Journal of Neuro-Ophthalmology, June 1991, Volume 11, Issue 2

Spinocerebellar degeneration with slow eye movements and abducens nerve palsy.

A 51-year-old woman with spinocerebellar degeneration manifested an unusual disorder of eye movements. She presented with bilateral abducens palsy and slow eye movements in the horizontal plane. Slow eye movements typically are seen with supranuclear lesions, whereas abducens palsies are of nuclear or infranuclear origin. This unique combination of eye movement disorders is discussed, as well as other features of ophthalmoplegias associated with spinocerebellar degeneration.

Tournai of Clinical Neuro- 0l'hthalllJollJl/ Y 11( 21: 118- 121. 1991. © 1991 Raven Press, Ltd., New York Spinocerebellar Degeneration with Slow Eye Movements and Abducens Nerve Palsy Bungo Okuda, M. D., Masahiro Yamasaki, M. D., Shuji Hashimoto, M. D., Kiyomi Maya, M. D., and Terukuni Imai, M. D. A 51- year- old woman with spinocerebellar degenera­tion manifested an unusual disorder of eye movements. She presented with bilateral abducens palsy and slow eye movements in the horizontal plane. Slow eye move­ments typically are seen with supranuclear lesions, whereas abducens palsies are of nuclear or infranuclear origin. This unique combination of eye movement dis­orders is discussed, as well as other features of ophthal­moplegias associated with spinocerebellar degenera­tion. Key Words: Spinocerebellar degeneration- Slow eye movements-- Abducens nerve palsy. From the Department of Neurology, Kitano Hospital, Osaka, Japan. Address correspondence and reprint requests to Dr. Bungo Okuda at Fifth Department of Internal Medicine. Hyogo Col­I" ge n( Medkine, 663 Nishinomiya, Japan. 118 Since Wadia and Swami's report in 1971 ( 1), slow eye movements have been frequently re­ported in association with spinocerebellar degen­eration ( 2- 5). Slow eye movements are defined as selectively impaired and slowed saccadic eye movements, usually considered as a supranuclear disorder of eye movement. Despite the slowing or loss of horizontal saccades, pursuit movements are in most cases preserved over the full range. How­ever, there are cases of spinocerebellar degenera­tion with slow eye movements presenting as a lim­ited range of eye movements ( 6) or slowing of eye movements in the vertical plane ( 7). On the other hand, few cases of spinocerebellar degeneration have been reported showing eye movement abnor­malities of neurogenic ( 8) or myogenic ( 9) origin. It is evident that various types of oculomotor defects have been associated with spinocerebellar degen­eration. We wish to report a case of spinocerebellar degeneration with both a supranuclear oculomotor defect ( in the form of slow eye movements) and nuclear or infranuclear abducens nerve palsies. CASE REPORT The patient was a 51- year- old woman without familial or personal history of any prior neurologic disorders. Three years before admission to our de­partment, she noted the onset of a tremor in the right hand when writing and an unsteady gait. At the same time she became aware of a tingling sen­sation in the left leg below the thigh and a gradual loss of temperature sense in both legs. One month later diplopia developed, and she was admitted to a university hospital, where she remained for ap­proximately one year. Her symptoms did not im­prove, and a family member drew attention to the manifest esotropia in this patient. Her state was SPINOCEREBELLAR DEGENERATION 119 subsequently complicated by bilateral deafness and tinnitus. The gait disturbance gradually pro­gressed, and within one and a half years after on­set of the disease she became unable to walk with­out support. When dysarthria became apparent, she was admitted to the Department of Neurology, Kitano Hospital. General physical examination revealed no ab­normalities other than a systolic murmur at the cardiac apex. On neurologic examination the pa­tient was well oriented and cooperative, but her speech was ataxic. Visual acuity, visual fields, and optic fundi were normal. The primary position of the right eye was in the midline, but the left eye was esotropic. Abduction of both eyes was mark­edly limited. Vertical eye movements were fully preserved and convergence was normal ( Fig. 1). Horizontal pursuit movements and saccades were slowed, especially the latter. Neither head turning nor blinking accompanied the saccades. Vertical eye movements were not slowed. Neither optoki­netic stimulation nor cold caloric testing evoked any deviation of the eyeballs. The horizontal ocu­locephalic reflex induced only adduction of the eyes. Bell's phenomenon was normally intact. The pupils were of equal size at 3 mm and responded sluggishly to light, but the near reflex was pre­served. The eyelids were not ptotic. Bilateral neu­rosensory deafness was noted, but other cranial nerves were intact. Muscle tone and power were normal, without muscular atrophy or fascicula­tion. The deep tendon reflexes were diminished in the upper limbs and completely absent in the lower limbs. Primitive reflexes were negative, while the Babinski response was positive on both sides. Superficial sense in the four limbs was im­paired in a glove- stocking manner and vibration sense was diminished in both lower limbs, while position sense was preserved. Limb coordination and equilibrium were severely disturbed. The pa­tient was quite ataxic on finger- to- nose and heel­to- knee testing. Sitting induced trembling of the head and trunk, and standing was difficult with­out support. Bladder and rectal function were nor­mal. Routine blood chemical examination and urinal­ysis were normal. Glucose tolerance test, thyroid function, and serum fatty acid fraction were nor­mal. The cerebrospinal fluid contained 4 mononu­clear cells/ mm3 , 57 mg/ dl protein and 70 mg/ dl glu­cose. Brain computerized tomography and electro­encephalogram demonstrated no abnormality, but on magnetic resonance imaging there was mild cerebellar atrophy. Electromyography ( EMG) showed neurogenic changes in the upper and lower limbs, mainly in the form of polyphasic waves. Nerve conduction velocity of peripheral nerves was within normal limits ( median nerve MCV 55.7, SCV 54.2; peroneal nerve MCV 42.5; sural nerve SCV 50.8 m/ s). Biopsy of the sural nerve showed a striking reduction of large diame­ter myelinated fibers, and also indicated chronic axonal degeneration. A tensilon test was negative. Forced duction test of external ocular muscles was normal. Auditory evoked potential could not be elicited, but visual evoked potential was normal. FIG. 1. Eye movements in all fields of gaze. Note bilateral abducens palsy, with nor­mal vertical gaze. JClin Neuro- ophthalmol. Vol. 11, No. 2, 1991 120 B. OKUDA ET AL. Electro- oculogram revealed that in the horizontal plane pursuit movements and saccades were slow, particularly the latter. Vertical pursuit movements were saccadic, but saccades were not slow in the vertical plane ( Fig. 2). DISCUSSION Saccades and pursuit movements are controlled by different mechanisms; slow eye movements are caused by selective impairment of saccades, the fast component of eye movements. Though there is some debate regarding which lesion is respon­sible for slow eye movements, the principal lesion is thought to be in the burst neurons of the para­median pontine reticular formation ( 4). In most cases with slow eye movements, pursuit move­ments are preserved over the whole range, and convergence is unaffected, despite slowing or loss of saccades in the horizontal plane. However, Warabi ( 7) reported siblings of patients with spinocerebellar degeneration who had slow sac­cades in the vertical direction rather than in the horizontal and surmised that the brain stem center for horizontal saccades and for vertical saccades exist separately. Neurological disorders with slow eye movements other than spinocerebellar degen­eration include Huntington's chorea ( 10), progres­sive supranuclear palsy ( 11), Wilson's disease ( 12), and ataxia telangiectasia ( 13). Cases with slow eve movements have been reported even in amvo­trophic lateral sclerosis ( 14), which is gener~ lly held not to involve oculomotor sYstems. It is fore­seen that a list of neurologic di; orders with slow EOG pursuit movement I nlegftt'rt horizontal target O. 5Hz EOG saccadic movement horizontal eye movements will become larger, and it is hoped that the lesion responsible for slow eye move­ments will be determined. Spinocerebellar degeneration with slow eye movements was first reported as viscosity by Gar­cin in 1958 ( 15). In 1961 Jampel reported a family that showed the combination of progressive oph­thalmoplegia associated with slow eye move­ments, retinal pigmentation, and hereditary spinocerebellar ataxia. In India in 1971, Wadia ( 1) reported heredofamilial spinocerebellar degenera­tion with slow eye movements. Subsequently sim­ilar cases have been reported by Singh et al. ( 2), Koeppen and Hans ( 3), Zee ( 4), and Murphy and Goldblatt ( 5). In these cases, horizontal saccades were selectively impaired or more severely slowed than pursuit movements, while there was no lim­itation of eye movements, and reflex activities on doll's head maneuver and caloric test were pre­served. On the contrary, the case reported by Jam­pel presented vertical gaze palsy and slowing of lateral saccades, followed by complete lateral gaze palsy. Slow eye movements have been explained as su­pranuclear ophthalmoplegia, based on full eye movements evoked by doll's head maneuver and caloric stimulation. In the present case, however, abduction of the eyes was impaired on voluntary effort, cold caloric test produced no deviation of the eyes, and oculocephalic maneuver elicited only adduction of the eyes. Abnormal response to cold caloric test may well be due to impairment of the acoustic nerve, as well as to neurosensory deaf­ness. Impaired oculocephalic reflex and esotropia FIG. 2. Electro- oculogram showing slow­ing of horizontal pursuit and saccadic movements. SPINOCEREBELLAR DEGENERAnON 121 indicate nuclear or infranuclear abducens nerve palsy in the present case. Spinocerebellar degen­eration with nuclear or infranuclear ophthalmople­gia has been reported by Yamamura et a1. ( 8) and Stephens et a1. ( 9). Yamamura et a1. reported a case of spinocerebellar degeneration with progressive external ophthalmoplegia and peripheral neurop­athy. Pathological findings suggested that oph­thalmoplegia was of neurogenic origin. Stephens et a1. described a family with Friedreich's ataxia and Charcot- Marie- Tooth disease associated with external ophthalmoplegia. Postmortem examina­tion of one case showed that the ophthalmoplegia was due to a primary ocular myopathy. The above­mentioned cases of spinocerebellar degeneration with nuclear or infranuclear ophthalmoplegia were characterized by progressive external ophthal­moplegia and ptosis, whereas there was no men­tion of slow eye movements in these cases. In the present case, it is unlikely that slowing of eye movements is caused by abducens nerve palsy, be­cause eye movements are slowed in adduction as well as in abduction. However, the combination of supranuclear dysfunction producing slow eye movements with bilateral nuclear or infranuclear involvement of the abducens nerves in this patient may also be explained by an anatomically more­restricted lesion in this patient. It is not uncommon to find clinical signs that are both supranuclear and nuclear in origin in patients presenting pontine syndromes because the lesion producing a supra­nuclear manifestation may be anywhere from a minute distance above the nuclear involvement up to and including the cortex. Thus, there are other possible explanations for the defects found in this patient. The horizontal gaze centers for saccadic movements lie in the paramedian pontine reticular formation just rostral to the sixth nerve nuclei; those for smooth pursuit in the dorsal pons are just caudal to the sixth nerve nuclei; and all are contig­uous with the vestibular nuclei. Thus, a very local­ized lesion in the region of the pontomedullary junction could have produced the majority of this patient's complaints. Another possibility is that there is a combination of profound bilateral ab­ducens palsies with subtle pareses of horizontal conjugate gaze, so that the former prohibited ab­duction, whereas the latter led to slowing of ad­duction movements on attempted horizontal gaze. Again, this could have been due to a rather focal lesion in the pontine tegmentum. We cannot ex­clude a somewhat more rostral dysfunction than the midpontine level in this patient, but the integ­rity of vertical gaze is consistent with integrity of the pathways at the mesencephalic level. At any rate, the outstanding feature of the present case is the concurrence of slow eye movements with bi­lateral abducens nerve palsies which have, to our knowledge, hitherto been unappreciated in spino­cerebellar degeneration. Several cases of spinocer­ebellar degeneration with peripheral neuropathy have been reported ( 16,17). The EMG and the sural nerve biopsy of the present case confirmed the presence of polyneuropathy, but the causal rela­tionship between abducens nerve palsy and poly­neuropathy remained unclear. REFERENCES 1. Wadia NH, Swami RK. A new form of heredofamilial spinocerebellar degeneration with slow eye movements. Brain 1971; 94: 359- 74. 2. Singh BM, Ivamoto H, Strobos RJ. Slow eye movements in spinocerebellar degeneration. Am JOphthalmoI1973; 76: 237­40. 3. 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