Head Nodding is Compensatory in Spasmus Nutans Irene Gottlob, MD,1,2 Alina A. Zubcov, MD,1,3 Sheryl S. WiZOV, l Robert D. Reinecke, MD1 Background: Spasmus nutans is defined as asymmetric nystagmus with associated head nodding in childhood. It is not clear whether head nodding is a compensatory mechanism to control the nystagmus or an involuntary movement of pathologic origin. Methods: The authors analyzed the relation between head and eye movements by simultaneous eye and head movement recordings of 35 patients with spasmus nutans. Results: In 21 of these patients, the fine, fast, dissociated nystagmus changed during head nodding to larger and slower symmetric eye movements with both eyes oscillating at the same amplitude in phase and 180° out of phase to the head movements, corresponding to a normal compensatory vestibulo-ocular reflex. Conclusion: These findings indicate that head nodding is compensatory in spasmus nutans. Ophthalmology 1992;99:1024-1031

Spasmus nutans patients have had their asymmetric nystagmus, head nodding , and abnormal head position reported by several authors. 1-3 Only a few reports, however, present well-documented recordings of eye and/or head movements of such patients.v? On eye movement recordings, the nystagmus in spasmus nutans was found to be intermittent, pendular, and fine, with an asymmetric amplitude high frequency (up to 15 Hz), and the right and left eye oscillating out of phase. The head nodding is intermittent, has a slow frequency (2 to 3 Hz), and varies in its amplitude between 2° and 25°.7 In a previous study," we showed that patients with spasmus nutans with and without brain pathology have the same characteristics on eye and head movement recordings. The differentiation between both patient groups must be made on the basis ofneuroimaging. The onset of nystagmus and head nodding often are not simultaneous. In addition, the freOriginally received: October 7, 199 1. Revision accepted: January 23, 1992. I The Foerderer Eye Movement Cent er For Children , Wills Eye Hospital, Dep artment of Ophthalmology, Jefferson Medical College of Thomas Jefferson Uni versity, Philadelphia.

2

First Un iversity Eye Clinic, Vienna, Austri a.

Department of Ophthalmology, Johann Wolfgang Goethe Universitat, Frankfurt/M, Germany.

3

Supported by a grant from the Max-Kade Foundation (Dr. Irene Gottlob), New York, New York. Reprint requests to Irene Gottlob, MD , Foerderer Eye Movement Center for Child ren , Wills Eye Hospit al, 9th & Walnu t Sts, Ph iladelphia, PA 19107.

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quency of the nystagmus is generally different from and higher than that of the head nodding. Therefore, most authors have concluded that there is no relation between nystagmus and head movements. However, Gresty et al" and Grest y and E1l 5 found that head shaking abolished the nystagmus in three patients. In contrast, Weissmann et al" found that passively generated head movements did not suppress the nystagmus. We observed that patients with spasmus nutans increase the head nodding when small visual targets are presented. The aim of this study is to analyze the relationship of head and eye movements in a large group of spasmus nutans patients. Simultaneous head and eye movement recordings were obtained from 35 patients with spasmus nutans. In three patients, the influence of passive head shaking on their nystagmus was investigated.

Patients and Methods All eye and head movement recordings from patients with spasmus nutans symptoms examined at the Foerderer Eye Movement Center for Children at Wills Eye Hospital between July 1985 and May 1990 were reviewed. According to our previous report ,' the diagnosis of spasmus nutans was based on head nodding and eye movement recordings of the nystagmus waveform (pendular, intermittent, fine, fast, right and left eye oscillating at different amplitudes and out of phase). Thirty-five patients were diagnosed as having spasmus nutans. Twenty-one of the 35 patients

Gottlob et al . Head Nodding in Spasmus Nutans Table 1. 35 Patients with Spasmus Nutans Head nodding suppresses nystagmus (no.] Mean age Male (no.) Female (no.) Strabismus or amblyopia (no.) Abnormal brain findings (no.) Glioma of optic nerve and chiasm (no.) Ependymoma of fourth ventricle (no.) Ar achnoid cyst in the left cran ial fossa (no.) Underdeveloped left hemisphere (no.) Decreased perfusion of left cerebellum and basal ganglia (no.) Excluded because of insufficient data (no.)

21 27 months 8 13

14 5 1 1

1 1 1

14

had nystagmus that changed during head movements on our recordings, and they were selected for detailed analyses for this study. In the remaining 14 patients with spasmus nutans, we did not detect a change of nystagmus during head nodding. All of these 14 patients showed at least short periods of head nodding. In six of them, the periods of head nodding were too brief for analysis. In eight patients, the recording quality was not good enough for analyzing the eye and head movements interrelationship (i.e., when head nodding was present, evaluation of the recordings of one of the eyes was not possible). Other characteristics of the group studied are summarized in Table I. The age of the 21 patients selected for this study was between 6 months and 5 years (mean, 27.1 months; standard deviation, 23.3 months). Eight patients were girls and 13 patients were boys. Computed tomography or magnetic resonance imaging were performed on all patients. In 16 patients, no pathology was found. One patient had a glioma of the optic tract and chiasm, one had an ependymoma of the fourth ventricle, one had an underdeveloped left hemisphere and developmental delay, and one patient had a small arachnoidal cyst in the left cranial fossa. One patient with cerebral palsy and developmental delay had normal results on computer tomography and magnetic resonance imaging but had a decreased perfusion of the left side of the cerebellum and of both basal ganglia on technetium brain scan examination. Eight of the 16 patients without pathology had strabismus or ambl yopia. The other 8 patients had no ophthalmologic abnormalities except the nystagmus . In the group of patients with brain pathology, only the patient with the arachnoidal cyst was orthophoric. The other four patients had strabismus. Bilateral optic disc pallor was noted in the patient with the chiasma! glioma . Eye and head movements were simultaneously recorded in all patients . For the electro-oculography, a Tracor system (Model RV-275 , Tracoustic Inc, Austin, TX) was used to record horizontal eye position. Silver-silver chloride electrodes or Stat-Trace II (Niko Med USA, New Brunswick, NJ) St-102 EKG electrodes" were placed na-

sally to the medial canthi and temporally to the lateral canthi, and the indifferent electrode was placed centrally abo ve the glabella. For six patients, simultaneous vertical electro-oculograms were recorded with four additional electrodes placed over the eyebrows and under the lower lashes of each eye. The electro-oculograph signals were DC amplified (X30,000) and filtered (bandpass DC-30Hz). For calibration, with cooperative children, a green laser target was back-projected on a screen at 1 meter and used for smooth pursuit and/or saccadic eye movement stimulation. Horizontal and vertical head positions were recorded using a magnetic search coil system that used a small coil affixed to the patient's head with an athletic headband. A model eye indicating degrees of deviation was used to calibrate the head coil before the examinations. Target positions, eye positions, and head positions were recorded on a six-channel strip chart recorder. In three cooperative patients, passive head movements were obtained by shaking the patient's head. Analysis of the recordings included oscillation frequency and phase relationship between the right and left eyes and the head mo vements from a recording period between 2 and 15 minutes.

Results The following eye movement recordings are representative of the 21 patients, showing an influence of head nodding on the nystagmus. In Figure I, examples of horizontal eye and head movement recordings of patient I, a 20-month-old girl with spasmus nutans with no detected brain pathology on computer tomography, are shown. During the recordings, displayed in Figure lA , the patient was sitting in front of a white screen, and no visual target was presented . No rhythmic head oscillations are seen. The nystagmus frequency of both eyes was around 7 Hz and the eyes oscillated approximately 1800 out of phase. As detailed pictures were presented to the patient, she began to nod her head. The recordings of the horizontal head nodding are seen in the lower tracing of Figure I B. The head movement recording had a sinusoidal shape with a frequency of about 3 Hz and an amplitude between 6 0 and 24 0 • The simultaneously recorded eye movements had the same frequency as the head movement. The right and left eye oscillated in phase , while both eyes were 1800 out of phase with the head movements. The eye and head mo vement recordings from Figure 1B represent a normal vestibulo-ocular response. Only compensatory eye movements to the head nodding stabilizing the direction of gaze are present. No nystagmus is seen during head nodding . In Figure IC, the patient still concentrated on the pictures. Her head nodding had a frequency of approximately 4 Hz. The amplitude of the head oscillation was approximately 8 0 at the beginning of the record ings. At this moment, she still had only compensatory eye movements and no nystagmus. In the second part of the recordings, the amplitude of the head nodding decreased

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Volume 99, Number 7, July 1992

Ophthalmology

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large head nodding on the beginning of the recordin gs and no rh ythmic head nodding (arrows) on the last part of th e recordings. D, alternating large amplitude head nodding and compensatory eye movements (asterisks) and small amplitu de he ad nodding and nystagmus (arrows).

and finally stopped. Without the rhythmic hea~ os~iIla­ tions, the fine asymmetric nystagmus as obsen:ed 10 FIgure lA reappears (arrows). In Figure 10, the patient nodded her head during the whole recording. However, amplitude of head nodding was variable between 3° and 14°. At the beginning of the recording, the head nodding had an amplitude of about 8°. At this moment, mamly compensatory eye movements are seen. During these recordings, ' patient I decreased the amplitude of the rhythmic head movements several times to under 4°, and fine asymmetric nystagmus reappeared (arrows). The nystagmus was suppressed only with larger head nodding amplitudes over 4° (asterisks). . Similarly , patient 2, a 2lf2-year-old boy WIth an ependymoma of the fourth ventricle, could suppress his nystagmus by nodding his head. In Figure 2.A, head nodding of an amplitude between I ° and 15° IS observed. The frequency of the head nodding is between 1 and 3 Hz. When the frequency was 3 Hz, the amplitude was under 3° and when the amplitude was higher, the frequency w~s onl~ 1 Hz. During the whole recording, nystagmus of both eyes is observed. The right and left eyes oscillated at about 180° out of phase.In Figure 2B, the amplitude

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of the head nodding was higher (between 10° and 20°), and the frequency continuous at about 2.5 Hz. During these recordings , patient 2 suppressed his nystagmus and showed only compensatory eye movements, both eyes in phase with each other and out of phase 180° to the head movements. Figure 3A shows horizontal and vertical eye movements of patient 3, a 4-year-old girl with spasmus nutans and no detected brain pathology. Both eyes show asymmetric vertical nystagmus between 3 and 5 Hz . Vertical eye movements are pendular, and both eyes oscillate most of the time 180° out of phase. The vertical head movement recordings show bursts of vertical head nodding of about 4 Hz with an amplitude up to 8° (asterisks). The head nodding did not change the nystagmus. The horizontal eye movements show a fine pendular nystagmus of the right eye of about 7 Hz, while no nystagmus of the left eye is seen. The recordings show that the right eye had an oblique nystagmus moving simultaneously to the right and down and to the left and up. On this part of the recording, the left eye had only a vertical movement. No rhythmic horizontal head movements are seen on these . recordings . At the beginning of the record ings of Figure

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3B, the patient had small vertical head nodding, under 4° of amplitude, and a frequency of approximately 4 Hz. No simultaneous horizontal head nodding is observed. Initially, the right eye showed simultaneous horizontal and vertical (oblique) nystagmus of about 6 Hz (asterisk) and then the nystagmus became mainly horizontal with a frequency of 7 Hz. In the left eye, slower oblique nystagmus of about 4 Hz is observed. The open circle indicates the beginning of passive head shaking. One of the examiners moved the patient's chin mainly horizontall y. The horizontal head movements had an amplitude of 10° to 15° with a frequency of 4 Hz. As the passive rhythmic head movements began, large horizontal oscillations of both eyes are observed. Both eyes oscillated most of the time in phase, and the fine nystagmus disappeared. The horizontal eye movements are about 45° out of phase with the horizontal head movements (arrows). Vertical head nodding of small amplitude of about 5° is observed simultaneously. On vertical eye movement recordings, small compensatory eye movements at a frequency of 4 Hz are seen. Superimposed, there is still some fine vertical nystagmus on the left eye. To show that horizontal eye movements in Figure 3B correspond to normal compensatory eye movements, we examined a 5-year-old and a 32-year-old subject without spasmus nutans during passive head shaking. A similar head and eye movement coordination was observed in

the 5-year-old boy (Fig 4). The open circle indicates the beginning of the passive head shaking. Both eyes oscillate in phase and about 30° out of phase to the head (arrows). Similar results were found in the adult subject. During passive head shaking, both eyes oscillated in phase with each other and about 20° out of phase to the head. The adult subject subsequently was asked to move her head actively while fixing on a target. During these active head, movements, both eyes were in phase with each other and exactly 180° out of phase to the head. Thus , in controls, during passive head shaking without fixating on an object, the eyes are not exactly 180° out of phase to the head. In Figure 5A, vertical and horizontal eye movements of patient 4, a 21f2-year-old boy with spasmus nutans and no detectable changes on magnetic resonance imaging, are represented. Vertical pursuit movements of 20° were stimulated by the laser target. A fine oblique nystagmus (nystagmus on the vertical and horizontal recordings) of approximately 8 Hz is observed in the right eye, while no nystagmus can be detected in ·the left eye. The same oblique nystagmus of the right eye and some horizontal nystagmus of the left eye is present at the beginning of the recordings in Figure 5B. The open circle indicates the beginning of passive horizontal head movements between 14° and 45° and at approximately 4 Hz. At the same moment, the patient had compensatory eye movements of approximately 4 Hz, the left and right eye oscillating

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Volume 99, Number 7, July 1992

Ophthalmology

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Figure 4. Horizontal eye and head movement recordings of a normal subject during passive head shaking (open circle). Arrows indicate that the head movements and eye movements are not exactly 180° out of phase .

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in phase. Only a few beats of horizontal nystagmus are observed, and, most of the time, the nystagmus is completely suppressed. The horizontal head movements are approximately 45 °out of phase with the horizontal eye movements (arrows). Only small vertical head nodding (under 2°) is observed. However, vertical compensatory eye movements appear as the head is shaken horizontally. Probably the head was tilted slightly during the shaking. Fine and fast vertical nystagmus is superimposed to the compensatory vertical eye movements (asterisks). In Figure 5C, we attempted to shake the patient's head vertically. Vertical rhythmic head movements of a frequency of about 3 Hz and an amplitude between go and 10° were obtained. Simultaneously, we also shook the patient's head horizontally, but the amplitude was under go and always smaller than in Figure 5B. Vertical eye movements are in phase, and almost no vertical nystagmus can be observed throughout these recordings. Vertical eye and head movements are approximately 30° out of phase (arrows). However , the fine horizontal nystagmus of the right eye is present continuously during the recordings (asterisks). These eye movement recordings were representative for all 21 spasmus nutans patients who showed an influ-

Gottlob et al

Head Nodding in Spasmus Nutans

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Figure 5. A, vert ical and horizontal eye and head movement recordin gs of patient 4 performing vertical pursuit movements of 20°. B, passive horizontal he ad shak in g (open circle). C, passive head shakin g mainly in a vertic al dir ection. Asterisks indicate nystagmus. Arrows ind icate that the he ad and eye movements are not exactly 180° out of pha se.

ence of head nodding on nystagmus. According to the inclusion criteria, all patients with spasmus nutans exhibited pendular fine, asymmetric, dissociated nystagmus. For five of the six patients on whom vertical and horizontal eye movement recordings were performed , nystagmus also was present on vertical recordings. These patients had oblique nystagmus. Patients had interm ittent rhythmic head nodding of a frequency between 1 and 5 Hz and an amplitude up to 25°. Most of the patients had oblique head nodding, recorded simultaneously on the horizontal as well as the vertical head movement recordings. When visual targets were presented to the patients , they began to nod their heads and/or the amplitude of head nodding became larger. In the 21 patients selected for this study, we found

that head nodding suppressed the fine and fast dissociated nystagmus and that during head nodding only compensatory eye movements were present. Often a small head nodding amplitude (under about 4°) was not sufficient to suppress the nystagmus, while the nystagmus disappeared completely with a higher amplitude head nodding. The same pattern of eye and head movement coordination was observed in the patients with brain pathology. In three patients , the head was shaken by one of the examiners. In all three patients, the passive head movements suppressed the nystagmus. During passive head shaking, both eyes always had conjugated movements, while the eye and head movements were not precisely in opposite phase (not 180° out of phase) in the 3 patients and 2 control subjects tested.

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Discussion In our study, we found an influence of head nodding on eye movements in 21 of35 patients with spasmus nutans. In the remaining 14 patients, no relations between nystagmus and head movements were detected. When visual targets, such as pictures from a child's book , were presented, most of our patients started to nod their heads or the amplitude of the head nodding became larger. Therefore, the head nodding seems to increase with the spatial complexity of the fixation target. This is in agreement with Gresty et al," who found that the head nodding in their spasmus nutans patient was specifically elicited by novel stimuli to which intense attention was paid. According to the inclusion criteria, all patients had fine, intermittent, pendular dissociated nystagmus of high frequency. In addition, we also recorded vertical eye movements in six patients and found that five of them had an additional vertical component demonstrating oblique nystagmus. Head nodding was sinusoidal , intermittent, of slow frequency (between 1 and 5 Hz) and large amplitude (up to 25 0 ) . Most of the patients had oblique head nodding, recorded simultaneously on the horizontal as well as the vertical head movement recordings. During intensive head nodding, the eye movements are compensatory and stabilize the direction of gaze of the patient. Weissmann et al" observed that the nystagmus of their patients with spasmus nutans was occasionally conjugate, sometimes lasting throughout a whole recording session. However, no head movements were recorded on their patients. It is probable that their recordings were performed during head nodding and that the conjugate nystagmus corresponds to the compensatory eye movements observed in our patients. To suppress the nystagmus , the head nodding has to be higher than a threshold amplitude. In Figure 10, it is shown clearly that the nystagmus of patient 1 reappears when the head nodding decreases to an amplitude lower than 4 0 • This was observed in several patients. These findings are in agreement with Gresty et al," who showed in their patient that head movements of small amplitude did not necessarily abolish the nystagmus. Weissmann et al" shook the head of one patient with spasmus nutans horizontally and did not find that the nystagmus was modified by the head movement. In contrast , we found in three patients that passive head movements suppressed the nystagmus. The suppression of the nystagmus appears to depend on the direction ofthe head shaking. When we shook the head horizontally, the horizontal nystagmus disappeared while the vertical nystagmus persisted (Figs 3B and 5B). In contrast, passive vertical head shaking mainly suppressed the vertical nystagmus (Fig 5C). Clinical observations l ,2,3,6,7 and head movement recordings? showed that spasmus nutans patients frequently nod their heads in an oblique direction and tilt their heads simultaneously. The direction of head nodding might have to be adjusted to the direction of the

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nystagmus to compensate for horizontal and vertical components. Possibly the patients' head tilt helps the patients to nod the head in a certain plane. It is interesting that during passive head shaking the conjugate eye movements of the three patients and the two control subjects were not precisely 1800 out of phase to the head movements , although the frequencies of head and eye movements were the same (Figs 3B, 4, 5B, and 5C). In contrast, during active head nodding, the patients' eyes and head typically moved 1800 out of phase. The difference might be explained by the fact that patients with active head movements generally fixed on an object and that patients with passive head shaking probably did not fixate but superimposed active eye movements to the vestibulo-ocular reflex. A relation between head and eye movements also has been reported in patients with other nystagmus forms. Improved reading acuity during head shaking has been described by Metz et al? in one patient with congenital nystagmus. The ocular nystagmus and the head movements were exactly 1800 out of phase and appeared to compensate for each other. Similarly, Gresty and Halmag yi'? described two patients with congenital nystagmus who reported that head nodding helped them to see. In one of these patients, eye and head movement recordings showed that the nystagmus disappeared during the rhythmic head movements. However, Gresty and Halmag yi found many more patients with congenital nystagmus in whom the head nodding appears to be an involuntary tremor that does not contribute to improvement in vision. It is noteworthy that patients with spasmus nutans and brain pathology show the same ability to suppress the nystagmus by head nodding . Despite the relatively small number of patients, this suggests a similar pathophysiological mechanism in patients with benign spasmus nutans and in those with spasmus nutans associated with brain lesions. In summary, our results show that the fine, fast, dissociated nystagmus changes during head nodding to larger, slower, symmetric eye movements with both eyes oscillating at the same amplitude in phase and 1800 out of phase to the head movements. These eye movements correspond to a normal vestibulo-ocular reflex. Therefore, head movements in spasmus nutans are compensatory and are not an involuntary movement of pathologic origin.

References I. Raudnitz RW. Zur Lehre vom Spasmus nutans. Jahrb f. Kinderh 1897;45:145-76. 2. 0sterberg G. On spasmus nutans. Acta Ophthalmol1937;15: 457-67. 3. Norton EWD, Cogan 00. Spasmus nutans. A clinical study of twenty cases followed two years or more since onset. Arch Ophtha1mol 1954;52:442-6.

Gattlab et al . Head Nodding in Spasmus Nutans 4. Gresty M, Leech J, Sanders M, Eggars H. A study of head and eye movement in spasmus nutans. Br J Ophthalmol 1976;60:652-4. 5. Gresty MA, EllJJ. Spasmus nutans or congenital nystagmus? Classification according to objective criteria [letter]. Br J Ophthalmol 1981;65:510-1. 6. Weissmann BM, Dell'Osso LF, Abel LA, Leigh RJ. Spasmus nutans. A quantitative prospective study. Arch Ophthalmol 1987;105:525-8. 7. Gottlob I, Zubcov A, Catalano RA, et aI. Signsdistinguishing spasmus nutans (with and without central nervous system

lesions) from infantile nystagmus. Ophthalmology 1990;97: 1166-75. 8. Lee JB, Reinecke RD. Skin impedance comparisons of electrodes for electro-oculography. J Pediatr Ophthalmol Strabismus 1991;28:87-9. 9. Metz HS, Jampolsky A, O'Meara DM. Congenital ocular nystagmus and nystagmoid head movements. Am J Ophthalmol 1972;74:1131-3. 10. Gresty M, Halmagyi GM. Head nodding associated with idiopathic childhood nystagmus. Ann NY Acad Sci 1981;374:6 14- 8.

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Head nodding is compensatory in spasmus nutans.

Spasmus nutans is defined as asymmetric nystagmus with associated head nodding in childhood. It is not clear whether head nodding is a compensatory me...
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