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Show Journal of Neuro- Ophthalmology 18( 1): 43- 46, 1998. © 1998 Lippincoll- Ravcn Publishers, Philadelphia Saccadic Ping- Pong Gaze Ken Johkura, M. D., Atsushi Komiyama, M. D., Mari Tobita, M. D., and Osamu Hasegawa, M. D. Ping- pong gaze ( PPG), or short- cycle periodic alternating gaze, consists of horizontal conjugate ocular deviations alternating every few seconds. This alternating gaze has been described as appearing to be smooth. However, our electrooculographic study of four consecutive unconscious patients with PPG showed smooth waveforms in one patient but saccadic cog-wheeling in three patients. In one of the three patients with saccadic PPG, a transition from smooth to saccadic waveforms was noted with clinical improvement. Whereas the patient with smooth PPG died immediately, the patients with saccadic PPG survived in a persistent vegetative state. These findings suggest that saccadic PPG is a clinical variant of PPG in patients in a lighter state of consciousness, possibly related to less extensive brain damage. Key Words: Ping- pong gaze- Short- cycle periodic alternating gaze- Saccadic ping- pong gaze- Electrooculography. Ping- pong gaze ( PPG), or short- cycle periodic alternating gaze, is an abnormal eye movement characterized by spontaneous alternating conjugate horizontal movements ( 1- 7). PPG is usually seen in unconscious patients with bilateral impairment of the cerebral hemispheres and implies that brain stem function is relatively intact ( 1- 5). In previous reports, this alternating gaze has been described as a smooth movement without saccadic components ( 3,6). Electrooculographic studies to date have substantiated the smooth waveforms of PPG ( 5,8,9). We present here the first demonstration of saccadic PPG verified by electrooculography in three patients and compare these findings with those from a patient with typical smooth PPG. METHODS Eye Movement Recordings Eye movements of patients 1- 4 were recorded with AC electrooculography ( time constant = 16 s). The am- Manuscript received August 18, 1997. From the Department of Neurology, Urafune Hospital, Yokohama City University School of Medicine, Yokohama, Japan ( K. J., M. T.); and Department of Neurology, Yokohama City University School of Medicine, Yokohama, Japan ( A. K., O. H.). Address correspondence and reprint requests to Dr. Ken Johkura, Department of Neurology, Urafune Hospital, Yokohama, City University School of Medicine, 3- 46 Urafune- cho, Minami- ku, Yokohama 232, Japan. plitudes of the eye movements were calibrated using Hir-schberg's corneal reflection test ( 5,10). Spontaneous eye movements, oculocephalic responses elicited by passive head rotation, and cold caloric responses were recorded. The velocities and saccadic waveforms of the eye movements were analyzed only in patient 3 because only his eye movements were recorded with sufficient resolution to permit such analysis. CASE REPORT Patient 1 A 20- year- old man was referred to our hospital because of a severe head injury. On arrival he was in a deep coma. Brain computed tomography ( CT) showed bilateral cerebral hemisphere contusions with severe swelling. Despite emergency treatment with surgical decompression, the patient remained in a comatose state, with equal and reactive pupils, and flaccid and areflexic extremities. His eyes did not oscillate at that time. Two weeks after admission, although he remained comatose, the patient developed decorticate posturing. Pupillary and corneal reflexes were normal. He showed symmetrically increased deep tendon reflexes and extensor plantar responses. At this stage, slow, spontaneous, conjugate horizontal eye movements were recognized when the eyelids were raised. A full excursion from left to right gaze took 1.5 s, and then the eyes reversed direction ( Fig. 1, Table 1). These movements were saccadic in nature ( Fig. 2A). Oculocephalic responses were present in both the horizontal and vertical directions. With cold caloric stimulation, after a latent period of ~ 10 s, the eyes deviated to the irrigated side and remained there for a few seconds. Then nystagmus with the slow phase directed to the irrigated side appeared and lasted approximately 2 min. A follow- up brain CT demonstrated the bilateral cerebral contusions but no brain stem abnormalities. Auditory brain stem evoked potentials ( ABEPs) were normal. Six weeks after admission, the horizontal saccadic alternating gaze disappeared. The patient remained in a persistent vegetative state. Patient 2 A 65- year- old man was admitted because of a disturbance in consciousness. He had Parkinson's disease treated with levodopa and dopamine agonists for 12 43 44 K. JOHKURA ETAL. vi £ ^ ;.!, i • i. • -* • far )& K ' « £ , FIG. 1. Saccadic ping- pong gaze in patient 1. Eyes deviated conjugately from one side to the opposite side. years. For 2 months before admission, he had convulsions several times a day. Seven hours before admission, he developed status epilepticus. On arrival he showed decerebrate posturing in response to painful stimuli, although he had no convulsions. His pupils were round and reactive. He showed slightly increased deep tendon reflexes and extensor plantar responses. Brain CT disclosed no abnormalities; electroencephalography showed diffuse low- voltage fast activity without epileptiform discharges. Both eyes moved conjugately in a saccadic fashion from one lateral position to the other, each cycle lasting - 3 s ( Table 1). This saccadic alternating gaze continued for 5 days. Oculocephalic responses were present in both the horizontal and vertical directions. With cold caloric stimulation, after a latent period of - 10 s, the eyes deviated to the irrigated side with nystagmus with the slow phase toward the irrigated side for ~ 1 min. He continued in a persistent vegetative state. Patient 3 This 67- year- old man suddenly lost consciousness, presumably due to ventricular fibrillation. Cardiopulmonary resuscitation was successful. Four days after admission, neurologic examination showed that he was still in a comatose state with intact brain stem reflexes. A brain CT showed no abnormal findings, and ABEPs were elicited with normal latencies. When the eyes were opened, slow, spontaneous, conjugate horizontal eye movements were noticed. Both eyes moved smoothly and rhythmically from one extreme lateral position to the other, taking - 2 s ( Fig. 2B, top; Table 1). One week after admission, saccadic components were occasionally superimposed upon smooth alternating gaze movements. These saccadic gaze movements consisted of rapid phases that were directed toward the gaze deviation and centripetally directed small slow phases. The velocities of rapid phases ranged from 60 to 100 deg/ sec. The frequency of the alternating saccadic deviation was the same as that of the smooth deviation, but the amplitude was smaller than that of the smooth deviation ( Fig. 2B, middle). With clinical improvement, the smooth alternating gaze deviation shifted permanently to the saccadic movement ( Fig. 2B, bottom). Oculocephalic responses were present in both the horizontal and vertical directions. With cold caloric stimulation, the eyes deviated tonically to the irrigated side for - 90 s, and then the periodic alternating gaze resumed with increasing amplitude until the original oscillation was restored. The patient remained in a persistent vegetative state and responded only to painful stimuli. Two weeks after admission, the horizontal saccadic alternating gaze disappeared. Patient 4 This 68- year- old man was referred to our hospital because of rapidly progressing disturbed consciousness. Two years earlier, the patient had undergone incomplete surgical removal of a prostatic cancer and was treated by irradiation. One day before admission, he complained of nausea and general fatigue, gradually followed by a decrease in alertness. On arrival, he failed to respond to painful stimuli and manifested hemoptysis, hematuria, and bleeding from gingiva. Laboratory examinations showed severe liver dysfunction with disseminated intravascular coagulation ( DIC). A brain CT was unremarkable. Pupils were equal and round and reacted normally to light; corneal reflexes were intact. He showed normal deep tendon reflexes and extensor plantar responses. When his eyes were opened, both moved smoothly and conjugately from one extreme side to the other, requiring 2 to 2.5 s ( Fig. 2C, Table 1). Oculocephalic responses were present both in the horizontal and vertical directions. Smooth periodic alternating gaze continued during head rotation. With cold caloric stimulation, after a latent period of - 10 s, the eyes deviated to the irrigated side and remained there for - 20 s. The patient died 5 h after admission. DISCUSSION Fisher in 1967 ( 1) described an unconscious patient with bilateral cerebral hemisphere infarction whose eyes moved slowly from one horizontal extreme lateral position to the other. Senelick ( 6) christened such an eye movement abnormality as PPG. Several investigators ( 2, 3,8,11) have reported similar eye movements characterized by short- cycle, spontaneous, alternating conjugate deviation in comatose patients. Although similar eye movements have been reported in a patient with a posterior fossa hemorrhage ( 6), PPG is considered to be a ./ Neuro- Ophthalmol, Vol. 18. No. 1, 1998 SACCADIC PING- PONG GAZE 45 TABLE 1. Clinical data of the patients Patient Eye movement Cycle ( sec) Amp ( degrees) Calorics Etiology Outcome 1 2 3 4 SPPG SPPG PPG -> SPPG PPG 3 3 4 4 - 5 25 30 45H> 25 60 Nystagmus with quick phase Nystagmus with quick phase Tonic deviation" Tonic deviation Contusion Vegetative Hypoxia Vegetative Hypoxia Vegetative D1C Death SPPG = saccadic ping- pong gaze; PPG = ping- pong gaze; DIC " Caloric test was conducted during the SPPG stage. disseminated intravascular coagulation. sign of bilateral cerebral hemisphere impairment ( 1- 4,8,11) or bilateral disconnection of the cerebrum from the brain stem ( 12) and is usually seen in unconscious patients. Our four patients showed these neuroophthal-mologic features characteristic of PPG. Periodic alternating gaze deviations also may exhibit a long cycle ( 13- 15); the eyes remain tonically deviated for 1- 2 min before shifting to the opposite side. This eye movement is thought to represent periodic alternating nystagmus ( PAN) without the rapid phases ( 5,13- 15) 3 sec. 3 sec. and is reported in patients with posterior fossa lesions ( 13- 15). The eye movements seen in our patients are distinct from PAN because of the short alternating cycles. Clinically, PPG has been described as smooth movements ( 2,3,6). Recent oculographic studies have demonstrated smooth waveforms with PPG ( 5,8,9). In contrast, our oculographic study showed saccadic waveforms in patients 1- 3. These waveforms had the following features: ( a) the amplitude of the eye deviations were smaller than that of smooth PPG; ( b) the horizontal eye deviations consisted of rapid phases that were directed toward the eye deviation and centripetally directed small slow phases; and ( c) the velocities of rapid phases ranged from 60 to 100 deg/ sec. A transition from smooth to saccadic waveforms was associated with clinical improvement in patient 3. Similar cogwheeling was induced by painful stimuli in an another reported patient with smooth PPG ( 5). Caloric testing evoked nystagmus in two of the three patients with saccadic PPG. The patients with saccadic PPG continued to live in a persistent vegetative state, whereas the patient with smooth PPG died immediately after admission. Although the precise mechanisms of smooth and saccadic PPG are unknown, these findings suggest that saccadic PPG is a clinical variant of PPG and that patients with saccadic PPG are in a lighter state of consciousness possibly related to less extensive brain damage than those with smooth PPG. Acknowledgment: We thank Dr. David S. Zee ( Johns Hopkins University, Baltimore, MD) for critically reviewing the manuscript. FIG. 2. Electrooculographic recording from patients 1, 3, and 4. A: The alternating gaze of patient 1 had a cogwheeling quality associated with saccadic components ( saccadic ping- pong gaze [ PPG]). B: In patient 3, at the beginning of the clinical course, the eyes moved smoothly from one extreme lateral position to the other ( top). One week later, saccadic components were occasionally superimposed upon smooth PPG, with the same frequency and reduced amplitude ( middle). Then the smooth PPG shifted permanently to saccadic PPG following clinical improvement ( bottom). 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