Journal ofNeurology, Neurosurgery, and Psychiatry 1990;53:519-521 519

SHORT REPORT J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.6.519 on 1 June 1990. Downloaded from

Vermal infarct with pursuit eye movement disorders

Charles Pierrot-Deseilligny, Pierre Amarenco, Etienne Roullet, Rene Marteau

Abstract the vermis was affected (lobules VI to X), Severe deficits of foveal smooth pursuit namely the clivus, the folium, the tuber, the and optokinetic nystagmus in all direc- pyramis, the uvula and the nodulus (fig 1). tions were electro-oculographically The inferior part of the left cerebellar hemi- recorded in an 80 year old woman. Mag- sphere was also damaged. The flocculus, the netic resonance imaging (MRI) showed different cerebellar peduncles and the brain- an infarct involving the postero-inferior stem were apparently spared. Moreover, the part of the vermis (lobules VI to X) and brainstem did .not appear to be compressed. a portion of the left cerebellar hemi- There was only slight diffuse atrophy in the sphere, with apparent preservation of cerebral hemispheres, without hydrocephalus. the flocculus and the brainstem. The role The posterior headache lasted one day, ver- of the vermal lesion in these pursuit eye tigo and left lateropulsion on walking cleared movement disorders is discussed. up within several days and the left tonic ocular deviation progressively disappeared within ten days. It has recently been shown that, besides the flocculus, the posterior part of the vermis Oculographic study (especially lobules VI and VII) is involved in Eye movements were recorded on the the control of pursuit eye movements in the eleventh day after the onset of the symptoms, monkey.'2 Our case reports for the first time a while the patient was fully alert, cooperative recent ischaemic lesion of the posterior vermis and attentive. She was not taking any other and eye movement recordings, suggesting that medication than acetyl-salycylic acid. Direct- this cerebellar structure is also involved in the current electro-oculography (EOG) was used, control of pursuit eye movements in humans. for each eye separately, in darkness, with the head immobilised. There was no nystagmus when the patient looked straight ahead or in Case report the extreme positions. With eyes open, there An 80 year old woman experienced sudden was no tonic deviation, but with eyes closed http://jnnp.bmj.com/ vertigo, with unsteadiness, vomiting, pos- there was a left conjugate eye deviation. terior headache, without auditory symptoms. Horizontal eye movements Saccades to com- For the previous five years she had received mand and visually guided saccades had nor- treatment for high blood pressure. On admis- mal latency, velocity and amplitude (fig 2A). sion her blood pressure was 160/80 mm Hg, In particular, no dysmetria was observed, her pulse rate was irregular at 1 15 per minute. whatever the position of the visual target (at

There was no drowsiness. Vertigo increased 5°, 150, 250 and 350 away from the midline) on October 1, 2021 by guest. Protected copyright. on change of head posture. Finger-to-nose and direction of saccades (left, right, or and rapid alternating movements of the left returns to the midline). upper limb were ataxic. Both eyes and head Foveal pursuit of a small luminous target were tonically deviated leftwards. However, moving sinusoidally at peak-to-peak ampli- oculocephalic movement allowed both eyes to tude of 500 was largely saccadic in both direc- Service de Neurologie, overcome this tonic deviation and reach the tions (fig 2B). Both catch-up saccades and Hopital Saint-Antoine extreme right position. Cranial nerves were smooth portions were larger leftwards than and Unite INSERM unaffected. There were no sensory or motor rightwards but smooth eye movement veloci- 289, Hopital de la reflexes were normal and Salpetriere, Paris, deficits, all tendon ties were similar in both directions. Smooth France plantar responses flexor. The electrocar- movement gains (ratio of peak eye velocity to C Pierrot-Deseilligny diogram showed atrial fibrillation. CT scan peak stimulus velocity) were low, bilaterally, P Amarenco on the of admission was to an control E Roullet performed day compared age-matched group, R Marteau normal. In particular, there was no hydro- for the two frequencies of stimulation used that there was Correspondence to: cephalus, which suggested (table). These gains were less than the lower Dr C Pierrot-Deseilligny, no compression of the brainstem by the limit of the normal range (control mean-2 H6pital de la Salpetriere, 47 boulevard de l'Hopital, cerebellum. SD). 75651 Paris cedex 13, France MRI performed four days later showed an Optokinetic nystagmus (OKN) was elicited Received 14 June 1989 infarct in the territory of the left posterior and using alternating black and white stripes mov- and in revised form 22 September 1989. inferior cerebellar artery, mainly the territory ing at 30°/s across a screen covering 60° of the Accepted 30 October 1989 of its medial branch.3 All the inferior part of visual field. It was severely impaired (fig 2C), 520 Pierrot-Deseilligny, Amarenco, Roullet, Marteau

Figure I Magnetic without any build up after sustained stimula- resonance imaging (T2). tion (1 minute). Slow phase gains were very J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.6.519 on 1 June 1990. Downloaded from A and B: horizontal to the control sections passing through low, bilaterally, compared the mid-pons and the group (table). These gains were also less than upper medulla, the lower limit of the'normal range. respectively. C: coronal reflex was tested section passing through the Vestibulo-ocular (VOR) posterior part of the by pseudo-sinusoidal rotation of the chair at cerebellum. Note the peak-to-peak amplitude of 450 while the infarct in the territory of looked at a small stationary light. The the left posterior and patient inferior cerebellar artery, movement elicited, a combination of VOR involving the vermis and smooth pursuit, appeared to be (lobules VI to X) and the qualitatively normal, with a gain near 1 (fig postero-inferior part of the left cerebellar hemisphere. 2D). Convergence, tested in the light, was Theflocculus (B, arrow), weak for both eyes. the cerebellar peduncles Vertical eye movements These movements and the brainstem (A, B) because EOG is unreli- did not appear to be were not quantified damaged. able in this plane. Nevertheless, abnormalities of upward and downward eye movement were similar. Saccades appeared to be normal, foveal smooth pursuit was largely saccadic, OKN was absent (without any slow movement), oculocephalic movements (pas- sive rotations of the head) were present, with a full amplitude.

Discussion This case included vestibular symptoms, a leftward tonic deviation of the eyes and abnor- malities of pursuit eye movements, which will be discussed successively. For several days, there was marked vertigo and leftward axial lateropulsion. Isolated and true vestibular symptoms may be observed in pure cerebellar infarcts, resulting from occlusions of the pos- terior and inferior cerebellar artery,4 or only its medial branch5 or of the anterior and inferior cerebellar artery.6 The vestibular symptoms could be due to lesions ofthe flocculus4 or ofthe nodulus and uvula.5 As the flocculus was apparently spared here, the vestibular symp- toms probably resulted from damage to the

nodulus and uvula. This vermal part of the http://jnnp.bmj.com/ vestibulo-cerebellum is reciprocally connected with the vestibular nuclei.7 Thus the impair- Figure 2 Lateral eye ment of this supravestibular control system movements (left eye). A) 0~~~~~~~~~~~~~~~~~ visually guided saccades: could explain the initial vestibular symptoms in a -M a, stimulation; b, eye tI L our patient. movement, normal. B) A leftward tonic conjugate eye deviation also Foveal pursuit: a, R stimulation (0 26 Hz); b, b existed initially, showing progressive im- on October 1, 2021 by guest. Protected copyright. eye movement, saccadic in provement within 10 days and leaving only a both directions. C) OKN (rightward stimulation i)-4250mss300 leftward deviation during eyelid closure on the and, after the vertical eleventh day (when eye movements were recor- arrow, leftward ded). Conjugate tonic deviation of the eyes has stimulation): impaired in X previously been reported in haemorrhagic or both directions. D) VOR: a a, stimulation; b, eye ischaemic8 lesions of the cerebellum. However, movement, apparently R those cases included brainstem compression. normal. In our patient, MRI showed that the brainstem b L was apparently spared. Moreover, the absence of drowsiness and the normal appearance ofthe II 1 f .4111 ventricles (without hydrocephalus) suggested that the brainstem was not compressed by the vermal infarct. Therefore it may be assumed that the tonic ocular deviation was due to the cerebellar lesion. However, it should be noted that in experimental unilateral lesions of the \ M a L/ cerebellum9 and in a unilateral infarct of the rostral cerebellum"0 tonic ocular deviation was b contralateral to the lesion, whereas it was lesion L ipsilateral here. As in our patient, the Vermal infarct with pursuit eye movement disorders 521

Table Horizontal smooth pursuit gains monkey (in particular when lobules V, VI and VII are damaged)' 1 as well as in humans.'6 It is J Neurol Neurosurg Psychiatry: first published as 10.1136/jnnp.53.6.519 on 1 June 1990. Downloaded from Rightgain Left gain Normalgain* possible that this part of the vermis is in fact Foveal 0 11 Hz (peak velocity: 0-47 0-44 0-72 (0-07) less crucial for saccade accuracy, or that smooth pursuit 15'/s) adaptative mechanisms were already operative 0 26 Hz (peak velocity: 0-33 0-36 0-67 (0-09) 41'/s) in our patient when eye movements were OKN (30°/s) 0 17 0 19 0-62 (014) recorded. that the posterior = = 76 range = 70-84 years]. Thus this case suggests *[mean (SD); n 10, mean age years, vermis is, like the flocculus, involved in pursuit eye movements. The activities of the flocculus and posterior vermis cells are not exactly involved all the postero-inferior portion ot the identical during slow eye movements.' In par- vermis along with the inferior part of the left ticular, the discharge of vermal cells is propor- cerebellar hemisphere, but it is difficult to tional to target velocity while that of floccular suggest a detailed explanation that would cells depend on eye and/or head velocity. The account for this deviation. projections of the flocculus and the vermis are Foveal smooth pursuit and OKN were also noticeably different.'7 18 The former severely imparied in all directions. Our patient projects on to the medial vestibular nucleus was 80 years old and there is usually a slight whereas the latter projects (via the fastigial impairment of pursuit eye movement in the nuclei) on to neurons located near the abducens elderly." However, as the pursuit deficits seen nucleus and probably involved in smooth pur- here were much more severe than those of an suit.' These differences in the activity, as well age-matched control group, it may be con- as in the efferent pathways, ofthe flocculus and sidered that old age was not the only cause of vermis are not yet well understood. Further these deficits. Drowsiness, inattention and cer- studies are needed to determine the specific tain medications may also impair pursuit eye roles of these two structures in the control of movements, but none of these was present. pursuit eye movements. Lastly, as already emphasised, there was no clinical or radiological evidence of damage to, We thank Miss S Rivaud for technical assis- or compression of, the brainstem which could tance. account for this impairment of pursuit eye movements. Therefore, it may be assumed that 1 Keller EL. Cerebellar involvement in smooth pursuit eye the cerebellar infarct itself was the primary movement generation. In: Clifford Rose F, Kennard C, cause of the eye movement disorders. eds. Physiological aspects of clinical neuro-ophthalmology. London: Chapman and Hall, 1988:341-55. It has been shown that the cerebellum is an 2 Suzuki DA, Keller EL. The role of the posterior vermis of essential relay in smooth pursuit eye movement monkey cerebellum in smooth-pursuit eye movement control. J Neurophysiol 1988;59:1-39. circuitry. These movements no longer existed 3 Amarenco P, Hauw JJ. Anatomie des arteres cerebelleuses. after total cerebellectomy in the monkey.9 In Rev Neurol 1989;145:267-76. 4 Duncan GW, Parker SW, Fisher CM. Acute cerebellar the cerebellum, the flocculus is important since infarction in the PICA territory. Arch Neurol 1975; the smooth pursuit eye movement gain is 32:364-8. 5 Amarenco P, Hauw JJ, Henin D, et al. Les infarctus du nearly 600' after flocculectomy.'2 The dif- territoire de l'artere cerebelleuse posterieure et inferieure. ference between a simple flocculectomy and a Etude clinico-pathologique de 28 cas. Rev Neurol 1989;145:277-86. http://jnnp.bmj.com/ total cerebellectomy suggests that other parts 6 Rubenstein RL, Norman D, Schindler R, Kassef L. of the cerebellum are involved in smooth Cerebellar infarction: a presentation of vertigo. Laryngo- scope 1980;90:505-14. pursuit eye movements. In the monkey, the 7 Carleton SC, Carpenter MB. Afferent and efferent connec- posterior part of the vermis (lobules VI and tions of the medial, inferior and lateral vestibular nuclei in the cat and monkey. Brain Res 1983;278:29-51. VII) contains cells involved in these move- 8 Lehrich JR, Winckler GF, Ojemann RG. Cerebellar infarc- ments2 and lesions at this level decrease the tion with brain stem compression. Arch Neurol 1970;22:490-8. smooth pursuit gain to about 60%.' In humans, 9 Westheimer G, Blair SM. Functional organization of

diffuse degenerative lesions of the cerebellum primate oculomotor system revealed by cerebellectomy. on October 1, 2021 by guest. Protected copyright. Exp Brain Res 1974;21:463-72. also result in decreased smooth pursuit gain.'3 10 Ranalli PJ, Sharpe JA. Contrapulsion of saccades and Focal lesions with eye movement recordings ipsilateral ataxia: a unilateral disorder of the rostral cerebellum. Ann Neurol 1986;20:31 1-6. are rare and our case could be the first to 11 Buttner U. Smooth pursuit eye movements, optokinetic suggest that pursuit eye movement disorders in nystagmus and vestibulo-ocular reflex suppression. In: Clifford Rose F, Kennard C, eds. Physiological aspects of humans may result from damage to the pos- clinical neuro-ophthalmology. London: Chapman and Hall, terior vermis. Indeed, this region was im- 1988:278-92. 12 Zee DS, Yamazaki A, Butler PH, Gucer G. Effects of paired, while the flocculus and the brainstem ablation of flocculus and paraflocculus on eye movements seemed to be unaffected. The nodulus and in primate. J Neurophysiol 1981;46:878-99. 13 Baloh RW, Yee RD. Honrubia V. Late cortical cerebellar uvula were also damaged in our patient, but atrophy. Clinical and oculographic features. Brain these structures do not appear to be involved in 1986;109: 159-80. 14 Waespe W, Cohen B, Raphan T. Dynamic modification of pursuit eye movements.'4 The lesion in the the vestibulo-ocular reflex by the nodulus and uvula. inferior part of the left cerebellar hemisphere Science 1985;228:199-202. 15 Ritchie L. Effects of cerebellar lesions on saccadic eye might have played a role in the smooth pursuit movements. J Neurophysiol 1976;39:1246-56. disorders in our patient. So far, it has not been 16 Selhorst JB, Stark L, Ochs AL, Hoyt WF. Disorders in cerebellar ocular motor control. I. Saccadic overshoot suggested that such a region could be involved dysmetria: an oculographic, control system and clinico- in these movements either experimentally or anatomical analysis. Brain 1976;99:497-508. 17 Langer T, Fuchs AF, Chubb MC, et al. Floccular efferents clinically. in the rhesus macaque as revealed by autoradiography and Lastly, saccade accuracy was preserved in horseradish peroxidase. J Comp Neurol 1985;235:26-37. 18 Yamada J, Noda H. Afferent and efferent connections of the our patient. Lesions of the posterior vermis are oculomotor cerebellar vermis in the macaque monkey. J known to result in saccade dysmetria, in the Comp Neurol 1987;265:224-41