Documenta Ophthalmologica 43,1 : 101-107, 1977 CEREBELLAR ROLE IN SMOOTH PURSUIT MOVEMENT* P. NEMET & S. RON
( Tel-A viv /R aanana, Israel) ABSTRACT It is generally believed that pursuit eye movements are unaffected by cerebellar cortical atrophy or cerebellectomy. The present study was performed on patients who underwent partial vermis and hemisphere ablations as a result of severe cranial injury or cerebellar tumors. Eye movements were measured by DC electro-o culography. A clear disparity of the slow phase of the optokinetic nystagmus was observed. When eye movements were contralateral to the ablated side the slow phase of optokinetic nystagmus was statisticaUy slower than drum or visual field velocity. It is suggested that the cerebellum network is involved in the mechanisms of the smooth pursuit movement. INTRODUCTION Disorders in eye movements have long been considered as clinical signs for specific neurological abnormalities. The clinician would like, therefore, to have at his fingertips a quick, simple test, if possible, to detect these abnormalities. The optokinetic nystagmus (OKN) is considered to be one of these tests. This eye movement is composed of slow phases or smooth pursuit movements and quick phases considered to be saccades (Ron, Robinson & Skavenski, 1972). While the ablation of cerebral hemisphere, vestibular nuclei, basal ganglia or superior coUiculi has little effect on OKN, ablation of the occipital lobe or the mesencephalic reticular formation strongly affect the OKN (Jung & Kornhuber, 1964). The smooth pursuit movements of the abnormal OKN are slower (i.e., their velocities do not match those of the moving stimuli). Clinically, cerebeUar ablation is not considered to cause smooth pursuit dysmetria (Daroff & Hoyt, 1971). In animals, cerebeUar lesions or cerebellectomy led to contradictory results (CoUewign, 1970; Kornlmber, 1968; Westheimer & Blair, 1973). No quantitative data of smooth pursuit eye movement in cerebeUar ablated humans have been reported, therefore, in this study such movements in patients were measured and analysed. It was found that, while voluntary nystagmus might exist, there is a substantial reduction of the smooth pursuit movements.
* The study was supported by a special grant from S.R. & P.N. Foundation.
101
METHODS Horizontal eye movements were measured by binocularly recording electrooculograms. Electrodes (Ag-AgC1) were placed at the outer canthi of the two eyes and the resulting signal led through a DC amplifier to a tape recorder. The data were played back later, photographed and analysed. In a dark room the subject was seated, his head held still in a firm chin rest facing a flat surface. To calibrate the electro-oculogram, a series of small lights, each subtending less than 0.1 degree were arranged 10, 20 and 30 degrees left and right of a center fixation point. To generate OKN, a drum with black and white stripes was placed in front of the subject and rotated uniformly at fixed velocities of 5, 10, 20, 30 and 40 deg/sec. When the eye-hand coordination was studied the subject was asked to 'look' at his fingers moving right and left in a swing of about + 30 degrees from the center. The experiment was first done in a lighted room and subsequently repeated in a dark room. The moving hand was holding a handle which moved in a smooth track and was connected with a thread to a potentiometer. From the potentiometer a voltage was received which represented the handle position (located just under the calibrating lights) with respect to the lights' center. A total of 9 patients who underwent partial cerebeUar ablation were studied. The group consisted of five patients who underwent partial hemisphere ablation on one side, three patients with partial hemisphere and vermis ablation and one who had his posterior vermis removed. Two healthy subjects were also studied from comparison. A total of 18 sessions for all patients were run. RESULTS AND DISCUSSION The major finding was that no patient was found to track normally, i.e. to have a smooth phase velocity matching the drum velocity, the discrepancy being larger for higher velocities. The top two records in Fig. I (A and B) were taken from a normal subject at drum velocity of 5 and 20 deg/sec. In most patients, tracking at slow velocities of 5 deg/sec smooth pursuit and drum velocities were about the same (Fig. 1, C). Quick phases appeared at larger intervals than in normal subjects (1-2 sec as compared to 0.5-1 sec) interrupting the smooth phase and thus returning the eyes to approximately their initial eye position. At higher velocities in all patients, eye movement velocity did not match drum velocity (Fig. 1, D). Six patients had equal impairment when the smooth pursuit was toward the ablated side or contralateral, whereas three patients performed better 102
RIGHT
DRUM
VELOCITY 5
deg/sec
A
20 deg/sec
B
5
deg/sec
C
20 deg/sec O
0o degrees
5OO msec Fig. 1. Optokinetic nystagmus evoked from a healthy subject (A and B) and from a patient (C and D) with partial right hemisphere ablation. The optokinetic nystagmus was induced by steady drum rotation at velocities indicated in the figure.
when the smooth pursuit was toward the ablated side. No correlation, however, was found between the neuroanatomical structure ablated (e.g. whether hemisphere alone or with vermis) and the extent or side of the impairment. Part of this difficulty emanates from the surgical procedure which makes it hard to deliniate the exact lesion made. One might suggest that a lesion of the vermis had a lesser effect on OKN than that of the hemisphere. The data of smooth phase velocities of OKN obtained from one
103
patient with lateral hemisphere ablation are summarized in Fig. 2. A total of 120 velocities were measured for a healthy subject (Fig. 2, Normal) and one patient (Fig. 2, Patient). The regression hnes represent the mean smooth movement velocity response to drum velocity. These results suggest that the neural mechanism which subserves pursuit of a moving target was affected. Whether this can be attributed to the damaged cell groups of the cerebellar cortex or to the nuclei, is a matter of speculation. In the monkey, total cerebellectomy was shown to result in the inability to perform smooth pursuit movements (Westheimer & Blair, 1973) while cerebellar cortical lesions, not including the deep nuclei, did not affect the pursuit movements of the OKN (Aschoff & Cohen, 1971). This question, however, cannot be answered from this study.
u
( Tel-A viv /R aanana, Israel) ABSTRACT It is generally believed that pursuit eye movements are unaffected by cerebellar cortical atrophy or cerebellectomy. The present study was performed on patients who underwent partial vermis and hemisphere ablations as a result of severe cranial injury or cerebellar tumors. Eye movements were measured by DC electro-o culography. A clear disparity of the slow phase of the optokinetic nystagmus was observed. When eye movements were contralateral to the ablated side the slow phase of optokinetic nystagmus was statisticaUy slower than drum or visual field velocity. It is suggested that the cerebellum network is involved in the mechanisms of the smooth pursuit movement. INTRODUCTION Disorders in eye movements have long been considered as clinical signs for specific neurological abnormalities. The clinician would like, therefore, to have at his fingertips a quick, simple test, if possible, to detect these abnormalities. The optokinetic nystagmus (OKN) is considered to be one of these tests. This eye movement is composed of slow phases or smooth pursuit movements and quick phases considered to be saccades (Ron, Robinson & Skavenski, 1972). While the ablation of cerebral hemisphere, vestibular nuclei, basal ganglia or superior coUiculi has little effect on OKN, ablation of the occipital lobe or the mesencephalic reticular formation strongly affect the OKN (Jung & Kornhuber, 1964). The smooth pursuit movements of the abnormal OKN are slower (i.e., their velocities do not match those of the moving stimuli). Clinically, cerebeUar ablation is not considered to cause smooth pursuit dysmetria (Daroff & Hoyt, 1971). In animals, cerebeUar lesions or cerebellectomy led to contradictory results (CoUewign, 1970; Kornlmber, 1968; Westheimer & Blair, 1973). No quantitative data of smooth pursuit eye movement in cerebeUar ablated humans have been reported, therefore, in this study such movements in patients were measured and analysed. It was found that, while voluntary nystagmus might exist, there is a substantial reduction of the smooth pursuit movements.
* The study was supported by a special grant from S.R. & P.N. Foundation.
101
METHODS Horizontal eye movements were measured by binocularly recording electrooculograms. Electrodes (Ag-AgC1) were placed at the outer canthi of the two eyes and the resulting signal led through a DC amplifier to a tape recorder. The data were played back later, photographed and analysed. In a dark room the subject was seated, his head held still in a firm chin rest facing a flat surface. To calibrate the electro-oculogram, a series of small lights, each subtending less than 0.1 degree were arranged 10, 20 and 30 degrees left and right of a center fixation point. To generate OKN, a drum with black and white stripes was placed in front of the subject and rotated uniformly at fixed velocities of 5, 10, 20, 30 and 40 deg/sec. When the eye-hand coordination was studied the subject was asked to 'look' at his fingers moving right and left in a swing of about + 30 degrees from the center. The experiment was first done in a lighted room and subsequently repeated in a dark room. The moving hand was holding a handle which moved in a smooth track and was connected with a thread to a potentiometer. From the potentiometer a voltage was received which represented the handle position (located just under the calibrating lights) with respect to the lights' center. A total of 9 patients who underwent partial cerebeUar ablation were studied. The group consisted of five patients who underwent partial hemisphere ablation on one side, three patients with partial hemisphere and vermis ablation and one who had his posterior vermis removed. Two healthy subjects were also studied from comparison. A total of 18 sessions for all patients were run. RESULTS AND DISCUSSION The major finding was that no patient was found to track normally, i.e. to have a smooth phase velocity matching the drum velocity, the discrepancy being larger for higher velocities. The top two records in Fig. I (A and B) were taken from a normal subject at drum velocity of 5 and 20 deg/sec. In most patients, tracking at slow velocities of 5 deg/sec smooth pursuit and drum velocities were about the same (Fig. 1, C). Quick phases appeared at larger intervals than in normal subjects (1-2 sec as compared to 0.5-1 sec) interrupting the smooth phase and thus returning the eyes to approximately their initial eye position. At higher velocities in all patients, eye movement velocity did not match drum velocity (Fig. 1, D). Six patients had equal impairment when the smooth pursuit was toward the ablated side or contralateral, whereas three patients performed better 102
RIGHT
DRUM
VELOCITY 5
deg/sec
A
20 deg/sec
B
5
deg/sec
C
20 deg/sec O
0o degrees
5OO msec Fig. 1. Optokinetic nystagmus evoked from a healthy subject (A and B) and from a patient (C and D) with partial right hemisphere ablation. The optokinetic nystagmus was induced by steady drum rotation at velocities indicated in the figure.
when the smooth pursuit was toward the ablated side. No correlation, however, was found between the neuroanatomical structure ablated (e.g. whether hemisphere alone or with vermis) and the extent or side of the impairment. Part of this difficulty emanates from the surgical procedure which makes it hard to deliniate the exact lesion made. One might suggest that a lesion of the vermis had a lesser effect on OKN than that of the hemisphere. The data of smooth phase velocities of OKN obtained from one
103
patient with lateral hemisphere ablation are summarized in Fig. 2. A total of 120 velocities were measured for a healthy subject (Fig. 2, Normal) and one patient (Fig. 2, Patient). The regression hnes represent the mean smooth movement velocity response to drum velocity. These results suggest that the neural mechanism which subserves pursuit of a moving target was affected. Whether this can be attributed to the damaged cell groups of the cerebellar cortex or to the nuclei, is a matter of speculation. In the monkey, total cerebellectomy was shown to result in the inability to perform smooth pursuit movements (Westheimer & Blair, 1973) while cerebellar cortical lesions, not including the deep nuclei, did not affect the pursuit movements of the OKN (Aschoff & Cohen, 1971). This question, however, cannot be answered from this study.
u
