THE ROLE OF ERG/VEP AND RECORDINGS IN CHILDREN WITH OCULAR MOTOR APRAXIA

FATIMA S. SHAWKAT, CHRISTOPHER M. HARRIS, DAVID S. I. TAYLOR and ANTHONY KRISS London

SUMMARY several reports of OMA or saccade failure occurring Ocular motor apraxia (OMA) is characterised by an congenitally, with no other clinical entity?-5 How­ intermittent inability to initiate voluntary sacca des, and ever, it can also occur as part of a wider neurological a failure to produce optokinetic and vestibular quick disorder: for example with structural brain abnorm­ phases. Some patients have no other abnormalities alities, such as agenesis of the corpus callosum6 and (idiopathic OMA), whereas in others it appears vermis hypoplasia;7 with neurodegenerative condi­ associated with a variety of neurological conditions tions;8 and with acquired neurological disease such as which may affect the sensory visual pathway. Electro­ posterior fossa tumours,9 ataxia telangiectasia,lO retinograms (ERGs), flash and pattern visual evoked fronto-parietal lesions,l1.l2 occipital cortex lesions,13 potentials (VEPs) and eye movements were assessed in cerebellar and brains tern neoplasm14 and olivoponto­ 53 children with OMA (age range 17 days to 14 years) cerebellar degeneration. 15.16 The inability to gener­ to determine their efficacy in helping to distinguish ate saccades often leads to the development of between idiopathic and non-idiopathic cases. Seven patients (13.2%) had idiopathic OMA and the remain­ compensatory behaviour to shift direction of ; ing 46 (86.8%) had other associated clinical conditions. this includes headthrusting, blinking and tilted head All patients had episodes of absent quick phases ('lock posture, which enables the use of vertical eye up') during optokinetic (OKN) and/or movements that are usually unaffected. Hypometric vestibular testing. Flash ERGs were abnormal in-only saccades, poor optokinetic nystagmus (OKN) and 7 patients (13.2%); 6 had syndromes involving a contraversive deviation of the eyes on vestibular pigmentary retinopathy (Joubert's, Bardet-Biedl, testing (due to the failure of OKN and vestibular infantile Refsum's, Kearns-Sayre's), and the seventh quick phases) have also been described in ,1 , had a cone dystrophy with vermis hypoplasia. VEPs OMA. 2 7 18 were normal in all 7 patients with idiopathic OMA. Earlier electrophysiological studies in patients with Thirty-three (72%) patients with OMA in association congenital OMA reported normal flash and pattern with neurological conditions had abnormal VEPs and visual evoked responses (VEPs) and electroretino­ 13 had normal VEPs (28%). There was a significant grams (ERGs).4,J3 However, a recent studiO found 2 positive correlation between VEP abnormality and poor OKN gain. VEPIERG testing and eye movement of 5 children diagnosed with 'Cogan's ocular motor studies are useful when OMA is suspected as they help apraxia' to have absent ERGs but normal flash in distinguishing isolated idiopathic cases from those VEPs. On the basis of these findings the authors with more widespread neurological abnormalities. suggest the existence of two variants of the condition, one with and the other without retinal dysfunction. Coganl in 1952, first used the term congenital ocular This prompted us to re-examine data from 53 motor apraxia (OMA) to describe the clinical signs children in whom saccade failure had been objec­ of 4 patients who had difficulties in generating tively identified and electrophysiological measure­ horizontal saccades. Since then, there have been ments had been made. Electro-oculography (EO G) and video monitoring was used to assess the eye Correspondence to: Fatima S. Shawkat, Department of movements. The extent of saccade failure was , Great Ormond Street Hospital for Children, London WCI 3JH, UK. Fax: 0171 829 8647. quantified and related to the YEP and ERG findings.

Eye (1996) 10,53-60 © 1996 Royal College of Ophthalmologists 54 F. S. SHAWKAT ET AL.

PATIENTS AND METHODS phase) was difficult to assess accurately because of Subjects difficulties in eliciting saccades for calibration. Over a period of 2 years, 53 patients referred to the However, it was clearly evident that in certain cases ophthalmology department with OMA underwent OKN was of extremely low gain or absent when both ERGNEP assessment and formal eye move­ compared with control subjects recorded in our 19 ment recording. Age at testing ranged from 17 days laboratory. Thus, OKN gain abnormalities were

0 = 1 = to 14 years, with a mean age of 3.5 years. There were qualitatively ordinally scaled into normal, 1 25 males and 28 females. Forty-one patients (77.4%) abnormal. An abnormal OKN score of was given to 25 were scanned (24 MRI, 17 CT). those with conspicuously reduced gain at deg/s Patients were divided into groups on the basis of stimulus speeds or when OKN was totally absent. clinical history and signs, and diagnostic findings VOR was tested by rotating the patient on the (neuro-imaging and biochemical studies). This Barany chair while in complete darkness. The chair 2 categorisation was carried out independent of, and was accelerated at 18 deg/s to a speed of 80 degls prior to, the VEP/ERG assessment. Seven children and this speed was maintained for 40 seconds before 2 40 had no other clinical abnormalities apart from the decelerating at 18 deg/s to rest. After another OMA and were labelled as having 'idiopathic' OMA. seconds at rest, the chair was rotated in the opposite Two children had normal MRI results with other direction. Per- and post-rotatory vestibular nystag­ symptoms: one had early onset vertical nystagmus mus were recorded in both directions. and microphthalmos, and the other was markedly hypotonic, developmentally delayed with gastro­ Electrophysiology 13 oesophageal reflux. There were patients with VEPs were recorded using silver/silver chloride EEG non-progressive neurological deficits secondary to electrodes placed in a line across the occipital scalp. perinatal or postnatal problems (anoxia, ischaemia or A midline electrode was sited at Oz (10-20 system, meningitis). Thirteen children had progressive, approximately 3 cm above the inion) and lateral neurodegenerative conditions (including Gaucher's electrodes were placed midway between the Oz disease, Krabbe's leucodystrophy, GM gangliosido­ 1 electrode and the ear. All occipital electrodes were sis, infantile Refsum's disease, Pelizaeus Merzbacher referred to a common frontal electrode at Fz (10-20 disease, propionic acidaemia) and 18 patients had system). The electroretinogram (ERG) was recorded structural brain anomalies (including agenesis of the from a lower eyelid skin electrode also referred to Fz. corpus callosum, vermis cyst, vermis hypoplasia in Full-field pattern reversal VEPs were elicited using a isolation, and in association with Joubert's syndrome, checkerboard pattern presented on a large TV Dandy Walker malformation, hydrocephalus, hemi­ display (sub tending 28 degrees horizontal by 21 megalencephaly, porencephalic cyst). degrees vertical). Stimulus check-sizes ranged from Neuro-radiological examination revealed a wide 25 minutes to 7 degrees. A Grass PS22 photic range of abnormalities the most common of which stimulator, held 15 cm in front of the eye, was used were brainstem abnormalities, cerebellar abnormal­ to elicit flash VEPs and mixed cone/rod ERGs under ities (particularly those involving the vermis), fully darkened laboratory conditions. delayed or absent myelination, and agenesis of the corpus callosum. Patients with idiopathic OMA had RESULTS normal scans. Eye Movements Clinical examination identified head thrusting beha­ Eye Movements viour in 30 of the patients (57%). The remaining 23 Horizontal eye movements were recorded using dc (43 %) did not head thrust and OMA was identified EOG. Silver/silver chloride electrodes were attached during the formal eye movement recording. The with tape at the outer canthi of either eye with a majority of patients with idiopathic OMA (86%) reference electrode at the mid-forehead. Older showed head thrusting behaviour; in contrast, it was patients sat alone in a Barany chair; younger evident in only 10% of patients with associated patients sat on a parent's lap. The head was neurodegenerative conditions. There was no obvious restrained by a head rest, or was held by the trend in children with structural malformations of the parent. Video monitoring of the patient was carried central nervous system (CNS), of whom 56% out through the entire recording session. Infra-red exhibited head thrusting, whereas fewer (30%) monitoring was used when testing the vestibulo­ patients with peri- or postnatal problems showed ocular reflex (VOR) in absolute darkness. this compensatory behaviour. OKN was elicited by rotating a brightly coloured Saccade failure during OKN and VOR testing was and patterned, full-field curtain around the patient. identified as episodes of absent quick phases (Fig. 1). Leftward and rightward OKN at speeds of 25 and 50 When quick phases at the end of an OKN or deg/s were recorded. Gain of OKN (slope of the slow vestibular nystagmus slow phase are absent the eyes OCULAR MOTOR APRAXIA 55

A. OKN to Leftward Curtain Rotation

R

L

B. VOR to Rightward Chair Rotation

R

L

Fig. 1. EOG traces of optokinetic nystagmus (A) elicited by leftward curtain rotation at a speed of 25 degls, and vestibular nystagmus (B) elicited by chair rotation (open arrow) at 80 degls. Episodes of 'lock up' (filled arrows), where there is failure in generating quick phases, can be clearly discerned during both tests.

remain in extreme lateral deviation in the direction infantile Refsum's, and 1 with Kearns-Sayre's of curtain rotation, or in the opposite direction to syndrome. The seventh patient had attenuated chair rotation. We call this phenomenon 'lock up', ERGs to bright white and red flash, but ERGs and this provides a measure of the severity of were preserved to dim blue flash, indicating retinal saccade failure. It is measured by the percentage of dysfunction primarily affecting the cones. time the eyes remained in extreme lateral deviation Flash and pattern VEPs were compared with age­ during OKN testing at the two speeds (25 and 50 appropriate laboratory norms. Thirty-eight patients deg/s) and during VOR testing. Measures of lock up (72%) had abnormal VEPs (that is attenuated and/or are therefore relative and independent of calibration. delayed). In 8 patients latencies were significantly Saccade failure was usually intermittent and normal prolonged (>2.5 SD) and in the remainder VEPs quick phases were detected in the majority of were significantly attenuated «2.5 SD). The seven patients. All patients who locked up during OKN cases with idiopathic OMA had normal VEPs (mean testing, invariably locked up during VOR testing. for 50' checks = 16.7 fLV at 106 ms; mean for flash = There were no significant differences (ANOVA, 24.1 fLV at 102 ms). p<0.5) in the extent of lock up between idiopathic Patients with neurological conditions could be OMA patients and patients with other associated divided into three main groups: (1) 13 patients had neurological problems. peri/postnatal problems, of whom 80% had abnormal OKN was also evaluated by assessing the gain of VEPs; (2) 1 8 patients had CNS structural anomalies, the slow phases at 25 deg/s stimulus speed. Eighty­ of whom 77% had abnormal VEPs; and (3) 13 one per cent of cases had marked OKN abnormali­ ties. All patients with idiopathic 'congenital ocular patients had progressive neurodegenerative disease, motor apraxia' had normal OKN gain, but there was of whom 85 % had abnormal VEPs. There were no no statistical difference (Kruskal-Wallis, p<0.5) conspicuous differences in YEP amplitude deficits between those with idiopathic OMA and those with between these general diagnostic categories; how­ OMA in association with other conditions. ever, YEP latencies were particularly prolonged in the neurodegenerative group of patients. This was Electrophysiology particularly marked for VEPs to pattern reversal ERGs were not detectable or significantly attenuated stimulation (Fig. 2). It can be seen from Fig. 2 that in 7 patients. Six of these patients with markedly pattern VEPs in the neurodegenerative patient attenuated scotopic and photopic ERGs had a group are delayed when compared with patients diagnosis in which there was a pigmentary retino­ with idiopathic OMA, or OMA associated with CNS pathy: 3 with Joubert's, 1 with Bardet-Biedl, 1 with structural malformations. Children with peri/post- 56 F. S. SHAWKAT ET AL.

150 �------,

140

130

Mean 120 Latency (ms.) 110 1llII2S' checks

100 t;illso' checks � 1 00' checks 90 D 3 deg. checks 80 137deg. checks

70_�"",-,__ _Flash Idiopathic OMA Structural Peri/Post-natal Diagnostic Category

Fig. 2. Bar chart of mean pattern and flash V EP latencies for the different diagnostic categories. It can be seen that patients with idiopathic OMA have latencies within the normal range, whereas those with neurodegenerative conditions have the most prolonged latencies, particularly when the smaller check-sizes are used. natal problems tended to have prolonged VEPs to and VOR testing and either YEP amplitude or the smaller check-sizes. latency. Table I compares the mean amplitudes and The occurrence of head thrusting in an OMA latencies for our laboratory controls with those of patient showed a significant positive correlation with the 7 patients with idiopathic OMA, the 38 patients the occurrence of an abnormal ERG (Spearman's with abnormal VEPs, and the two sub-groups of r = 0.305, p<0.04) and a negative correlation, that abnormal latencies and amplitudes. Patients with was just beyond the levels of significance, with the idiopathic OMA had VEPs within the normal range. occurrence of a YEP abnormality (r = -0.274, Fig. 3 shows the ERGs and VEPs to flash and P = 0.057. However, analysis of individual YEP pattern (50' checks) stimulation of a patient with parameters showed a significant negative correlation idiopathic OMA, a patient who had suffered between head thrusting and YEP amplitudes to the perinatal hypoxia, a patient with a progressive smallest 25' checks (r = -0.422, p<0.004). This neurodegenerative condition (propionic acidaemia) negative correlation implies that head thrusting was and a child with Joubert's syndrome and retinal less likely to be present in patients with well­ dysfunction. preserved VEPs to the small checks. However, head thrusting is more likely to occur in patients with abnormal ERGs. Eye Movement and Electrophysiological Correlates OKN gain abnormality showed a positive correla­ There were no significant correlations between tion with the occurrence of abnormal VEPs severity of saccade failure (lock up) during OKN (Spearman's r = 0.385, p<0.005). When YEP mea-

Table I. Mean YEP amplitudes and latencies for control subjects. idiopathic OMA patients, OMA patients with general YEP abnormalities and OMA patients divided into those with amplitude and latency abnormalities

OMA and general OMA and OMA and Control subjects Idiopathic OMA abnormal YEPs degraded VEPs delayed VEPs

25' checks 15.2 !Joy :!::1O.7 11.3 !JoV :!:: 5.8 6.9 !Joy :!:: 6.4 5.5!JoV :!:: 6.4 8.3 !JoV :!:: 8.3 106.9 ms :!:: 6.1 109.5 ms :!:: 7.2 124.6 ms :!::22.9 107.9 ms :!::11.6 141.3 ms :!::18.5 50' checks 17.6 !JoV :!::11.1 16.7 !Joy :!:: 9.6 6.5 !Joy :!:: 5.9 5.2 !Joy :!:: 3.5 11.3 !Joy :!:: 9.6 103.3 ms :!:: 4.6 105.9 ms :!:: 4.6 119.3 ms :!::19.3 112.5 ms :!::14.9 142.2 ms :!::14.2 100' checks 14.6 !Joy :!:: 8.0 11.8 !Joy :!:: 6.2 6.2 !JoV :!:: 5.6 5.1 !JoV :!:: 4.5 8.8 !JoV :!:: 7.2 105.7 ms :!:: 4.4 103.2 ms :!::10.1 117.7 ms :!::19.5 110.3 ms :!::16.6 135.2 ms :!::14.1 3° checks 11.6 !JoV :!:: 6.8 8.1 !Joy :!:: 4.6 6.9 !Joy :!:: 5.7 5.3 !Joy :!:: 3.4 11.5 !Joy :!:: 8.2 101.1 ms :!:: 5.6 102.1 ms :!:: 8.1 109.4 ms :!::22.4 108.9 ms :!::11.3 127.2 ms :!::15.1 7° checks 10.7 !Joy :!:: 6.7 8.0 !Joy :!::23 6.0 !Joy :!:: 5.2 4.4 !JoV :!:: 3.3 9.8 !JoV :!:: 7.2 lOLl ms :!:: 6.5 106.7 ms :!:: 5.0 111.7 ms :!::25.3 104.3 ms :!::25.5 129.4 ms :!:: 14.5 Flash YEP 29.5 !JoV :!::13.5 24.1 !Joy :!::11.6 16.1 !Joy :!::19.3 17.3 !JoV :!::21.5 11.6 !Joy :!:: 6.5 90.4 ms :!:: 8.3 102.0 ms :!::22.3 103.1 ms :!::24 98.2 ms :!::23.7 120.3 ms :!::16.7 OCULAR MOTOR APRAXIA 57

A. Idiopathic OMA B. Perinatal Anoxia

Left Eye ERG

Right Eye ERG

Flash YEP

50' YEP

I , I, I , I , I , I , I , I I I , I , I I , , I , I , I , I , I , I , I , I , I , o 90 180 270 o 90 180 270 msec 110!1v msec +

C. Neurodegenerative D. Joubert Syndrome

Left Eye ERG

Right Eye ERG

Flash YEP

50' YEP

, I, I, I , I , I , I I I I I I I I I I I I, I , I , I I I , I , I I I , I , I I o 90 180 270 o 90 180 270 msec msec

Fig. 3. Left and right eye ERGs and binocular flash and 50' pattern VEPs from a patient with idiopathic OMA (AJ, a patient who had perinatal anoxia (BJ, a patient with propionic acidaemia from the neurodegenerative group and a patient with Joubert's syndrome (DJ.

sures were analysed separately, positive significant OKN deficits (r = -0.283, p<0.05): greater OKN correlations were found between OKN gain deficits deficits are likely to be found in patients with and the latencies of VEPs to the three smaller attenuated flash VEPs.

checks: 25' (r = 0.396, p<0.004), 50' (r = 0.379,

p<0.008) and 100' checks (r = 0.301, p

check-sizes, and negatively with YEP flash ampli­ 11. Holmes G. Spasm of . Trans Ophthalmol Soc tudes. Prolonged latencies and attenuated flash VEPs UK 1930;50:253-62. 12. Hecaen H, de Ajuriaguerra J. Balint's syndrome were found in patients with OMA in association with (psychic paralysis of visual fixation). Brain 1954; neurological conditions and in particular with 77:373-400. neurodegenerative and acquired diseases. In such 13. Reed HR, Israels S. Congenital ocular motor apraxia: a patients, global brain abnormalities are common and form of horizontal gaze palsy. Br J Ophthalmol likely to involve parietal cortex, brains tern and 1956;40:444-8. cerebellum. Thus, this association between YEP 14. Zaret CR. Behrens MM, Eggers HM. Congenital ocular motor apraxia and brainstem tumour. Arch and OKN abnormalities can be expected. However, OphthalmoI1980;98:327-30. these results do not necessarily imply that OMA has 15. Moe Pc. Ocular motor apraxia in three families. a cortical origin. 1971;221:451. This study has demonstrated the value of electro­ 16. Aicardi J, Barbosa C, Andermann E, et al. Ataxia­ physiological and eye movement testing in separating ocular motor apraxia: a syndrome mimicking ataxia­ telangiectasia. Ann NeuroI1988;24:497-502. patients with idiopathic OMA from those with OMA 17. Zee DS, Chu FC, Keigh RJ, et al. Blink-saccade as part of a wider and more severe neurological synkinesis. Neurology 1983;33:1233-6. condition. We found no evidence of an idiopathic 18. Shawkat FS, Harris CM, Russell-Eggitt I, et al. OMA variant with retinal involvement; if ERGs or Oculomotor and neuroradiological correlates in con­ VEPs are abnormal, then further investigation is genital saccade palsy (ocular motor apraxia). Invest Ophthalmol Vis Sci 1994;35:2034. needed to identify the underlying cause. Various 19. Harris CM, Jacobs M, Taylor D. The development of neurodegenerative diseases, perinatal insults and bi-ocular and monocular optokinetic gain from 1 to 7 cerebellar and brainstem anomalies appear to months. Invest Ophthalmol Vis Sci 1994;35:2655. predispose the patient to intermittent saccade fail­ 20. Magni RL, Spadea A, Pece A, et al. Electroretino­ ure. This may not be easily detectable without OKN graphic findings in congenital oculomotor apraxia (Cogan's syndrome). Doc Ophthalmol 1994;86:259-66. or vestibular testing. Eye movement examination 21. Campo RV, Aaberg TM. Ocular and systemic and ERG/VEP testing are complementary non­ manifestations of the Bardet-Biedl syndrome. Am J invasive investigations which together give valuable Ophthalmol 1982;94:750-6. information for diagnosis. 22. Lavy T, Harris CM, Shawkat FS, et al. An ERG, YEP, and eye movement assessment of children with Bardet­ We wish to thank the Iris Fund for their support. Biedl syndrome. In: Lennerstrand G, editor. Update on strabismus and pediatric ophthalmology. Boca Raton, Key words: ERG, Eye movements. Ocular motor apraxia. YEP. FL: CRC Press, 1995:549-52. 23. Kearns TP, Sayre GP. Retinitis pigmentos a, external ophthalmoplegia and complete heart block: unusual syndrome with histologic study in one of 2 cases. Arch REFERENCES Ophthalmol 1958;60:280-9. et al. 1. Cogan DG. A type of ocular motor apraxia presenting 24. Weleber RG, Tongue AC, Kenneway NG, jerky head movements. Trans Am J Ophthalmol Ophthalmic manifestations of infantile phytanic acid Otolaryngol 1952;56:853-62. storage disease. Arch OphthalmoI1984;102:1317-21. 2. Zee DS, Yee RD, Singer HS. Congenital ocular motor 25. Moser HW. Peroxisomal disease. Adv Pediatr 1989; apraxia. Brain 1977;100:581-99. 36:1-38. 3. Godel V, Nemet P, Lazar M. Congenital ocular motor 26. Metz HS, Meshel L. Ocular saccades in progressive apraxia: familial occurrence. Ophthalmologica 1979; external ophthalmoplegia. Ann Ophthalmol 1974; 179:90-3. 6:623-8. 4. Gittinger JW, Sokol S. The visual evoked potential in 27. Ringel SP, Wilson WB, Barden MT. Extraocular the diagnosis of congenital ocular motor apraxia. Am J muscle biopsy in chronic progressive external ophthal­ OphthalmoI1982;93:700-3. moplegia. Ann Neurol 1979;6:326-39. 5. Rosenberg ML, Wilson E. Congenital ocular motor 28. Leigh RJ, Zee DS. The neurology of eye movements, apraxia without head thrusts. J Clin Neuro-ophthalmol 2nd ed. Philadelphia: FA Davis, 1991. 1987;7:26-8. 29. Daroff RB, Solitaire GB, Pincus JH, et al. Spongioform 6. Orrison WW, Robertson Wc. Congenital ocular motor encephalopathy with chronic progressive external apraxia: a possible disconnection syndrome. Arch ophthalmoplegia: central ophthalmoplegia mimicking Neurol 1979;36:29-31. ocular myopathy. Neurology 1966;16:161-9. 7. et al. et al. Lambert SR, Kriss A, Gresty M, Joubert 30. Hrbek A, Kariberg P,� Kjellmer I, Clinical syndrome. Arch OphthalmoI1989;107:709-13. application of evok d electroencephalogra�hic . 8. Cogan DB, Chu FC, Re\ug,o\dD, et al. Ocu\at l1\O\Gt te��Gn�e� \n ne'Vl-bGm \l\hn\�. \. �erinata\ asphyx�a. signs in some metabolic diseases. Arch Ophthalmol Dev Med Child Neurol 1977;19:34-44. 1981 ;99:1802-8. 31. Hakamada S, Watanabe K, et al. 9. Hara K ' The Lyle DJ. A discussion of ocular motor apraxia with a �volution ?f visual and auditory evoked potentials in case presentation. Trans Am Ophthalmol Soc 1961; mfants WIth perinatal disorder. Brain Dev 1981; 59:274-85. 3:339-44. 10. Stell R, Bronstein et al. AM, Plant GT, Ataxia 32. Tarlo MJ, Murphy � . WJ, Whyte HE. Prognostic telangiectasia: a reappraisal of the ocular motor �ehabIhty of SEPs and VEPs in asphyxiated term features and their value in the diagnosis of atypical mfants. Dev Med Child NeuroI1992;34:507-15. cases. Mov Disord 1989;4:320-9. 33. Taylor MJ. Evoked potentials in paediatrics. In: 60 F. S. SHAWKAT ET AL.

Halliday AM, editor. Evoked potentials in clinical 41. Jacobs M, Shawkat F, Harris CM, et at. Eye movements testing, 2nd ed. London: Churchill Livingstone, 1993: and electrophysiological findings in an infant with 489-521. hemicerebral . Dev Med Child Neurol 34. Vivian AJ, Harris CM, Kriss A, et al. Oculomotor signs 1993;35:431-5. in infantile Gaucher disease. Neuroophthalmol 1993; 42. Troost BT, Daroff RB, Weber RB, Dell'Osso LF. 13:151-5. Hemispheric control of eye movements. II. Quantita­ 35. Markand ON, Garg BP, DeMeyer WE, et at. tive analysis of smooth pursuit in a hemispherectomy Brainstem auditory, visual and somatosensory evoked patient. Arch Neurol 1972;27:449-52. potentials in leukodystrophies. Electroencephalogr Clin Neurophysiol 1982;54:39-48. 43. Sharpe JA, Lo AW. Voluntary and visual control of 36. Ehle AL, Sklar F. Visual evoked potentials in infants the vestibuloocular reflex after cerebral hemidecortica­ with hydrocephalus. Neurology 1979;29:1541-4. tion. Ann Neurol 1979;10:164-72. 37. Guthkelch AM, Sclabassi RJ, Vries JK. Changes in the 44. Baloh RW, Sills A, Honrubia V. and visual evoked potentials of hydrocephalic children. optokinetic nystagmus: results of quantitative testing in 1982;11:599-602. patients with well-defined nervous system lesions. Ann 38. Watanabe K, Yamada H, Hara K, et al. Neurophysio­ Otol Rhinol Laryngol 1977;86:108-14. logical evaluation of newborns with congenital hydro­ 45. Kjallman L, Frisen L. The cerebral ocular pursuit cephalus. Clin Electroencephalogr 1984;15:22-31. pathways: a clinicoradiological study of small-field 39. Thurston SE, Leigh RJ, Crawford T, et at. Two distinct optokinetic nystagmus. J Clin Neuro-Ophthalmol deficits of visual tracking caused by unilateral lesions of ] 986;6:209-14. cerebral cortex in humans. Ann Neurol 1988;23: 266-73. 46. Heide W, Koenig E, Dichgans J. Optokinetic nystag­ 40. Morrow MJ, Sharpe JA. Cerebral hemispheric locali­ mus, self-motion sensation and their after-effects in sation of smooth pursuit asymmetry. Neurology patients with occipito-parietal lesions. Clin Vis Sci 1990;40:284-92. 1990;5:145-56.