Cerebral Contribution to the Visual Suppression of Vestibular Nystagmus Setsuko Takemori, MD; Michihiko Ono, MD; Takahiro Maeda, MD
with cerebral leexamined to locate cerebral areas involved in visual suppression. Visual suppression was reduced or abolished when the lesions were in the parietal lobe, especially in the dorsoposterior region. This part of the parietal lobe seems to modify visual suppression of caloric nystagmus that is mediated by the flocculus and nodulus of the cerebellum as well as the pons. In patients with frontal lobe lesions including the parietal lobe, visual suppression was reduced or abolished. Thus, the parietal lobe is important for this visual suppression mechanism. \s=b\
Thirty-two patients
sions
were
(Arch Otolaryngol 105:579-581, 1979)
is well known that vestibular is inhibited by visual fixation. Visual fixation is demon¬ strated by measuring visual suppres¬ sion of vestibular nystagmus.' -' In humans' and rhesus monkeys,- the normal amount of visual suppression is about 50%. It has been established that visual suppression depends on the integra¬ tion of the flocculus in the cerebel¬ lum.' The nodulus has also been impli¬ cated in the mediation of this reflex.' Maekawa et al'"' reported that ipsilateral illumination or electric stimula¬ tion of the optic disc and chiasm evoked prominent activation of Purkinje cells in the flocculus via climbing fiber afférents and also via mossy fiber afférents. This pathway has been traced through the dorsal portion of the posterior accessory optic tract, the so-called central tegmental optic tract and the rostral portion of the
It nystagmus
Accepted
for publication Sept 21, 1978. From the Departments of Neurotology (Dr Takemori) and Neurosurgery (Drs Ono and Maeda), Toranomon Hospital, Toranomon, To-
inferior olive to the flocculus. The from the pontine nuclei to the flocculus or nodulus were also demonstrated by using horseradish
projection
peroxidase.7
Some cases of cerebral disorders have failure of visual fixation; howev¬ er, sources of cerebral control have not been well identified. This study clari¬ fies the cerebral contribution to visual fixation demonstrated by visual sup¬ pression of vestibular nystagmus.
nystagmus (Fig 1). The mean maximum slow-phase velocity of caloric nystagmus in darkness during 10 s (a) and the mean slow phase velocity in light during 5 to 10 s (b) were
sion
measured. Percent of visual suppres¬ was represented by the following
expression: visual suppression (%) (a b)/a x 100 Visual suppression was 54% ± 12% in 52 =
-
normal adults. Visual suppression of 10% to 40% was defined as "reduced," and visual suppression under 10% was defined as "abolished."
METHODS Caloric nystagmus was evoked by irriga¬ tion of the external auditory canal with 20 mL of ice water for 20 s. Caloric nystagmus was recorded by electronystagmography (ENG) in darkness when the patients' eyes were covered. When caloric nystagmus reached the maximum and constant slow phase velocity, the lights were turned on for 5 to 10 s and the patients fixed their eyes on the cross mark on the ceiling or on the examiner's index finger, which was 50 cm above the patients' eyes. The lights were turned off and their eyes were re¬ covered until the cessation of caloric nystagmus. Visual suppression was repre¬ sented by measuring the visual inhibition on the slow-phase velocity of caloric
RESULTS
Thirty-two patients with cerebral by angiography or by computerized tomography were
lesions confirmed
tested. Of 17 frontal lobe lesions, 14 were frontal lobe tumors. In seven cases, visual suppression was normal, and in seven suppression was reduced or abolished. Three frontal lobe lesions were
frontoparietal tumors. In two suppression was normal,
cases, visual
and in one case it was reduced. Five patients had temporal lobe lesions: two temporal lobe tumors and three temporoparietal lobe tumors. In the case of the two temporal lobe
Fig 1.—Normal visual suppression. Caloric nystagmus toward left in darkness and light while eyes were fixed on examiner's index finger (f). Visual suppression was 56% in this case. A, Eye movement, calibration at 10°. B, Eye velocity, calibration at 20°/s. C, Slow-wave velocity, cali¬ bration at 20°/s (A, B, and C are same subjects through 3).
kyo. Reprint requests to Department of Neurotology, Toranomon Hospital, Toranomon 2-2-2, Minato-Ku, Tokyo, Japan (Dr Takemori).
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as
in
Fig
1
2.—Arteriovenous malformation. Left, Caloric nystagmus toward left; visual suppression was reduced. Center, Caloric nystagmus toward right; visual suppression was abolished. Right, Left carotid angiography. Fixation points were cross mark on ceiling (c) and examiner's index finger
Fig
(f).
3.—Left parieto-occipital lobe tumor. Left, Caloric nystagmus toward left; visual suppression was reduced. Center, Caloric nystagmus toward right; visual suppression was abolished. Caloric nystagmus even showed augmentation in light. Right, Computerized tomographic scan; arrow indicates tumor. Fixation points were cross mark on ceiling (c) and examiner's index finger (f).
Fig
Fig 4.—Right frontal lobe tumor with left hemiplegia. Left, Slow-phase velocity of caloric nystagmus toward left; visual suppression was reduced (14%) and it recov¬ ered (53%) after operation. Center, Slow-phase velocity of nystagmus toward right; visual suppression was abolished (—8%) and it became normal after operation. Right, Computerized tomographic scan; arrow indicates tumor.
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tumors, visual suppression was nor¬ mal, as it was in one case of temporoparietal lobe tumor. In two cases of temporoparietal lobe tumor, visual suppression was reduced or abolished. Eight patients had parietal lobe
two parietal lobe tumors, three vascular lesions, and three parieto-occipital lobe tumors. Visual suppression was reduced in the two patients with parietal lobe tu¬ mors, and was reduced or abolished in the six patients with vascular lesions or parieto-occipital lobe tumors. Two patients had occipital lobe lesions (vascular); visual suppression was normal in both.
lesions, including
REPORT OF CASES
40-year-old
Case l.-A
man
formation of the left middle cerebral artery with an intracerebral hematoma. The patient had right homonymous hemianopia. On Aug 10, 1977, surgery was performed. Neurotological examinations were conducted on Oct 20, 1977. Optokinetic nystagmus of the right was strongly impaired; saccadic and ataxic eyetracking patterns were observed. Visual suppression of caloric nystagmus in both directions was abolished or reduced
(Fig 2).
19-year-old girl complained of headache and twinkling sensa¬ tion when she looked to the right. This condition had been present for four years. A left parieto-occipital lobe tumor was found by computerized tomography. On May 20, 1977, surgery was performed. The Case 2.—A
recurring
tumor
was
fibrillary astrocytoma histologically. a
COMMENT
The results of the present study strongly suggest that certain areas of the parietal and parieto-occipital lobes are required for visual suppression of vestibular nystagmus. All of the patients in this study who had lesions in these areas showed either a reduc¬ tion or an absence of the normal visual
suppression
suddenly-
complained of severe headache, nausea, and vomiting on May 10, 1977, and was admitted to the hospital. Left carotid angiography showed an arteriovenous mal¬
determined
the lesion side was abolished (—8%), and visual suppression of caloric nystagmus toward the normal side was reduced (14%). Twenty days after the operation, optoki¬ netic nystagmus and eye-tracking patterns appeared normal. Visual suppression of caloric nystagmus toward both directions became normal (Fig 4).
as
Neurotological examinations were per¬ formed before and after the operation. Optokinetic nystagmus toward the right was strongly impaired, and saccadic eyetracking movements toward the left were present. Visual suppression of caloric nystagmus was reduced or abolished in both directions (Fig 3). Case 3.-A 52-year-old man suddenly lost consciousness with a convulsive attack on March 13, 1978. After this attack, he had gait disturbance and the left hemiplegia. A metastatic right frontal lobe tumor was found by computerized tomography. (On Dec 16, 1977, this patient had surgery for sigmoid carcinoma.) Neurotological examinations were per¬ formed. Optokinetic nystagmus toward the left was strongly impaired, and saccadic eye-tracking patterns were seen. Visual suppression of caloric nystagmus toward
response. These results are consistent with those of other workers who have suggested that the parietal lobes are involved in the integration of visual information for the purpose of spatial orientation and stabilization. Holmes^ reported that disturbance of visual orientation was found in cases of parietal lobe lesions. DennyBrown et al" also reported that visual inattention to the normal side was seen after the parietal lobe destruc¬ tion in rhesus monkeys. Smith, et al'u examined 31 anatomically verified cases and concluded that a positive optokinetic nystagmus sign in cortical lesions was most suggestive of in¬ volvement of the parietal lobe. Other researchers have established parts of the parietal lobes as areas important for the control of eye movements. The neurons that responded to visual fixa¬ tion or to visual tracking were found in area 7."" Balint" reported that psychic paralysis of visual fixation, lack of full voluntary control of eye movements while random movements were normal, and oculomotor apraxia were found in a case of bilateral lesions of the parieto-occipital areas.
Visual suppression was reduced or abolished when the lesions were in the dorsal parts of the parieto-occipital lobes, especially in the parietal lobe,
including area 7.
In contrast to these ings, lesions in other
find¬ of the
positive areas
cerebrum were not strongly asso¬ ciated with disturbances of visual suppresion. Neither temporal lobe nor occipital lobe pathologic features were associated with the abnormal visual
suppression.
In the
patients
with frontal lobe
lesions, visual suppression
was
only
reduced or abolished when the lesions extended to the parietal lobe. Recent¬ ly, there has been a report correlating unit activity in the prefrontal cortex to visual fixation that could be related to visual suppression.11 Therefore, the possibility that frontal areas are involved in visual suppression should be considered. However, the parietal lobes seem to be the main cerebral source of control of visual suppression, and they seem to modify this quick and prompt reflex that is visual suppression me¬ diated by the vestibulocerebellum and pons. Robert F.
manuscript.
Hink, PhD, assisted in editing this
References 1. Takemori S: Visual suppression test. Ann Otol 86:80-85, 1977. 2. Takemori S, Cohen B: Visual suppression of vestibular nystagmus in rhesus monkeys. Brain Res 72:203-212, 1974. 3. Takemori S, Cohen B: Loss of visual suppression of vestibular nystagmus after flocculus lesions. Brain Res 72:213-224, 1974. 4. Takemori S: Visual suppression of vestibular nystagmus after cerebellar lesions. Ann Otol 84:318-326, 1975. 5. Maekawa K, Simpson JI: Climbing fiber responses evoked in vestibulocerebellum of rabbit from visual system. J Neurophysiol 86:649\x=req-\ 666, 1973. 6. Maekawa K, Takeda T: Mossy fiber responses evoked in the cerebellar flocculus of rabbits by stimulation of the optic pathway. Brain Res 98:590-595, 1975. 7. Hoddevik GH: The pontine projection to the flocculonodular lobe and the paraflocculus studied by means of retrograde axonal transport of horseradish peroxidase in the rabbit. Exp Brain Res 30:511-526, 1977. 8. Holmes G: Disturbances of visual orientation. Br J Ophthalmol 2:449-468, 1918. 9. Denny-Brown D, Chambers RA: The parietal lobe and behavior. Res Pub Assoc Nerv Ment Dis 36:35-117, 1958. 10. Smith JL, Cogan DG: Optokinetic nystagmus: A test for parietal lobe lesions. Am J Ophthalmol 48:187-193, 1959. 11. Hyv\l=a"\rinenJ, Poranen A: Function of the parietal associate area 7 as revealed from cellular discharges in alert monkeys. Brain 97:673-692, 1974. 12. Mountcastle VB, Lynch JC, Georgopoulos A, et al: Posterior parietal association cortex of the monkey: Command function for operation within extrapersonal space. J Neurophysiol 38:871-908, 1975. 13. Sakata H, Shibutani H, Kawano K: Information processing in the parietal association areas. Adv Neurol Sci 21:1155-1167, 1977. 14. Balint R: Seelenl\l=a"\hmungdes Schauens, optische Ataxie, r\l=a"\umlicheSt\l=o"\rungder Aufmerksamkeit. Monatsschr Psychiatry Neurol 25:51-81, 1909. 15. Fuster JM: Unit activity in prefrontal cortex
during delayed-response performance:
Neuronal correlations of transient memory. J Neurophysiol 36:61-78, 1973.
Downloaded From: http://archotol.jamanetwork.com/ by a DALHOUSIE UNIVERSITY-DAL-11762 User on 06/20/2015
with cerebral leexamined to locate cerebral areas involved in visual suppression. Visual suppression was reduced or abolished when the lesions were in the parietal lobe, especially in the dorsoposterior region. This part of the parietal lobe seems to modify visual suppression of caloric nystagmus that is mediated by the flocculus and nodulus of the cerebellum as well as the pons. In patients with frontal lobe lesions including the parietal lobe, visual suppression was reduced or abolished. Thus, the parietal lobe is important for this visual suppression mechanism. \s=b\
Thirty-two patients
sions
were
(Arch Otolaryngol 105:579-581, 1979)
is well known that vestibular is inhibited by visual fixation. Visual fixation is demon¬ strated by measuring visual suppres¬ sion of vestibular nystagmus.' -' In humans' and rhesus monkeys,- the normal amount of visual suppression is about 50%. It has been established that visual suppression depends on the integra¬ tion of the flocculus in the cerebel¬ lum.' The nodulus has also been impli¬ cated in the mediation of this reflex.' Maekawa et al'"' reported that ipsilateral illumination or electric stimula¬ tion of the optic disc and chiasm evoked prominent activation of Purkinje cells in the flocculus via climbing fiber afférents and also via mossy fiber afférents. This pathway has been traced through the dorsal portion of the posterior accessory optic tract, the so-called central tegmental optic tract and the rostral portion of the
It nystagmus
Accepted
for publication Sept 21, 1978. From the Departments of Neurotology (Dr Takemori) and Neurosurgery (Drs Ono and Maeda), Toranomon Hospital, Toranomon, To-
inferior olive to the flocculus. The from the pontine nuclei to the flocculus or nodulus were also demonstrated by using horseradish
projection
peroxidase.7
Some cases of cerebral disorders have failure of visual fixation; howev¬ er, sources of cerebral control have not been well identified. This study clari¬ fies the cerebral contribution to visual fixation demonstrated by visual sup¬ pression of vestibular nystagmus.
nystagmus (Fig 1). The mean maximum slow-phase velocity of caloric nystagmus in darkness during 10 s (a) and the mean slow phase velocity in light during 5 to 10 s (b) were
sion
measured. Percent of visual suppres¬ was represented by the following
expression: visual suppression (%) (a b)/a x 100 Visual suppression was 54% ± 12% in 52 =
-
normal adults. Visual suppression of 10% to 40% was defined as "reduced," and visual suppression under 10% was defined as "abolished."
METHODS Caloric nystagmus was evoked by irriga¬ tion of the external auditory canal with 20 mL of ice water for 20 s. Caloric nystagmus was recorded by electronystagmography (ENG) in darkness when the patients' eyes were covered. When caloric nystagmus reached the maximum and constant slow phase velocity, the lights were turned on for 5 to 10 s and the patients fixed their eyes on the cross mark on the ceiling or on the examiner's index finger, which was 50 cm above the patients' eyes. The lights were turned off and their eyes were re¬ covered until the cessation of caloric nystagmus. Visual suppression was repre¬ sented by measuring the visual inhibition on the slow-phase velocity of caloric
RESULTS
Thirty-two patients with cerebral by angiography or by computerized tomography were
lesions confirmed
tested. Of 17 frontal lobe lesions, 14 were frontal lobe tumors. In seven cases, visual suppression was normal, and in seven suppression was reduced or abolished. Three frontal lobe lesions were
frontoparietal tumors. In two suppression was normal,
cases, visual
and in one case it was reduced. Five patients had temporal lobe lesions: two temporal lobe tumors and three temporoparietal lobe tumors. In the case of the two temporal lobe
Fig 1.—Normal visual suppression. Caloric nystagmus toward left in darkness and light while eyes were fixed on examiner's index finger (f). Visual suppression was 56% in this case. A, Eye movement, calibration at 10°. B, Eye velocity, calibration at 20°/s. C, Slow-wave velocity, cali¬ bration at 20°/s (A, B, and C are same subjects through 3).
kyo. Reprint requests to Department of Neurotology, Toranomon Hospital, Toranomon 2-2-2, Minato-Ku, Tokyo, Japan (Dr Takemori).
Downloaded From: http://archotol.jamanetwork.com/ by a DALHOUSIE UNIVERSITY-DAL-11762 User on 06/20/2015
as
in
Fig
1
2.—Arteriovenous malformation. Left, Caloric nystagmus toward left; visual suppression was reduced. Center, Caloric nystagmus toward right; visual suppression was abolished. Right, Left carotid angiography. Fixation points were cross mark on ceiling (c) and examiner's index finger
Fig
(f).
3.—Left parieto-occipital lobe tumor. Left, Caloric nystagmus toward left; visual suppression was reduced. Center, Caloric nystagmus toward right; visual suppression was abolished. Caloric nystagmus even showed augmentation in light. Right, Computerized tomographic scan; arrow indicates tumor. Fixation points were cross mark on ceiling (c) and examiner's index finger (f).
Fig
Fig 4.—Right frontal lobe tumor with left hemiplegia. Left, Slow-phase velocity of caloric nystagmus toward left; visual suppression was reduced (14%) and it recov¬ ered (53%) after operation. Center, Slow-phase velocity of nystagmus toward right; visual suppression was abolished (—8%) and it became normal after operation. Right, Computerized tomographic scan; arrow indicates tumor.
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tumors, visual suppression was nor¬ mal, as it was in one case of temporoparietal lobe tumor. In two cases of temporoparietal lobe tumor, visual suppression was reduced or abolished. Eight patients had parietal lobe
two parietal lobe tumors, three vascular lesions, and three parieto-occipital lobe tumors. Visual suppression was reduced in the two patients with parietal lobe tu¬ mors, and was reduced or abolished in the six patients with vascular lesions or parieto-occipital lobe tumors. Two patients had occipital lobe lesions (vascular); visual suppression was normal in both.
lesions, including
REPORT OF CASES
40-year-old
Case l.-A
man
formation of the left middle cerebral artery with an intracerebral hematoma. The patient had right homonymous hemianopia. On Aug 10, 1977, surgery was performed. Neurotological examinations were conducted on Oct 20, 1977. Optokinetic nystagmus of the right was strongly impaired; saccadic and ataxic eyetracking patterns were observed. Visual suppression of caloric nystagmus in both directions was abolished or reduced
(Fig 2).
19-year-old girl complained of headache and twinkling sensa¬ tion when she looked to the right. This condition had been present for four years. A left parieto-occipital lobe tumor was found by computerized tomography. On May 20, 1977, surgery was performed. The Case 2.—A
recurring
tumor
was
fibrillary astrocytoma histologically. a
COMMENT
The results of the present study strongly suggest that certain areas of the parietal and parieto-occipital lobes are required for visual suppression of vestibular nystagmus. All of the patients in this study who had lesions in these areas showed either a reduc¬ tion or an absence of the normal visual
suppression
suddenly-
complained of severe headache, nausea, and vomiting on May 10, 1977, and was admitted to the hospital. Left carotid angiography showed an arteriovenous mal¬
determined
the lesion side was abolished (—8%), and visual suppression of caloric nystagmus toward the normal side was reduced (14%). Twenty days after the operation, optoki¬ netic nystagmus and eye-tracking patterns appeared normal. Visual suppression of caloric nystagmus toward both directions became normal (Fig 4).
as
Neurotological examinations were per¬ formed before and after the operation. Optokinetic nystagmus toward the right was strongly impaired, and saccadic eyetracking movements toward the left were present. Visual suppression of caloric nystagmus was reduced or abolished in both directions (Fig 3). Case 3.-A 52-year-old man suddenly lost consciousness with a convulsive attack on March 13, 1978. After this attack, he had gait disturbance and the left hemiplegia. A metastatic right frontal lobe tumor was found by computerized tomography. (On Dec 16, 1977, this patient had surgery for sigmoid carcinoma.) Neurotological examinations were per¬ formed. Optokinetic nystagmus toward the left was strongly impaired, and saccadic eye-tracking patterns were seen. Visual suppression of caloric nystagmus toward
response. These results are consistent with those of other workers who have suggested that the parietal lobes are involved in the integration of visual information for the purpose of spatial orientation and stabilization. Holmes^ reported that disturbance of visual orientation was found in cases of parietal lobe lesions. DennyBrown et al" also reported that visual inattention to the normal side was seen after the parietal lobe destruc¬ tion in rhesus monkeys. Smith, et al'u examined 31 anatomically verified cases and concluded that a positive optokinetic nystagmus sign in cortical lesions was most suggestive of in¬ volvement of the parietal lobe. Other researchers have established parts of the parietal lobes as areas important for the control of eye movements. The neurons that responded to visual fixa¬ tion or to visual tracking were found in area 7."" Balint" reported that psychic paralysis of visual fixation, lack of full voluntary control of eye movements while random movements were normal, and oculomotor apraxia were found in a case of bilateral lesions of the parieto-occipital areas.
Visual suppression was reduced or abolished when the lesions were in the dorsal parts of the parieto-occipital lobes, especially in the parietal lobe,
including area 7.
In contrast to these ings, lesions in other
find¬ of the
positive areas
cerebrum were not strongly asso¬ ciated with disturbances of visual suppresion. Neither temporal lobe nor occipital lobe pathologic features were associated with the abnormal visual
suppression.
In the
patients
with frontal lobe
lesions, visual suppression
was
only
reduced or abolished when the lesions extended to the parietal lobe. Recent¬ ly, there has been a report correlating unit activity in the prefrontal cortex to visual fixation that could be related to visual suppression.11 Therefore, the possibility that frontal areas are involved in visual suppression should be considered. However, the parietal lobes seem to be the main cerebral source of control of visual suppression, and they seem to modify this quick and prompt reflex that is visual suppression me¬ diated by the vestibulocerebellum and pons. Robert F.
manuscript.
Hink, PhD, assisted in editing this
References 1. Takemori S: Visual suppression test. Ann Otol 86:80-85, 1977. 2. Takemori S, Cohen B: Visual suppression of vestibular nystagmus in rhesus monkeys. Brain Res 72:203-212, 1974. 3. Takemori S, Cohen B: Loss of visual suppression of vestibular nystagmus after flocculus lesions. Brain Res 72:213-224, 1974. 4. Takemori S: Visual suppression of vestibular nystagmus after cerebellar lesions. Ann Otol 84:318-326, 1975. 5. Maekawa K, Simpson JI: Climbing fiber responses evoked in vestibulocerebellum of rabbit from visual system. J Neurophysiol 86:649\x=req-\ 666, 1973. 6. Maekawa K, Takeda T: Mossy fiber responses evoked in the cerebellar flocculus of rabbits by stimulation of the optic pathway. Brain Res 98:590-595, 1975. 7. Hoddevik GH: The pontine projection to the flocculonodular lobe and the paraflocculus studied by means of retrograde axonal transport of horseradish peroxidase in the rabbit. Exp Brain Res 30:511-526, 1977. 8. Holmes G: Disturbances of visual orientation. Br J Ophthalmol 2:449-468, 1918. 9. Denny-Brown D, Chambers RA: The parietal lobe and behavior. Res Pub Assoc Nerv Ment Dis 36:35-117, 1958. 10. Smith JL, Cogan DG: Optokinetic nystagmus: A test for parietal lobe lesions. Am J Ophthalmol 48:187-193, 1959. 11. Hyv\l=a"\rinenJ, Poranen A: Function of the parietal associate area 7 as revealed from cellular discharges in alert monkeys. Brain 97:673-692, 1974. 12. Mountcastle VB, Lynch JC, Georgopoulos A, et al: Posterior parietal association cortex of the monkey: Command function for operation within extrapersonal space. J Neurophysiol 38:871-908, 1975. 13. Sakata H, Shibutani H, Kawano K: Information processing in the parietal association areas. Adv Neurol Sci 21:1155-1167, 1977. 14. Balint R: Seelenl\l=a"\hmungdes Schauens, optische Ataxie, r\l=a"\umlicheSt\l=o"\rungder Aufmerksamkeit. Monatsschr Psychiatry Neurol 25:51-81, 1909. 15. Fuster JM: Unit activity in prefrontal cortex
during delayed-response performance:
Neuronal correlations of transient memory. J Neurophysiol 36:61-78, 1973.
Downloaded From: http://archotol.jamanetwork.com/ by a DALHOUSIE UNIVERSITY-DAL-11762 User on 06/20/2015
