Quantitative Measurements of Eye Movements in a Patient with Tullio Phenomenon

Contribution

QUANTITATIVE MEASUREMENTS OF EYE MOVEMENTS IN A PATIENT WITH TULLIO PHENOMENON

Klaus G. Rottach,* Regina D. von Mayde!\,* Alfred 0. DiScenna,* AriZ. Zivototsky,t Lea Averbuch-Heller, * and R. John Leigh, *tt§

*Departments of Neurology, tBiomedical Engineering, :!:Otolaryngology and §Neuroscience, Veterans Affairs Medical Center and University Hospitals, Case Western Reserve University, Cleveland, Ohio Reprint address: R. John Leigh, M.D., Department of Neurology, University Hospitals, 2074 Abington Road, Cleveland, OH 44106. Tel: (216) 844-3190; Fax:(216) 844-3160; E-mail: [email protected]

0 Abstract-The Tullio phenomenon consists of how it might help to determine whether the dis vestibular symptoms on exposure to high-intensity turbance is more typical of dysfunction of semi acoustic stimuli, reflecting pathological stimula circular canals or otoliths. Such information tion of semicircular canals or otoliths. We report a might ultimately help in planning treatment. patient with posttraumatic Tullio phenomenon to illustrate how precise measurement of eye move ments during auditory stimulation, using the mag Patient and Methods netic search coil technique, may characterize movements that are not clinically apparent or eas ily measured by other means. Such measurements Case report in patients with surgically verified lesions may further elucidate the mechanisms responsible for A 36-year-old woman developed Tullio phe this phenomenon. nomenon following head trauma. One year prior to our evaluation, she had been hit by an 0 Keywords- Tullio phenomenon; nystagmus; automatic door and fell, apparently without los perilymph fistula; magnetic search coil. ing consciousness; she sustained bilateral jaw dislocation. She had not experienced dizziness prior to the head injury, but afterwards reported Introduction that "my eyes move" whenever her phone rang. This feeling would start immediately when the The Tullio phenomenon refers to sound-in phone started to ring and stopped as the ringing duced vestibular symptoms (1 ). Although prior stopped. When this happened, she sometimes papers have reported clinicaL audiologicaL and felt c. little , but dici nm exper]ence ro posturographical findings, documentation of tatory vertigo or oscillopsia. She also reported eye movements has been hindered by the limita sometimes feeling unsteady when she made fast tions of electro-oculography (2), because the head movements. Her prior medical history was movements are often small and may be predom remarkable for a congenital, fmnilial hearing inantly torsional (that is, rotations around the deficit that had not been specifically diagnosed. line of sight). The magnetic search coil tech Since childhood she had worn hearing aids in nique allows precise measurement of eye and both ears that provided satisfactory improve head rotations in all three planes, and is now ment of her hearing. She had not noticed any quite widely available (3). We used this tech additional hearing loss since the accident. By nique to study a patient with posttraumatic Tul alternately removing each of her hearing aids lio phenomenon and present data to illustrate she was able to identify her right ear as respon-

RECEIVED 12 June 1995; AccEPTED 3 January 1996. 255 256 K. G. Rottach et al sible for the problem: the symptoms only oc hanced vestibulo-ocular reflex (VVOR) and curred when the right hearing aiel was in place. convergence were also tested. Data analysis She was unable to provoke the phenomenon by was performed using interactive programs writ the V alsalva maneuver or by applying manual ten in the ASYST language. Gain (ratio of eye pressure to her external auditory canal. Clinical movement and target movement) of saccadic examination showed a nystagmus with horizon amplitude, smooth pursuit, and VVOR velocity tal and torsional components that was present were calculated (4,5). Peak velocities of sac exclusively during the time that her telephone cades, convergence angle, and slow-phase ve was ringing. lt was low-amplitude. variable, locities of nystagmus were measured. and sometimes could only be detected with cll1 'Nas 1.0 noticeable :1ead 1virh ucousric stimulation. To stan or body tilt during acoustic stimulation. To date, dm·dize the sound stimulus, we first used sound our patient has not undergone surgical explont frequencies of 125, 250, 500, 750, lOOO, 1500, tion of her middle ear, but intends to consider 2000, 3000, 4000, 6000, and 8000Hz through a this if her symptoms persist. hearing testing device (J\!Iaico portable audiom eter). During this testing with headphones, the Eye Movement Measurements. The patient gave patient did not wear her hearing aids. Sound informed consent according to the Helsinki pressures up to 105 dB HL were applied and, Declaration of 197 5. Horizontal, vertical, and probably due to the severity of hearing loss, torsional rotations of both eyes and of the head none elicited the Tullio phenomenon. Equip were recorded using the magnetic search coil ment was not available for accurate sound field technique (3,4). Search coils were calibrated testing. Therefore, we tested the patient while prior to the experimental session using a pro she wore her hearing aids and used her tele tractor device. Data were filtered (bandwidth 0 phone, which reliably induced the Tullio phe to 100 Hz) prior to digitization at 300 Hz (for nomenon. The telephone was placed 0.4 m from routine ocular motor testing) or 1000Hz (for re the patient, and it was determined that it had no cordings with acoustic stimulus). For determi effect on the search-coil signal. Each phone ring nations of the latency to onset of nystagmus, the lasted about 2 s. We measured the effect of the sound of the phone was recorded through ami telephone ring on the stability of gaze during crophone and digitized without filtering at a fixation of the stationary laser clot and in com sampling rate of 1000 Hz. In order to determine plete darkness as the patient attempted to look the frequency components, recordings of the at the remembered target location. We also ap sound were performed at sampling rates of 3000 plied acoustic stimulation during smooth pur and 5000 Hz, and the main frequencies were suit and VVOR testing. evaluated using a Fast Fourier transform. The visual stimulus consisted of a red laser spot that was rear-projected, under the control of mirror Results galvanometers (General Scanning CX 660), onto a semitranslucent tangent screen at a view 1. Routirw Ocular Jv!otor Testing ing distance of 1.2 m. Saccadic gain was 0.90 horizontally and 0.98 vertically. Saccadic amplitude/peak-velocity re Experi1nental Stimuli and Data Analysis lationships were normal. Smooth pursuit tracking gain was 0.97 horizontally and 0.96 vertically. 1. Routine ocular motor testing. We tested re The gain of the VVOR was 1.04 horizontally fixation saccades as the target made :±: 10° hori and 1.07 vertically. The patient was able to con zontal and vertical jumps. Smooth pursuit was verge 21 o in response to a near stimulus. These tested as the target (laser spot) moved sinusoi results are all within the normal range (4-6). dally through :±: 20° at 0.3 Hz in either the hori However, during all conditions except fixation zontal or vertical direction. The visually en- of a stationary target, there was a low-ampli- Tullio Phenomenon 257 tude, torsional nystagmus, With qmck phases stimuli during fixation paradigms (9 with a tar beating clockwise with respect to the patient. get and 13 in complete darkness), and nystag This nystagmus was variable, being maximal mus was triggered every time; the mean latency during smooth pursuit when slow phase veloc to onset was 16 m. This response was the same ity was 1.6°/S and beating frequency was 3 Hz. during fixation of a stationary target and during Attempted fixation in complete darkness re attempted fixation in darkness. There was no ef vealed, in addition to the torsional nystagmus, fect on the vertical component, that is, during variable horizontal left-beating and vertical fixation there was no vertical eye movement, down-beating components. The horizontal and and in darkness the spontaneous downbeat nys vertical slow phase velocity reached a maxi tagmus (if present) continued. The average slow mum of 1.2°/s, and the frequency sometimes phase velocity was 1.1 o /s (max. 1.5° Is) horizon reached 2 Hz. She was unaware of this sponta tally and 0.8°/s (max. 1.3°/s) torsionally; the av neous nystagmus. erage frequency of quick phases was 0.6 Hz.

2. Recordings with acoustic stimulation A

The sound stimulation reliably provoked a horizontal right-beating and a torsional clock Ci ~ 0 c wise beating nystagmus; an example is shown 0 il -1 in Figure 1. We applied a total of 22 sound 0 Q. ~ -2 C'O Cl 10,------, -3 ~rightho~. 0 2 4 8 ~lefthor. time (sec)

B Ci ------~---- rightvert. ~ 6 gc ------leftvert. '(ii 0 Q. ~ 0 ~ l:l 4 ~righttors. ltl ~ -1 Cl '(j) ~lefttors. 8. -2 Q) ltl -3 2 Cl

-4 -~-·M*•I•M•I.t·~···- sound 0 2 4 0 2 3 4 5 time (sec) time (secl Figure 2. 1 uliio phenomenon during attempted fixa Figure 1. Tullio phenomenon during fixation of a sta tion in complete darkness. Horizontal position signal tionary target. As soon as the acoustic stimulation of the right eye is shown. Conventions are the same starts, conjugate horizontal right-beating and torsiona[ as those in Figure 1. (A) Horizontal left-beating spon clockwise-beating nystagmus commenced. Note the taneous nystagmus takes place in darkness without absence of any spontaneous nystagmus prior to, and acoustic stimulation. At the beginning of this record of vertical nystagmus during, this sound stimulation. ing, sound stimulation had just ended and, at the end, The single position traces are offset for convenience a new stimulation had begun. Note that direction of of display; upward deflections indicate rightward the slow phase reverses each time. (B) Two seconds (horizontal), upward (vertical), or clockwise (torsional) of sound stimulation in darkness. As soon as the eye rotations, with respect to the patient. The sound sound starts, the slow phase movement reverses di signal is only displayed for timing information. Its rection from rightwards to leftwards, and the nystag record is distorted by the aliasing effects of a sam mus is now beating to the right. As the sound stops pling rate at 1000 Hz, well below the required Nyquist the direction of the movement again immediately re frequency for this signal. verses. 258 K. G. Rottach et al

Note that the horizontal left-beating spontane and was followed by a smaller tonic effect that ous nystagmus (present only in darkness) lasted as long as the sound stimulation. Surgical changed its direction to right-beating during exploration in this patient showed a subluxated acoustic stimulation (Figure 2). stapes footplate with a hypertrophic stapedius Sound stimulation had no influence on the muscle, causing pathologically large move performance of smooth pursuit (gain horizontal ments of the stapes footplate during the sound 0.98, vertical 0.97) or VVOR (gain horizontal induced stapedius reflex. Thus, the saccule or 1.06, vertical 1.07). No head movements were utricle may have been directly stimulated by the induced by the acoustic stimulation. stapes footplate. Other patients who have been Frequency analysis of the telephone ring re- thought to have an otolithic type of Tullio phe aomenon have .·mown either tonic torsional eye movements with head tilt ( 10), conjugate verti cal eye movements (11), or horizontal nystagmus ( 12). Patients with Tullio phenomenon attrib Discussion uted to pathological stimulation of a semicircu lar canal have been less clearly defined (9,13,14). Tullio mainly studied the phenomenon that In our patient, sound stimuli induced a hori carries his name in pigeons (1); his experiments zontal right-beating and torsional clockwise have been repeated and extended by others beating nystagmus (the horizontal component (7 ,8). If a small opening is made into the vesti was more pronounced) with a latency similar to bule of the bony labyrinth, a stereotyped re that of the vestibula-ocular reflex (16 m) (15). sponse to acoustic stimuli occurs, consisting of When she was not maintaining steady fixa a contralateral head tilt; this is interpreted as be tion-either during other eye movements or ing due to utricular stimulation. An opening when in darkness-there was a low-amplitude made into one of the bony canals leads to head nystagmus beating leftward, clockwise, and nystagmus in the plane of the affected canal; for downward; this suggested a small vestibular im the lateral canal, quick phases of head nystag balance. During sound stimulation, the horizon mus are directed towards the side of the acous tal nystagmus reversed its direction, but the tor tic stimulation. This type of head nystagmus is sional (and vertical) nystagmus did not. There the way that a pigeon responds to stimulation of was no vertical (skew) eye movement or head the crista. Huizinga (7) suggested that the artifi tilt that might suggest otolithic stimulation. cial opening in the bony labyrinth has the same Thus, we postulate that the reversal of horizon effect with regard to sound waves as the round tal nystagmus was due to sound stimulation of window has to the cochlea: it allows the sound the crista of the right horizontal semicircular ca waves, which otherwise would have been extin nal, which overcame a component of an under guished through interference, to escape from lying vestibular imbalance. Our patient had the labyrinthine t1uid. In this case, fluid move congenital hearing loss-which is associated ment stimulates not only the cochlea. but also with Tullio phenomenon ( 16)-but only devel the crista of the affected canal. oped symptoms after bead trauma. suggesting a Prior clinical studies also suggest otolithic fistula as the cause, although this was not surgi and semicircular-canal variants of Tullio phe cally confirmed. nomenon, although the mechanism is often in In many reported patients with Tullio phe doubt. The otolithic type has been well charac nomenon, it is difficult to be sure of the under terized in a patient studied by Dieterich and col lying mechanism; this problem often arises be leagues (9), who showed a tonic, torsional, and cause the eye movements have not been well vertical (skew) eye deviation, head tilt, postural characterized. We have shown that it is possible imbalance, and a subjective tilt of the visual en to make precise measurements of 3-dimensional vironment (the ocular tilt reaction). An initial eye and head movements using the search coil phasic vertical and torsional deviation of the technique, which is now available at most eyes occurred with a latency of about 20 ms, teaching centers. This procedure is safe, well Tullio Phenomenon 259 tolerated, and is the standard by which other moderate-to-severe (loss ranging 50 dbHL at methods are judged (17). In patients such as 200Hz to 85 dbHL at 8000Hz) in the left ear ours, it allows reliable characterization of eye and severe-to-profound (loss ranging 60 dbHL movements that are small and may remain un at 250Hz to 100 dbHL at 8000Hz) in the right detected by clinical examination. Better charac ear. Impedance audiometry demonstrated nor terization of the eye movements in Tullio phe mal tympanic membrane mobility but absent nomenon in patients in whom the underlying stapedial reflexes, bilaterally. disorder has been surgically confirmed may elu cidate the mechanisms by which the symptoms Acknovvledgnwnrs-We are grateful to G. Murray. and signs arise. Ph.D., for providing the audiology equipment, to B. Rottach for translating the article of C. E. Benjamins, and to Dr. Robert L. Tomsak for refening the patient. Addendum Supported by USPHS grant EY06717, the Depart ment of Veterans Affairs, and the Even or Armington We were able to obtain an audiogram subse Fund (to Dr. Leigh), Deutsche Forschungsgemein quent to measurement of eye movements. This schaft (to Dr. Rottach), and Ernst Jung Stiftung (to confirmed a bilateral sensorineural hearing loss, Dr. Von Maydell).

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