Epileptic Nystagmus Joseph M. R. Furman, MD, PhD,"t Patricia K. Crumrine, MD,tS and Oscar M. Reinmuth, M D t
We report a 52-year-old woman with episodes of vertigo accompanied by right beating nystagmus and left posterior temporoparietal sharp waves and spikes on electroencephalogram without change in level of consciousness. Electrooculography demonstrated that the episodes of nystagmus were not preceded by gaze deviation and that nystagmus slow component velocities were linear. This patient's epileptic nystagmus may have been the result of excitation of cerebral ocular pursuit pathways. Furman JMR, Crumrine PK, Reinmuth OM. Epileptic nystagmus. Ann Neurol 1990;27:686-688
Accurate measurement of eye position during epileptic nystagmus is available in the English literature for only a single patient 111. Other reports of eye movements during seizures are limited to clinical observation or eye position records made with electroencephalographic (EEG) equipment 12-7}, which does not allow for proper assessment of nystagmus slow component velocity. Such information is critical for a determination of the underlying pathophysiology of epileptic nystagmus. We report a patient with epileptic nystagmus whose slow component velocities were linear, a finding not previously described. Also of interest is that our patient did not lose consciousness, a previously reported 17-91 but unusual feature of epileptic nystagmus.
Patient Report A 52-year-old right-handed woman was evaluated for the complaint of episodic true vertigo associated with blurred vision and gait instability. Episodes occurred five to eight times daily, each lasting approximately 1 minute. The patient was asymptomatic between episodes except for constant tinnitus in the left ear without associated hearing loss. Past medical history was significant for migraine headaches (without vertigo) for 20 years before this evaluation, treated with propranolol, and generalized tonic-clonic seizures from age 18 to 44 years, treated with phenytoin. The patient had not had a generalized tonic-clonic seizure for 8 years before this ~~
~
From the Departments of *Otolaryngology, ?Neurology, and SPediatrics, University of Pittsburgh, Pittsburgh, PA. Received Aug 23, 1989, and in revised form Dec 12. Accepted for publication Jan 5 , 1990. Address correspondence to Dr Furman, Department of Otolaryngology, Eye & Ear Institute, Suite 500, 203 Lothrop St, Pittsburgh, PA 15213.
evaluation, during which time medication included phenobarbital 30 mg at bedtime and carbamazepine 200 mg twice daily. General physical examination and neurological examination were entirely within normal limits, including evaluation of the patient's extraocular movements and gait. Quantitative vestibular and ocular motor function testing by using DC coupled electrooculography (EOG) with a highfrequency filter (40 Hz) revealed normal saccadic, pursuit, and optokinetic movements. Static and paroxysmal positional nystagmus were absent. Caloric and sinusoidal rotational responses were normal. Audiometric tests, including pure tone thresholds, speech discrimination, tympanometry, acoustic reflexes, tone decay, and brainstem auditory evoked responses, were all normal. A magnetic resonance scan of the head was normal. While seated in the vestibular laboratory, prior to caloric and rotational testing, the patient experienced a typical episode of vertigo associated with right-beating jerk nystagmus (Fig 1).N o gaze deviation was observed before the onset of nystagmus. The onset of the nystagmus shown in Figure 1 was not captured because of a delay in activating the chart recorder. Although absolute eye position cannot be determined with EOG without asking a subject to fixate a target as a point of reference, we estimated that our patient was gazing straight ahead when her nystagmus terminated. Slow component velocities were linear with a maximum velocity of about 65 degreedsec and a maximum beat frequency of 4lsec. Subsequently, simultaneous EEG and closed circuit TV (CCTV) monitoring revealed episodes of con jugate right-beating horizontal jerk nystagmus associated with repetitive spikes in the left posterior temporal region (Fig 2). Figure 3 indicates the time course of the patient's symptoms of vertigo, rightbeating nystagmus, and spike activity seen on the EEG. The interictal EEG contained epileptiform features characterized by sharp waves and spikes from the left posterior temporal and parietal regions. Focal slowing consisting of theta frequency was seen from these same areas.
Discussion The patient described in this report manifested epileptic nystagmus whose slow component velocity waveform was linear. Whereas exponentially decreasing slow component velocity is characteristic of gazeevoked nystagmus and exponentially increasing slow component velocities are of uncertain significance, linear slow component velocities are often a sign of vestibular imbalance or pursuit system defects [lo}. Thus, on the basis of the nystagmus slow component waveform alone, the patient's epileptic nystagmus may have resulted from activation of either the vestibular or the ocular pursuit system. The patient experienced vertigo during her episodes of epileptic nystagmus. Isolated episodes of nystagmus and vertigo are rarely caused by epileptic discharge although eye movements during seizures are not uncommon. The cause of this patient's vertigo may relate to activation of the superior temporal gyrus, a region purported to give rise to the conscious sensation of vertigo during vestibular stimulation 1111. The pa-
686 Copyright @ 1990 by the American Neurological Association
Fig 1. DC electrooculographicrecording of eye position during a vertiginous episode. Upper trace is horizontal eye position, lower trace is vertical eye position. Note the linear velocity during horizontal nystagmus slow components. Blinkr are indicated b~Bs in the vertical trace.
Fig 2. Electroencephalogramduring a vertiginous episode. (A) Seconds 2-4. The patient states she is having a spell; lateral nystagmoid eye movements can be seen at the F7 and F8 electroaks. Review of simultaneous closed circuit TV revealed a rightbeating nystagmus beginning 2 second afte. the onset of symptoms. (B) Seconds 11-15. Presence of rhythmicfast activity in lejit posterior temporal region (T5). Nystagmus persists. (C) Seconds 17-1 9. Further development of ldt posterior temporoparietal discharge; nystagmus decreases. (0)Seconds 32-34. Nystagmus has ceased and patient states spell is over. Epileptifm discharge continued for 8 more seconds (not shown).
tient’s EEG discharge during her spells was quite near this region. Studies in both humans and nonhuman primates suggest that the parietal lobe is important for the initiation and maintenance of ipsilateral ocular pursuit [12141. We hypothesize that this patient’s left-sided temporoparietal epileptic discharges may have induced a right-beating pursuit excitation nystagmus. A similar hypothesis was posited by Smith and Docherty [b], who ascribed their patient’s ictal nystagmus to “an automatism . . . analogous to optokinetic nystagmus.” The rapid build-up of nystagmus slow component velocity (seen on CCTV) and the rapid decay of nystagmus slow component velocity (see Fig 1) suggest that our patient’s nystagmus was due to activation of the pursuit system rather than activation of a subcortical optokinetic pathway that feeds brainstem vestibuloocular structures; electrical stimulation studies of the nucleus of the optic tract in monkeys results in a gradual rather than a rapid build-up and decline of nystagmus slow component eye velocity [lS]. The absence of gaze deviation and exponentially decreasing slow component velocity suggests that our patient, unlike the patient reported by Thurston and colleagues 111, did not have a gaze-evoked epileptic nystagmus. Also, the absence of vestibular and audiometric abnormahties
Brief Communication: Furman et al: Epileptic Nystagmus 687
with both a gaze-evoked 111 and a pursuit excitation nystagmus. DC coupled recordings of slow component velocity waveform d o w a distinction to be made between these two types of ictal nystagmus.
EEG DISCHARGE 1
I
NYSTAGMUS
’
SYMPTOMS
OF VERTIGO
gl *gl
I
I
I
0
10
20
’ I 30
I 40
1 50
T I M E (SEC)
Fig 3. Time course of patient’s signs and symptoms during the vertiginous episode depicted in Figure 2. Note that the patient’s symptoms of vertigo, nystagmus, and electroencephalographic discharge begin and cease at different times.
suggests that our patient did not have a lesion in peripheral or central vestibular structures. It is of interest that the patient’s signs and symptoms (see Fig 3) were not all contemporaneous and that her EEG discharge persisted beyond her symptoms. This suggests that (1) her seizure focus was subcortical and nearer the structures important for a conscious sensation of vertigo than to those structures important for ocular pursuit; (2) a higher level of electrical activity was required for the generation of nystagmus than was required for an awareness of vertigo; or (3) there was a different time course of electrical discharge in different cerebral regions. In each of the 10 reported cases in the English language literature of horizontal epileptic nystagmus associated with a focal seizure disorder for which data are available {l,2, 4 , 81, the direction of nystagmus was contralateral to the side of epileptic focus. This patient’s nystagmus and seizure focus were also contralateral to one another. This relationship between side of seizure focus and nystagmus direction is consistent
688 Annals of Neurology
The authors acknowledge the helpful suggestions of Dr Mark Hurtt and thank Karen Chianelli for assistance in preparing the manuscript.
Vol 27 No 6 June 1990
References 1. Thurston SE, Leigh RJ, Osorio I. Epileptic gaze deviation and nystagmus. Neurology 1985;35:1518- 1521 2. Barry E, Sussman NM, Bosley TM, Harner RN. Ictal blindness and status epilepticus amauroticus. Epilepsia 1985;26:577-584 3. Bender MB. The oculomotor system. New York: Harper and Row, 1964:300 4. Beun AM, Beintema DJ, Binnie CD, et al. Epileptic nystagmus. Epilepsia 1984;25:609-614 5. Kaplan PW, Lesser RP. Vertical and horizontal epileptic gaze deviation and nystagmus. Neurology 1989;39:1391-1393 6. Smith NJ, Docherty TB. Nystagmus: an unusual manifestation of temporal lobe epilepsy. 1 Electropbyd Tech 1982;8:7-13 7. White JC. Epileptic nystagmus. Epilepsia 1971;12:157-164 8. Barry E. Epileptic gaze deviation and nystagmus. Neurology 1986;36:875-876 9. Goldberg GS, Adelman JV. Ictal nystagmus: a case report. Electroencephalogr Clin Neurophysiol 1980;49:74P 10. Leigh RJ, Zee DS. The neurology of eye movements. Philadelphia: F. A. Davis Co, 1983 11. Friberg L, Olsen TS, Roland PE, et al. Focal increase of blood flow in the cerebral cortex of man during vestibular stimulation. Brain 1985;198:609-62 3 2. Baloh RW, Yee RD, Honrubia V. Optokinetic nystagmus and parietal lobe lesions. Ann Neurol 1980;7:269-276 3. Diirsteller MR, Wurtz RH. Pursuit and optokinetic deficits following chemical lesions of cortical areas MT and MST. J Neurophysiol 1988;60:940-965 4. Tusa RJ, Ungerleider LG. Fiber pathways of cortical areas mediating smooth pursuit eye movements in monkeys. Ann Neurol 1988;23:174-183 15. Schiff D, Cohen B, Raphan T. Nystagmus induced by stimulation of the nucleus of the optic tract in the monkey. Exp Brain Res 1988;70:1-14
We report a 52-year-old woman with episodes of vertigo accompanied by right beating nystagmus and left posterior temporoparietal sharp waves and spikes on electroencephalogram without change in level of consciousness. Electrooculography demonstrated that the episodes of nystagmus were not preceded by gaze deviation and that nystagmus slow component velocities were linear. This patient's epileptic nystagmus may have been the result of excitation of cerebral ocular pursuit pathways. Furman JMR, Crumrine PK, Reinmuth OM. Epileptic nystagmus. Ann Neurol 1990;27:686-688
Accurate measurement of eye position during epileptic nystagmus is available in the English literature for only a single patient 111. Other reports of eye movements during seizures are limited to clinical observation or eye position records made with electroencephalographic (EEG) equipment 12-7}, which does not allow for proper assessment of nystagmus slow component velocity. Such information is critical for a determination of the underlying pathophysiology of epileptic nystagmus. We report a patient with epileptic nystagmus whose slow component velocities were linear, a finding not previously described. Also of interest is that our patient did not lose consciousness, a previously reported 17-91 but unusual feature of epileptic nystagmus.
Patient Report A 52-year-old right-handed woman was evaluated for the complaint of episodic true vertigo associated with blurred vision and gait instability. Episodes occurred five to eight times daily, each lasting approximately 1 minute. The patient was asymptomatic between episodes except for constant tinnitus in the left ear without associated hearing loss. Past medical history was significant for migraine headaches (without vertigo) for 20 years before this evaluation, treated with propranolol, and generalized tonic-clonic seizures from age 18 to 44 years, treated with phenytoin. The patient had not had a generalized tonic-clonic seizure for 8 years before this ~~
~
From the Departments of *Otolaryngology, ?Neurology, and SPediatrics, University of Pittsburgh, Pittsburgh, PA. Received Aug 23, 1989, and in revised form Dec 12. Accepted for publication Jan 5 , 1990. Address correspondence to Dr Furman, Department of Otolaryngology, Eye & Ear Institute, Suite 500, 203 Lothrop St, Pittsburgh, PA 15213.
evaluation, during which time medication included phenobarbital 30 mg at bedtime and carbamazepine 200 mg twice daily. General physical examination and neurological examination were entirely within normal limits, including evaluation of the patient's extraocular movements and gait. Quantitative vestibular and ocular motor function testing by using DC coupled electrooculography (EOG) with a highfrequency filter (40 Hz) revealed normal saccadic, pursuit, and optokinetic movements. Static and paroxysmal positional nystagmus were absent. Caloric and sinusoidal rotational responses were normal. Audiometric tests, including pure tone thresholds, speech discrimination, tympanometry, acoustic reflexes, tone decay, and brainstem auditory evoked responses, were all normal. A magnetic resonance scan of the head was normal. While seated in the vestibular laboratory, prior to caloric and rotational testing, the patient experienced a typical episode of vertigo associated with right-beating jerk nystagmus (Fig 1).N o gaze deviation was observed before the onset of nystagmus. The onset of the nystagmus shown in Figure 1 was not captured because of a delay in activating the chart recorder. Although absolute eye position cannot be determined with EOG without asking a subject to fixate a target as a point of reference, we estimated that our patient was gazing straight ahead when her nystagmus terminated. Slow component velocities were linear with a maximum velocity of about 65 degreedsec and a maximum beat frequency of 4lsec. Subsequently, simultaneous EEG and closed circuit TV (CCTV) monitoring revealed episodes of con jugate right-beating horizontal jerk nystagmus associated with repetitive spikes in the left posterior temporal region (Fig 2). Figure 3 indicates the time course of the patient's symptoms of vertigo, rightbeating nystagmus, and spike activity seen on the EEG. The interictal EEG contained epileptiform features characterized by sharp waves and spikes from the left posterior temporal and parietal regions. Focal slowing consisting of theta frequency was seen from these same areas.
Discussion The patient described in this report manifested epileptic nystagmus whose slow component velocity waveform was linear. Whereas exponentially decreasing slow component velocity is characteristic of gazeevoked nystagmus and exponentially increasing slow component velocities are of uncertain significance, linear slow component velocities are often a sign of vestibular imbalance or pursuit system defects [lo}. Thus, on the basis of the nystagmus slow component waveform alone, the patient's epileptic nystagmus may have resulted from activation of either the vestibular or the ocular pursuit system. The patient experienced vertigo during her episodes of epileptic nystagmus. Isolated episodes of nystagmus and vertigo are rarely caused by epileptic discharge although eye movements during seizures are not uncommon. The cause of this patient's vertigo may relate to activation of the superior temporal gyrus, a region purported to give rise to the conscious sensation of vertigo during vestibular stimulation 1111. The pa-
686 Copyright @ 1990 by the American Neurological Association
Fig 1. DC electrooculographicrecording of eye position during a vertiginous episode. Upper trace is horizontal eye position, lower trace is vertical eye position. Note the linear velocity during horizontal nystagmus slow components. Blinkr are indicated b~Bs in the vertical trace.
Fig 2. Electroencephalogramduring a vertiginous episode. (A) Seconds 2-4. The patient states she is having a spell; lateral nystagmoid eye movements can be seen at the F7 and F8 electroaks. Review of simultaneous closed circuit TV revealed a rightbeating nystagmus beginning 2 second afte. the onset of symptoms. (B) Seconds 11-15. Presence of rhythmicfast activity in lejit posterior temporal region (T5). Nystagmus persists. (C) Seconds 17-1 9. Further development of ldt posterior temporoparietal discharge; nystagmus decreases. (0)Seconds 32-34. Nystagmus has ceased and patient states spell is over. Epileptifm discharge continued for 8 more seconds (not shown).
tient’s EEG discharge during her spells was quite near this region. Studies in both humans and nonhuman primates suggest that the parietal lobe is important for the initiation and maintenance of ipsilateral ocular pursuit [12141. We hypothesize that this patient’s left-sided temporoparietal epileptic discharges may have induced a right-beating pursuit excitation nystagmus. A similar hypothesis was posited by Smith and Docherty [b], who ascribed their patient’s ictal nystagmus to “an automatism . . . analogous to optokinetic nystagmus.” The rapid build-up of nystagmus slow component velocity (seen on CCTV) and the rapid decay of nystagmus slow component velocity (see Fig 1) suggest that our patient’s nystagmus was due to activation of the pursuit system rather than activation of a subcortical optokinetic pathway that feeds brainstem vestibuloocular structures; electrical stimulation studies of the nucleus of the optic tract in monkeys results in a gradual rather than a rapid build-up and decline of nystagmus slow component eye velocity [lS]. The absence of gaze deviation and exponentially decreasing slow component velocity suggests that our patient, unlike the patient reported by Thurston and colleagues 111, did not have a gaze-evoked epileptic nystagmus. Also, the absence of vestibular and audiometric abnormahties
Brief Communication: Furman et al: Epileptic Nystagmus 687
with both a gaze-evoked 111 and a pursuit excitation nystagmus. DC coupled recordings of slow component velocity waveform d o w a distinction to be made between these two types of ictal nystagmus.
EEG DISCHARGE 1
I
NYSTAGMUS
’
SYMPTOMS
OF VERTIGO
gl *gl
I
I
I
0
10
20
’ I 30
I 40
1 50
T I M E (SEC)
Fig 3. Time course of patient’s signs and symptoms during the vertiginous episode depicted in Figure 2. Note that the patient’s symptoms of vertigo, nystagmus, and electroencephalographic discharge begin and cease at different times.
suggests that our patient did not have a lesion in peripheral or central vestibular structures. It is of interest that the patient’s signs and symptoms (see Fig 3) were not all contemporaneous and that her EEG discharge persisted beyond her symptoms. This suggests that (1) her seizure focus was subcortical and nearer the structures important for a conscious sensation of vertigo than to those structures important for ocular pursuit; (2) a higher level of electrical activity was required for the generation of nystagmus than was required for an awareness of vertigo; or (3) there was a different time course of electrical discharge in different cerebral regions. In each of the 10 reported cases in the English language literature of horizontal epileptic nystagmus associated with a focal seizure disorder for which data are available {l,2, 4 , 81, the direction of nystagmus was contralateral to the side of epileptic focus. This patient’s nystagmus and seizure focus were also contralateral to one another. This relationship between side of seizure focus and nystagmus direction is consistent
688 Annals of Neurology
The authors acknowledge the helpful suggestions of Dr Mark Hurtt and thank Karen Chianelli for assistance in preparing the manuscript.
Vol 27 No 6 June 1990
References 1. Thurston SE, Leigh RJ, Osorio I. Epileptic gaze deviation and nystagmus. Neurology 1985;35:1518- 1521 2. Barry E, Sussman NM, Bosley TM, Harner RN. Ictal blindness and status epilepticus amauroticus. Epilepsia 1985;26:577-584 3. Bender MB. The oculomotor system. New York: Harper and Row, 1964:300 4. Beun AM, Beintema DJ, Binnie CD, et al. Epileptic nystagmus. Epilepsia 1984;25:609-614 5. Kaplan PW, Lesser RP. Vertical and horizontal epileptic gaze deviation and nystagmus. Neurology 1989;39:1391-1393 6. Smith NJ, Docherty TB. Nystagmus: an unusual manifestation of temporal lobe epilepsy. 1 Electropbyd Tech 1982;8:7-13 7. White JC. Epileptic nystagmus. Epilepsia 1971;12:157-164 8. Barry E. Epileptic gaze deviation and nystagmus. Neurology 1986;36:875-876 9. Goldberg GS, Adelman JV. Ictal nystagmus: a case report. Electroencephalogr Clin Neurophysiol 1980;49:74P 10. Leigh RJ, Zee DS. The neurology of eye movements. Philadelphia: F. A. Davis Co, 1983 11. Friberg L, Olsen TS, Roland PE, et al. Focal increase of blood flow in the cerebral cortex of man during vestibular stimulation. Brain 1985;198:609-62 3 2. Baloh RW, Yee RD, Honrubia V. Optokinetic nystagmus and parietal lobe lesions. Ann Neurol 1980;7:269-276 3. Diirsteller MR, Wurtz RH. Pursuit and optokinetic deficits following chemical lesions of cortical areas MT and MST. J Neurophysiol 1988;60:940-965 4. Tusa RJ, Ungerleider LG. Fiber pathways of cortical areas mediating smooth pursuit eye movements in monkeys. Ann Neurol 1988;23:174-183 15. Schiff D, Cohen B, Raphan T. Nystagmus induced by stimulation of the nucleus of the optic tract in the monkey. Exp Brain Res 1988;70:1-14
