-363
6. Henn V,
Lang W, Hepp K, Reisine H. Experimental gaze palsies in monkeys and their relation to human pathology. Brain. 1984;107:619-636.
7. Horn AKE,
Büttner-Ennever JA. Premotor neurons for vertical eye movements in the rostral mesencephalon of monkey and human: histologic identification by parvalbumin immunostaining. J Comp Neurol. 1998;392:413-427.
8. Suzuki Y,
Büttner-Ennever JA, Straumann D, Hepp K, Hess BM, Henn V. Deficits in torsional and vertical rapid eye movements and shift of Listing's plane after uni- and bilateral lesions of the rostral interstitial nucleus of the medial longitudinal fasciculus. Exp Brain Res. 1995;106:215-232.
9. Büttner-Ennever JA,
Cohen B, Pause M, Fries W. Raphe nucleus of the pons containing omnipause neurons of the oculomotor system in the monkey, and its homologue in man. J Comp Neurol. 2004;267:307-321.
10. Kaneko CRS.
Effect of ibotenic acid lesions of the omnipause neurons on saccadic eye movements in Rhesus macaques
. J Neurophysiol. 1996;75:2229-2242.
11. Miura K,
Optican LM. Membrane channel properties of premotor excitatory burst neurons may underlie saccade slowing after lesions of omnipause neurons. J Comp Neurol. 2006;20:25-41.
12. Ramat S,
Leigh RJ, Zee DS, Optican LM. What clinical disorders tell us about the neural control of saccadic eye movements. Brain. 2007;130:10-35.
13. Ahmadi S,
Muth-Selbach U, Lauterbach A, Lipfert P, Neuhuber WL, Zeilhofer HU. Facilitation of spinal NMDA receptor currents by spillover of synaptically released glycine. Science. 1998;300:2094-2097.
14. Takagi M,
Zee DS, Tamargo RJ. Effects of lesions of the oculomotor vermis on eye movements in primate: saccades. J Neurophysiol. 1998;80:1911-1931.
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