OCCULAR BOBBING: CLINICAL SIGNIFICANCE M. Braems and I. Dehaene*
The authors report four cases of ocular bobbing: two cases of primary pontine haemorrhage and two cases of basilar thrombosis, one of which is presented as a 'locked in' syndrome. The clinical significance of ocular bobbing is discussed. Ocular bobbing is a rather uncommon disorder of the movements of the eyes, characterized by abrupt downward jerks of the eyes followed by a slow return to their midposition. This disorder was first reported by Fisher (1964). It subsequently became obvious that several related forms occur (SUSAC, HOYT, DAROFF and LAWRENCE, 1970). With regard to the prognostic significance a distinction can be made between typical and atypical bobbing. Typical bobbing has the following characteristics: I. the eye-balls suddenly move downwards and slowly return to their midposition. 2. the eye movements are conjugated and the excursions are between one-fourth and one-third of the normal range of vertical gaze. 3. the downward phase of the eye movement is more rapid than the upward phase, but the eyes may occasionally stay turned downwards for l0 seconds before drifting upwards again. 4. caloric stimulation, even with ice-water, usually has no influence on the movements. 5. there is a total paralysis of spontaneous and reflex horizontal eye movements. 6. in most cases there is a state of deep coma, although this is not obligatory. Additional paralysis of the oculomotor nerve can modify the typical bobbing to a monocular or paretic bobbing. All other variants belong to the atypical bobbing, including those cases in which horizontal movements are not completely absent, those in which bobbing occurs only after caloric stimulation or those in which bobbing occurs only in association with a hippus. * Departments of Neurology and Psychiatry, Radiology and Neurosurgery, St. Jansziekenhuis, Brugge, Belgium. Clin. Neurol. Neurosurg. 1975-2
Case 1. An 81-year-old man who had been hypertensive for a length of time and was in a deep coma on admission, There were spontaneous movements of both legs. Also after painful stimulation flexion of the legs could be obtained. Tendon and periosteal reflexes on the left side were brisk; plantar reflexes were indifferent. The pupils were miotic, not pinpoint and reactive to light. The horizontal oculo-cephalic reflexes were absent, and after ice-water irrigation to the ears, one after another, no ocular deviation was seen. There was a frequent ocular bobbing with tendency to downward excursion of the gaze. Bloodpressure was 180/100 mm Hg. The clinical course was unfavourable and the patient died ten days after admission to the hospital. Lumbar puncture showed bloody cerebrospinal fluid. Pathological examination (Dr. Michielsen - Dr. Van Vuchelen): The heart showed left and right ventricular hypertrophy, coronary sclerosis and an old posterior wall
101 infarction. A recent gastric bleeding was found. The brain did not show abnormalities on the outside. In the pontine area a recent bleeding was found with a maximum diameter of 3 cm. The bleeding had ruptured in the IVth ventricle (fig. 1). Conclusion: typical ocular bobbing in a patient in a comatose state, caused by a pontine haemorrhage.
Case 2. A 73-year-old man collapsed shortly before his admission to the hospital. On admission the consciousness was normal. There was no weakness of the limbs; tendon reflexes were normal. There was a right-sided facial paralysis with a positive Bell's sign. Facial sensation was normal. The pupils were equal and reacting to light. Three hours after admission deterioration was found. The pupils were pinpoint and did not respond to light. The eyes were in midposition. The patient could look downward on command. Horizontal oculocephalic reactions were absent. Occasional rapid downward excursions of the eyes were noticed. There was a bilateral facial paralysis, the movements of the tongue were very limited and a left hemiplegia was present. There was no nuchal rigidity. The patient was hyperventilating. One hour later the patient was in deep coma. Oculo-cephalic reactions were absent and occasional ocular bobbing was observed, returning to midposition of the eyes. The patient died on the following day, nine hours after admission to the hospital. Lumbar puncture showed bloody cerebrospinal fluid. Pathological examination (Dr. Michielsen, Dr. Van Vuchelen). Symmetrical brain. The trigonal bloodvessels were not sclerotic and the basilar artery was patent over the whole length of its course. There was a restricted pontine haemorrhage on the right side, which had ruptured in the IVth ventricle (fig. 2). Conclusion: An initially conscious patient with signs of pontine dysfunction. In this period ocular bobbing was already present. The decision whether this was a typical bobbing could not be made because caloric tests were not done. Autopsy revealed a pontine haemorrhage. Case 3: A 61-year-old man was admitted to the hospital a few hours after onset of unconsciousness. He had been incontinent for urine. He had been feeling dizzy over the past few weeks. On admission he was in deep coma, without response to painful stimuli. Bloodpressure was 150/70 mm Hg. Pulse was regular 60 beats/min. There was no nuchal rigidity. The pupils were equal and reacting to light. The cilio-spinal reflex was positive on both sides. The left corneal reflex was weaker than the right one. The eyes were skewed, with the left eye lower than the right eye. No spontaneous horizontal eye movements were observed but there were occasional vertical eye movements, with a rapid downward phase an a slow return upward. These bobbing movements were slightly asynchronous and occurred more regular on the right side. Horizontal and vertical oculo-cephalic reactions were absent. Ice-water irrigation to the right ear elicited slow ocular deviation to the right without influence on
102 the ocular bobbing. There were no spontaneous limb movements. The reflexes were brisk and symmetric. Lumbar puncture revealed clear and normal spinal fluid. During the first two days after admission a deep coma was still present, On the third day breathing became more irregular. Pulmonary infections did occur. The pupils remained equal, miotic but responsive to light. Ocular bobbing was still present, more pronounced on the right eye than on the left one. Oculo-cephalic reactions were missing. Ice-water irrigation to the right ear evoked outward deviation of the right eye without deviation of the left eye (internuclear ophthalmoplegia). Ice-water irrigation to the left ear gave no response. The patient died the following day.
Pathological examhlation (Dr. Michielsen, Dr. Van Vuchelen): Coronary sclerosis with a fibrous scar of a myocardial infarction and right ventricular hypertrophy. There was an obvious atheromatosis of the internal carotid arteries, the vertebral arteries and the basilar artery. In the basilar artery a recently organized thrombus was found extending from its origin over a length of 1 cm. In the pons there was a large irregular infarction with ischaemic necrosis and interstitial oedema. Conclusion : atypical ocular bobbing in a comatose patient with signs of a pontine dysfunction and internuclear ophthalmoplegia due to basilar thrombosis and pontine infarction.
103 Case 4. A 69-year-old man was feeling dizzy on the day of admission. He was admitted because of an acute hemiplegia on the right side, which was gradually regressing. Three hours later consciousness deteriorated gradually towards coma, with relapse on the right hemiplegia. Spontaneous decerebrate rigidity occurred. Both corneal reflexes were positive; oculo-cephalic reactions were retained and the pupils were miotic but reactive to light. The cerebrospinal fluid was normal. A left carotid angiogram showed no abnormalities. Twelve hours after admission ocular bobbing was noted. Horizontal oculo-cephalic reactions were missing; the vertical reactions were present. Ice-water irrigation to the right ear elicited abduction of the right eye while the left eye remained immobile (internuclear ophthalmoplegia). By irrigation to the left ear a tonic deviation to the left was obtained. After a period of three days spontaneous blinking of the eyes was observed. The patient also appeared to be able to open his eyes on command. There were voluntary upward and downward gaze movements, while active horizontal movements were impossible. Ice-water tests gave the same picture as before. An ocular bobbing was still present. The pupils remained miotic and responsive. All active movements except the vertical eye movements, were impossible. Painful stimulation elicited a decerebrate attitude. The clinical situation remained unchanged during the following fifteen weeks, after which the patient died from a pneumonia. Pathological examination (Dr. J. J. Martin, Born-Bunge Foundation, BerchemAntwerpen): There was a diffuse atheromatosis of the circle of Willis with a thrombosis of the middle and higher portions of the basilar artery. An infarction of the ventro-rostral part of the pons was found, extending into the caudal paramedian tegmentum and rostrally into both cerebral peduncles. Conclusion: 'Locked-in' syndrome, as result of a ventral pontine infarction. Atypical ocular bobbing during the first comatose phase, continuing in a later period with clear consciousness.
The occurrence of typical bobbing with great certainty indicates the presence of an intra-pontine lesion. However, in the nineteen cases collected by SUSAC et al. (1970) three exceptions were found. Two of these were reported by HAMEROFF, GARCIAMULLIN and EECKHOLDT (1969). In the first case brain-stem ischemia was presumed but no signs of acute neuronal changes were actually found. In the second case autopsy revealed a cerebellar haemorrhage with compression of the pons and midbrain. Microscopic examination failed to show ischemia or haemorrhagic lesions in the brain stem. In one case ofSUSAC et al. (1970) a cerebellar haematoma was found. The fact that exceptions do occur means that bobbing should not be regarded as a pathognomonic sign of primary pontine lesion. The problem raised by this is particularly relevant in the differential diagnosis between primary pontine haemorrhage and cerebeilar haemorrhoage in which the clinical symptoms may be very similar (PLUM and POSNER, 1966). Typical ocular bobbing is infrequent as a symptom of
104 cerebellar haemorrhage. orrhage.
I n the series o f FISHER ( 1 9 6 4 ) o f 2 5 cases o f c e r e b e l l a r h a e m -
In the series o f FISHER (1964) o f 25 cases o f c e r e b e l l a r h a e m o r r h a g e
o n e case is m e n t i o n e d w i t h b o b b i n g .
In this case an a t y p i c a l b o b b i n g was seen.
T h e p r e s e n c e o f t y p i c a l b o b b i n g in a c o m a t o s e p a t i e n t , t o g e t h e r w i t h o t h e r signs o f b r a i n s t e m d y s f u n c t i o n , i n d i c a t e s w i t h g r e a t c e r t a i n t y the e x i s t e n c e o f p o n t i n e haemorrhage or infarction.
O u r c a s e c o n f i r m s this thesis.
O u t o f e i g h t e e n cases w i t h typical b o b b i n g verified by a u t o p s y n i n e w e r e p o n t i n e h a e m o r r h a g e s , f o u r were p o n t i n e i n f a r c t i o n s , o n e was a c e r e b e l l a r h a e m o r r h a g e , o n e was a h a e m o r r h a g i c c e r e b e l l a r i n f a r c t i o n , o n e was a p o n t i n e g l i o m a a n d o n e was a trauma.
(HAMEROFF et al., 1969) t h e r e was an o c c l u s i o n o f a v e r t e b r a l
Fisher Plum et al. Hameroff et al. Nelson et al.
1964 1966 1969 1970
Susac et al.
Henry et al. present case
Nordgren et al.
Cambier et al.
Case I Case 2
typical dubious typical typical typical typical typical typical typical paretic dubious typical dubious
coma conscious coma dubious coma coma conscious conscious conscious coma coma coma coma
Case Case Case Case Case Case Case Case
typical typical typical atypical atypical typical atypical atypical
coma coma conscious (locked in) conscious (locked in) conscious (locked in) coma coma conscious (locked in)
Case Case Case Case Case Case Case Case Case Case
1 2 2 I 2 3 4 2 4 6
1 2 2 5 I 2 3 4
Pontine tumour (1)
Daroff et al.
Cerebell. Haemorrh. (2)
Fisher Hameroff et al.
Case 4 Case 4
Cerebell. Infarction (1)
Susac et al.
Basilar thrombosis Trauma Metabolic disturb.
Homeroff et al.
Susac et al.
Case 3 Case I Case 9
typical typical atypical
coma coma coma
Survival: Pontine infarction
Susac et al.
Case 3 Case 7
Haemorrhage Cardial arrest Trauma Bromism Hydrocephalus
Boddie Hameroff et al. Newman et al. Paty et al. Susac et al.
1972 1969 1971 1972 1970
typical paretic typical dubious atypical atypical atypical
105 artery without recent brainstem infarction. In three additional cases with pontine haemorrhage in which ice-water caloric stimulation is not mentioned, the type of bobbing can not be decided (Table I). In the cases of atypical bobbing there is no complete paralysis of the horizontal eye movements. Its clinical value as a sign of pontine dysfunction remains very great, though less than in the case of typical bobbing. The phenomenon is also observed in more diffuse cerebral pathology and does not necessarily point to irreversible lesions. It appears (Table I) that atypical bobbing is reported in cases ofpontine infarction, three of which show a 'locked-in' syndrome (NORDGREN, MARKESBERY,FUKUDA and REEVES, 1971; CAMBIER, HENIN, ESCOUROLLE, MASSON, DEHEN and LAGARDE, 1974; present case 4). Atypical bobbing does not seem to occur in cases of pontine haemorrhage. PATY and SHERR (1972) report a case of bromism, SUSAC et al. (1970) a case of hypoglymic coma and NEWMAN,GAY and HEXLBRUIN(1971) report a patient showing atypical bobbing after a bulletwound. Bobbing may occur in conscious patients; this applies to cases of pontine haemorrhage (NELSON and JOHNSON, 1970; SUSAC et al., 1970, present case 2) as well as to cases of pontine infarction; bobbing is described in cases of 'locked-in' syndrome (NORDGREN et al., 1971 ; CAMBXERet al., 1974, present case 4). This term was introduced by PLUM and POSNER (1966) to describe a clinical picture characterized by a quadriplegia and a paralysis of the lower cranial nerves; communication with the outside world can be established through preserved vertical eye movements and blinking only. It is mostly caused by ventral pontine infarction. Bobbing is to be distinguished from other spontaneous vertical eye movements, such as 'down beat' nystagmus (CO6AN, 1968). In this movement there is also a rapid downward component. It can be distinguished from bobbing by the higher regularity and frequency, as well as by the clinical picture in which this symptom occurs. Down beat nystagmus is mainly found in congenital anomalies of the foramen magnum, with or without Arnold-Chiari malformation. Ocular myoclonus is the ocular movement occurring together with palatal myoclonus; they may also be accompanied by myoclonus of the pharynx, larynx, diaphragm and limbs. The eye movements are pendular, rhythmic and synchronous with the palatal myoclonus. These ocular myoclonus can occur in the horizontal and in the vertical direction. The term ocular bobbing was used to designate myoclonus by YAP, MAYOand BARRON (1968), which leads to confusion. Opsoclonus is a constant chaotic eye movement without any rhythmicity occurring both in the horizontal and vertical planes. There are alternating spells of violent movement and of comparative rest. The movements go on during sleep and after closing of the eyes. In most cases opsoclonus is accompanied by cerebellar signs and non-synchronous myoclonic movements of face, neck, and upper limbs. In those cases pleocytosis is usually found in the cerebrospinal fluid (MCLEAN, 1970). Opsoclonus associated with malignancy has been reported recently. In these cases there was subacute parenchymatous degeneration of the cerebellum (ELLENBERGER and
106 NETSKY, 1970). BODDIE (1972) reports a case with b o b b i n g in the initial phase followed, after its disappearance, by irregular, n o n rhythmical, conjugate ocular m o v e m e n t s , mainly in the vertical plane, which he designated as opsoclonus. The physio-pathology of ocular b o b b i n g has n o t yet been made clear. FISHER(1964) regards this p h e n o m e n o n as n o r m a l roving m o v e m e n t s in the vertical plane, in the presence of a h o r i z o n t a l gaze paralysis. DAROFE and WALDMAN (1965) suppose b o b b i n g to be the result of an intact d o w n w a d gaze m e c h a n i s m , which may be triggered by stimuli of e.g. vestibular origin. This theory is supported by NEWMAN et al. (1971). A c c o r d i n g to HAMEROEF et al. (1969) there is a loss of cortical a n d subcortical i n h i b i t i o n of vertical gaze m o v e m e n t as a result of paralysis of the p o n t i n e gaze centre. NELSON and JOHNSON (1971) underline the fact that in the case of p o n t i n e lesion the cortico-nuclear c o n n e c t i o n s for vertical gaze m o v e m e n t have been spared, while the cortico-nuclear fibres for horizontal gaze m o v e m e n t s , which descend further d o w n w a r d s to the pons, are damaged. However, this does not yet explain the typical b o b b i n g pattern. CAMB1ER et al. (1974) suppose that a lesion of the p o n t i n e p a r a m e d i a n reticular f o r m a t i o n may be able to i n t e r r u p t all horizontal eye m o v e m e n t s , while in the vertical plane only the saccadic d o w n w a r d m o v e m e n t s are retained. A c c o r d i n g to this hypothesis b o b b i n g would be the sole saccadic eye m o v e m e n t which r e m a i n s possible.
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