Ann 0101 88 :1979
INHIBITION OF LABYRINTHINE NYSTAGMUS BY VISUAL FIXATION: EFFECTS OF ABLATION OF VISUAL CORTEX AND SUPERIOR COLLICULI EMIL
P.
JOSEPH
LIEBMAN,
U.
TOGLIA,
MD MD
PmLADELPlllA, PENNSYLVANIA
A study was conducted to destroy two specific areas of the eat's visual system in order to determine if these lesions would affect the visual inhibition of calorically-induced vestibular nystagmus. The occipital visual cortex was removed in eight cats and the superior colliculi were removed bilaterally in nine cats. Postoperative vestibular testing revealed no significant change in the electronystagmography tracings and response to visual fixation. These findings suggest that, in cats, the visual inhibition of labyrinthine nystagmus is not dependent upon the integrity of the visual cortex or superior colliculi. The hypothesis is brought forward that the visual inhibition of the vestibular nystagmus is merely a reflex of the brain stem to light stimulus, mediated via the cerebellum.
Much is known about the close relationship between visual and vestibular systems with relation to the pathophysiology of the vestibulo-ocular reflex: the vestibular system produces compensatory eye movements necessary for visual fixation during active and passive motion; and eye movements, i.e., optokinetic, interfere with the normal occurrence of vestibular nystagmus. Less is known about the integration of vestibular and visual stimuli at various levels of CNS function. Hom et all and Bisti et al" have demonstrated that the neurons of the visual cortex and superior colliculi are influenced by vestibular stimuli (head tilt); this conclusion is disputed by Schwartzkroin" and needs further investigation. On the other hand several experiments have shown that visual stimulations inhibit vestibular nystagmus in animals':" and man;9-16 furthermore. the absence of visual inhibition or the enhancement of nystagmus bv visual fixation is believed to signify CNS lesions. The question is here raised whether the inhibition of labyrinthine nystagmus by visual fixation is mediated via the cerebral visual cortex or is a brain stem reflex to a light stimulus similar to the pupillary light reflex. METHODS AND MATERIALS Seventeen cats were used in this series of
experiments. Eight (group 1) had surgical removal of the occipital visual cortex (Fig.l) and nine (group 2) had bilateral surgical destruction of the superior colliculi (Fig. 2). Surgical anesthesia was achieved with intravenous sodium pentobarbital. There was one postoperative death due to failure to recover from anesthesia in group 1, and two operative fatalities in group 2 due to hemorrhage from laceration of dural sinuses. In addition to these two operative procedures described, one animal from group 1 had removal of the superior colliculi three months following the first operation, and one animal from group 2 had ablation of the occipital visual cortex bilaterally three months following the first operation. All animals were sacrificed at least three months after the experiment. The anterior vascular system was irrigated with 10% formalin solution. The brains were removed and stored in 10% formalin until blocked and sectioned. Sections were stained with eresyl violet. Sections were taken so that intervals were not greater than 0.5 mm. Testing Procedures. The nystagmus induced by caloric tests was recorded with ENG using time constant of three seconds. A channel recorded the on-off activity of the light stimulus on the ENG tracing (Fig. 3). The board on which the animal was placed was situated so that the line between the external auditory canal and0 the inferior orbital ridge was elevated 45 above the horizontal plane. Ice water was introduced into the external auditory canal through intravenous tubing via zravity flow. The ice water was permitted to flow until an active horizontal nystagmus was present. Both ears were tested allowing five minutes rest between each test. Each ear was
From the Departments of Otolaryngology and Neurology, Temple University School of Medicine and Hospital, Philadelphia, Pennsylvania.
419 Downloaded from aor.sagepub.com at Bobst Library, New York University on May 14, 2015
420
LIEBMAN-TOGLIA
on
off
It
eng
"""""-
A
It
on
-.....,.,.--_....-.---.f
__
off
Fig. 3. ENG: Top line indicates on-off times of light stimulus (It). Bottom line shows synchronous electronystagmographic recording (eng). A) Inhibition of nystagmus; B) No inhibition of nystagmus.
Fig. 1. Bilateral visual cortex ablation. The least damage is shown by the area outlined by fine oblique lines. Total shaded area shows the most surgical damage. All other specimens fell within these two limits. Appropriate gyri are labeled on the left cerebral hemisphere. tested in the same manner except that a light source approximately 60 em in front of the animal was activated periodically. The light source consisted of a 50 w incandescent bulb which was automatically turned off and on. The on time was approximately seven seconds and the off time was approximately 12 seconds. A synchronous signal was simultaneously recorded on the ENG tracing to indicate the on-off times. Thus a baseline was first ob-
tained without light stimulus to determine that each animal's vestibular system was reactive and then after a five minute rest period the test was repeated with intermittent light stimulus to record changes in nystagmus produced by the light. Each animal was retested several times to determine the consistency of response. A rest period of several days was allowed between each testing procedure. After a recovery period of four weeks following each surgical procedure, animals were retested exactly as done preoperatively. RESULTS
Preoperative testing disclosed that 12 cats consistently evidenced inhibition of vestibular nystagmus as demonstrated by repeated decrease in nystagmus with
Fig. 2. Histologic demonstrations of bilateral lesions of the superior colliculi. Sections are shown caudal (A) to rostral (D). CA - Cerebral aqueduct; III - III nerve nucleus; RN - Red nucleus; MG - Medial geniculate; X - Marker.
Downloaded from aor.sagepub.com at Bobst Library, New York University on May 14, 2015
421
INHIBITION OF LABYRINTHINE NYSTAGMUS
TABLE 1. INHIBITION OF LABYRINTH NYSTAGMUS BY VISUAL FIXATION
Group 1
Group 2
(Visual cortex group) Preoperative Postoperative (Superior colliculus group) Preoperative Postoperative
Present
Absent
Total
5 4
3 3
7"
7
2 2
9 7....
5
8
'One cat died postoperatively. "Two cats died at surgery.
each light stimulus (Fig. 3). Five of these cats were from group 1 and seven from group 2 (Table 1). Vision appeared normal in all cats as judged from their ability to ambulate around furniture and other objects in a small room without difficulty. No correlation was proven with the intensity of the light and the use of a strobe light. The postoperative results of the ENG testing are summarized in Table 1. Ablations of the visual cortex or the superior colliculi produced no major changes in the distributions of cats demonstrating visual inhibition (other than those due to the death of the animal) (Figs. 4 and 5). Thus, a cat exhibiting visual inhibition before surgery demonstrated the effect following surgery as well. Those who did not exhibit inhibition before surgery did not after surgery In two animals both surgical procedures were performed. One cat from group 1 (visual cortex) had subsequent
removal of the superior colliculi three months after the visual cortex ablation and one cat from group 2 (superior colliculi) had subsequent removal of the visual cortex three months after the superior colliculi ablation. These animals who both exhibited light-evoked inhibition preoperatively continued to show visual suppression postoperatively. DISCUSSION
There are many reports in the literature relative to the effects of ablation of the visual cortex and the superior colliculi on pattern discrimination.t"?" ocular motility" and labyrinthine nystagmus. 2 2 , 2 3 Some experiments have specifically dealt with the mechanisms or pathways involved in the visual suppression of nystagmus. 2 4 , 26 Several experiments have shown this phenomenon is mediated through the accessory optic tract and the inferior olive. Axons of these Purkinje cells in tum inhibit cells of the vestibular nuclei, including cells which mediate horizontal vestibulo-ocular reflexes." Lisberger and Fuchs'" have also shown that activity at the
III ........ '
• Ii
."7
on off It -J._"---r-....._ ..r-_ _....r_IL-_......
It
•
'lJ ---..........IioAI...~....MAO\Mo..~_\A.M.....lIMfAI~
eng
B
Fig. 4. ENG tracings A) before and B) after ablation of visual cortex. Good inhibition of nystagmus with the light stimulus on both pre- and postremoval of the visual cortex bilaterally.
.'
Fig. 5. ENG tracings A) before and B) after ablation of superior colliculi; good inhibition of nystagmus with light stimulus; both pre- and postremoval of superior colliculi bilaterally.
Downloaded from aor.sagepub.com at Bobst Library, New York University on May 14, 2015
422
LIEBMAN-TOGLIA
flocculus Purkinje cells is closely associated with visual suppression of compensatory eye movements. Finally, Takemori and Cohen'" found that visual suppression of vestibular nystagmus is lost after destruction of the flocculus on both sides. Is this phenomenon dependent on the activity of the cerebral cortex, and particularly the visual cortex? The influence of the cerebral cortex on the activity of the vestibular system has been amply investigated in the past: 3 0 - 3 5 stimulation of parietotemporal cortex in guinea pigs and rabbits may cause nystagmus. It would be interesting to ascertain whether stimulation of the visual
cortex and superior colliculi (especially in decerebellated animals) affects in any way the suppressive mechanism of visual fixation on labyrinthine nystagmus. Our experiments with ablation of the occipital visual cortex and superior colliculi suggest that either the inhibition of labyrinthine nystagmus depends on a secondary (extraoccipital) visual system or it is simply the effect of a brain stem reflex to a light stimulus somewhat similar to the pupillary light reflex mediated only via the cerebellum. In order to support the second hypothesis this experiment should be repeated after total decortication.
REFERENCES 1. Horn G, Stechler G, Hill RM: Receptive fields of units in the visual cortex of the cat in the presence or absence of bodily tilt. Exp Brain Res 15: 113-132, 1972 2. Bisti G, Maffei L, Piccoli no M: Variations of the visual responses of the superior colliculus in relation to body roll. Science 175: 456-457, 1972 3. Schwartzkroin PA: The effect of body tilt on the directionality of units in cat visual cortex. Exp Neurol 36:498-501, 1972 4. Wood CC, Spear PD, Braun JJ: Direction specific defects in the horizontal optokinetic nystagmus following removal of visual cortex in the cat. Brain Res 60:231-237, 1973 5. Henriksson NC, Fernandez C, Kohut RI: The caloric test in the cat. Acta Otolaryngol (Stockh) 53:21-32, 1961 6. Crampton GH: Effects of visual experience on vestibular nystagmus habituation in the cat. Acta Otolaryngol (Stockh) 55:516526 7. Silverstein H: The cortical influence on the vestibular apparatus. Arch Otolaryngol 76: 158-166, 1962 8. Takemori S, Cohen B: Visual suppression of vestibular nystagmus in rhesus monkeys. Brain Res 72:203-212, 1974 9. Aschan G, Bergstedt M, Stanle J: Nystagmography. Recording of nystagmus in clinical neuro-otological examinations. Acta Otolaryngol (Stockh) [Suppl 129] 1956 10. McCabe BF: Vestibular suppression in figure skaters. Trans Am Acad Ophthalmol Otolaryngol 64:264-269, 1960 11. Jongkees LBW, Philipzoon AJ: Electronystagmography. Acta Otolaryngol (Stockh) [SuppI189:1-111] 1964 12. Mahoney JL, Harlan WL, Bickford RG: Visual and other factors influencing caloric nystagmus in normal subjects. Arch Otolaryngol 66:46-53, 1957
13. Collins WE, Guedry FE, Posner JB: Control of caloric nystagmus by manipulating arousal and visual fixation distance. Ann Otol Rhinol Laryngol 71: 187-202, 1962 14. Naito T, Tatsurni T, Matsunage T, et al: The effect of eye-closure upon nystagmus. Acta Otolaryngol (Stockh) [Suppl 179 :72-85] 1956 15. Sokolouski A: The influence of mental activity and visual fixation upon caloric-induced nystagmus in normal subjects. Acta Otolaryngol (Stockh) 61:209-220, 1966 16. Hart CW: Ocular fixation and the caloric test. Laryngoscope 77 :2103-2113, 1967 17. Colavita FA: Auditory cortical lesions and visual pattern discrimination in cat. Brain Res 39:437-447, 1972 18. Winans SS: Visual cues used by normal and visual-decorticate cats to discriminate figures of equal luminous flux. J Comp Physiol Psychol 74:167-178, 1971 19. Sprague JM, Meikle TH Jr: The role of the superior colliculus in visually guided behavior. Exp Neurol 11:115-146, 1965 20. Meyers RE: Visual deficits after lesions of brain stem tegmentum in cats. Arch Neurol 11 :73-90, 1964 21. Pasik T, Pasik P, Bender M: The superior colliculi and eye movements. Arch Neural 15:420-436, 1966 22. Spiegel EA, Scala NP: Effects of quadrigeminal lesions upon labyrinthine nystagmus. Confinia Neural 7 :68-76, 1946 23. Proctor LR: Experimental observations on postural nystagmus. III. Lesions of the colliculi. Ann Otol Rhinol Laryngol 71 :891-912, 1962 24. Fukuda 1. Highstein SM, Ito M: Cerebellar inhibitory control of the vestibulo-ocular reflex investigated in rabbit IIIrd nucleus. Exp Brain Res 14:511-526, 1952 25. Takemori S: Visual suppression of ves-
Downloaded from aor.sagepub.com at Bobst Library, New York University on May 14, 2015
INHIBITION OF LABYRINTHINE NYSTAGMUS tibular nystagmus after cerebellar lesions. Ann Otol Rhinol Laryngol 84:318-326, 1975 26. Mackawa K, Simpson JL: Climbing fiber response evoked in vestibulocerebellum of rabbit from visual system. J Neurophysiol 36: 649-666, 1973 27. Ito M, Nisimaru N, Yamamoto M: Specific neural connections for the cerebellar cortical vestibulo-ocular reflexes. Brain Res 60: 238-243, 1973 28. Lisberger SG, Fuchs AF: Response of flocculus cells to adequate vestibular stimulation in the alert monkey: Fixation versus compensatory eye movements. Brain Res 69 :347353, 1974 29. Takemori S, Cohen B: Loss of visual suppression of vestibular nystagmus after flocculus lesions. Brain Res 72:213-224, 1974 30. Spiegel EA, Aronson L: The interaction of cortical and labyrinthine impulses to ocular
423
muscle movements. Am J Physiol109:693-703, 1934 31. Wycis HT, Spiegel EA: Influence of cortical areas upon vestibulo-ocular reflex arc. Fed Proc 4:79-80, 1945 32. Arslan M, Molinari GA: Modifications of the activity of the vestibular nuclei in the cat following stimulation of the temporal lobe. Acta Otolaryngol (Stockh) 59:338-344, 1965 33. Pompeiano 0, Walberg F: Descending connections to the vestibular nuclei: An experimental study of the cat. J Comp Neurol 108: 455-503, 1957 34. Gildenberg PL, Hassler R: Influence of stimulation of the cerebral cortex on vestibular nuclei units in the cats. Exp Brain Res 14: 77-94, 1971 35. DiGiorgio AM, Manni E: Anatomical and functional relationship of the cerebral nystagmogenic area to some subcortical centers. Arch Ital BioI 101 :48-58, 1963
REPRINTS - Emil P. Liebman, MD, Dept. of Otorhinology, Temple University, Health Sciences Center, Philadelphia, PA 19140.
PROFESSOR OF SURGERY/OTOLARYNGOLOGY University of California at San Diego Qualifications include: 1) Eligible for certification of the American Board of Otolaryngology; 2) Medical licensure in California; 3) Special skills and experience in neurotologic surgery; 4) Experience and skill in teaching at undergraduate and postgraduate levels; 5) Experience and skill in administration in an academic environment. Salary related to academic rank of appointment within the established salary schedule of the UCSD Clinical Departments Compensation and Incentive Plan. UCSD is an Equal Opportunity!Affirmative Action Employer. Contact: Alan M. Nahum, MD, Head, Division of Otolaryngology, University Hospital (H-895), 225 West Dickinson, San Diego, CA 92093.
Downloaded from aor.sagepub.com at Bobst Library, New York University on May 14, 2015
INHIBITION OF LABYRINTHINE NYSTAGMUS BY VISUAL FIXATION: EFFECTS OF ABLATION OF VISUAL CORTEX AND SUPERIOR COLLICULI EMIL
P.
JOSEPH
LIEBMAN,
U.
TOGLIA,
MD MD
PmLADELPlllA, PENNSYLVANIA
A study was conducted to destroy two specific areas of the eat's visual system in order to determine if these lesions would affect the visual inhibition of calorically-induced vestibular nystagmus. The occipital visual cortex was removed in eight cats and the superior colliculi were removed bilaterally in nine cats. Postoperative vestibular testing revealed no significant change in the electronystagmography tracings and response to visual fixation. These findings suggest that, in cats, the visual inhibition of labyrinthine nystagmus is not dependent upon the integrity of the visual cortex or superior colliculi. The hypothesis is brought forward that the visual inhibition of the vestibular nystagmus is merely a reflex of the brain stem to light stimulus, mediated via the cerebellum.
Much is known about the close relationship between visual and vestibular systems with relation to the pathophysiology of the vestibulo-ocular reflex: the vestibular system produces compensatory eye movements necessary for visual fixation during active and passive motion; and eye movements, i.e., optokinetic, interfere with the normal occurrence of vestibular nystagmus. Less is known about the integration of vestibular and visual stimuli at various levels of CNS function. Hom et all and Bisti et al" have demonstrated that the neurons of the visual cortex and superior colliculi are influenced by vestibular stimuli (head tilt); this conclusion is disputed by Schwartzkroin" and needs further investigation. On the other hand several experiments have shown that visual stimulations inhibit vestibular nystagmus in animals':" and man;9-16 furthermore. the absence of visual inhibition or the enhancement of nystagmus bv visual fixation is believed to signify CNS lesions. The question is here raised whether the inhibition of labyrinthine nystagmus by visual fixation is mediated via the cerebral visual cortex or is a brain stem reflex to a light stimulus similar to the pupillary light reflex. METHODS AND MATERIALS Seventeen cats were used in this series of
experiments. Eight (group 1) had surgical removal of the occipital visual cortex (Fig.l) and nine (group 2) had bilateral surgical destruction of the superior colliculi (Fig. 2). Surgical anesthesia was achieved with intravenous sodium pentobarbital. There was one postoperative death due to failure to recover from anesthesia in group 1, and two operative fatalities in group 2 due to hemorrhage from laceration of dural sinuses. In addition to these two operative procedures described, one animal from group 1 had removal of the superior colliculi three months following the first operation, and one animal from group 2 had ablation of the occipital visual cortex bilaterally three months following the first operation. All animals were sacrificed at least three months after the experiment. The anterior vascular system was irrigated with 10% formalin solution. The brains were removed and stored in 10% formalin until blocked and sectioned. Sections were stained with eresyl violet. Sections were taken so that intervals were not greater than 0.5 mm. Testing Procedures. The nystagmus induced by caloric tests was recorded with ENG using time constant of three seconds. A channel recorded the on-off activity of the light stimulus on the ENG tracing (Fig. 3). The board on which the animal was placed was situated so that the line between the external auditory canal and0 the inferior orbital ridge was elevated 45 above the horizontal plane. Ice water was introduced into the external auditory canal through intravenous tubing via zravity flow. The ice water was permitted to flow until an active horizontal nystagmus was present. Both ears were tested allowing five minutes rest between each test. Each ear was
From the Departments of Otolaryngology and Neurology, Temple University School of Medicine and Hospital, Philadelphia, Pennsylvania.
419 Downloaded from aor.sagepub.com at Bobst Library, New York University on May 14, 2015
420
LIEBMAN-TOGLIA
on
off
It
eng
"""""-
A
It
on
-.....,.,.--_....-.---.f
__
off
Fig. 3. ENG: Top line indicates on-off times of light stimulus (It). Bottom line shows synchronous electronystagmographic recording (eng). A) Inhibition of nystagmus; B) No inhibition of nystagmus.
Fig. 1. Bilateral visual cortex ablation. The least damage is shown by the area outlined by fine oblique lines. Total shaded area shows the most surgical damage. All other specimens fell within these two limits. Appropriate gyri are labeled on the left cerebral hemisphere. tested in the same manner except that a light source approximately 60 em in front of the animal was activated periodically. The light source consisted of a 50 w incandescent bulb which was automatically turned off and on. The on time was approximately seven seconds and the off time was approximately 12 seconds. A synchronous signal was simultaneously recorded on the ENG tracing to indicate the on-off times. Thus a baseline was first ob-
tained without light stimulus to determine that each animal's vestibular system was reactive and then after a five minute rest period the test was repeated with intermittent light stimulus to record changes in nystagmus produced by the light. Each animal was retested several times to determine the consistency of response. A rest period of several days was allowed between each testing procedure. After a recovery period of four weeks following each surgical procedure, animals were retested exactly as done preoperatively. RESULTS
Preoperative testing disclosed that 12 cats consistently evidenced inhibition of vestibular nystagmus as demonstrated by repeated decrease in nystagmus with
Fig. 2. Histologic demonstrations of bilateral lesions of the superior colliculi. Sections are shown caudal (A) to rostral (D). CA - Cerebral aqueduct; III - III nerve nucleus; RN - Red nucleus; MG - Medial geniculate; X - Marker.
Downloaded from aor.sagepub.com at Bobst Library, New York University on May 14, 2015
421
INHIBITION OF LABYRINTHINE NYSTAGMUS
TABLE 1. INHIBITION OF LABYRINTH NYSTAGMUS BY VISUAL FIXATION
Group 1
Group 2
(Visual cortex group) Preoperative Postoperative (Superior colliculus group) Preoperative Postoperative
Present
Absent
Total
5 4
3 3
7"
7
2 2
9 7....
5
8
'One cat died postoperatively. "Two cats died at surgery.
each light stimulus (Fig. 3). Five of these cats were from group 1 and seven from group 2 (Table 1). Vision appeared normal in all cats as judged from their ability to ambulate around furniture and other objects in a small room without difficulty. No correlation was proven with the intensity of the light and the use of a strobe light. The postoperative results of the ENG testing are summarized in Table 1. Ablations of the visual cortex or the superior colliculi produced no major changes in the distributions of cats demonstrating visual inhibition (other than those due to the death of the animal) (Figs. 4 and 5). Thus, a cat exhibiting visual inhibition before surgery demonstrated the effect following surgery as well. Those who did not exhibit inhibition before surgery did not after surgery In two animals both surgical procedures were performed. One cat from group 1 (visual cortex) had subsequent
removal of the superior colliculi three months after the visual cortex ablation and one cat from group 2 (superior colliculi) had subsequent removal of the visual cortex three months after the superior colliculi ablation. These animals who both exhibited light-evoked inhibition preoperatively continued to show visual suppression postoperatively. DISCUSSION
There are many reports in the literature relative to the effects of ablation of the visual cortex and the superior colliculi on pattern discrimination.t"?" ocular motility" and labyrinthine nystagmus. 2 2 , 2 3 Some experiments have specifically dealt with the mechanisms or pathways involved in the visual suppression of nystagmus. 2 4 , 26 Several experiments have shown this phenomenon is mediated through the accessory optic tract and the inferior olive. Axons of these Purkinje cells in tum inhibit cells of the vestibular nuclei, including cells which mediate horizontal vestibulo-ocular reflexes." Lisberger and Fuchs'" have also shown that activity at the
III ........ '
• Ii
."7
on off It -J._"---r-....._ ..r-_ _....r_IL-_......
It
•
'lJ ---..........IioAI...~....MAO\Mo..~_\A.M.....lIMfAI~
eng
B
Fig. 4. ENG tracings A) before and B) after ablation of visual cortex. Good inhibition of nystagmus with the light stimulus on both pre- and postremoval of the visual cortex bilaterally.
.'
Fig. 5. ENG tracings A) before and B) after ablation of superior colliculi; good inhibition of nystagmus with light stimulus; both pre- and postremoval of superior colliculi bilaterally.
Downloaded from aor.sagepub.com at Bobst Library, New York University on May 14, 2015
422
LIEBMAN-TOGLIA
flocculus Purkinje cells is closely associated with visual suppression of compensatory eye movements. Finally, Takemori and Cohen'" found that visual suppression of vestibular nystagmus is lost after destruction of the flocculus on both sides. Is this phenomenon dependent on the activity of the cerebral cortex, and particularly the visual cortex? The influence of the cerebral cortex on the activity of the vestibular system has been amply investigated in the past: 3 0 - 3 5 stimulation of parietotemporal cortex in guinea pigs and rabbits may cause nystagmus. It would be interesting to ascertain whether stimulation of the visual
cortex and superior colliculi (especially in decerebellated animals) affects in any way the suppressive mechanism of visual fixation on labyrinthine nystagmus. Our experiments with ablation of the occipital visual cortex and superior colliculi suggest that either the inhibition of labyrinthine nystagmus depends on a secondary (extraoccipital) visual system or it is simply the effect of a brain stem reflex to a light stimulus somewhat similar to the pupillary light reflex mediated only via the cerebellum. In order to support the second hypothesis this experiment should be repeated after total decortication.
REFERENCES 1. Horn G, Stechler G, Hill RM: Receptive fields of units in the visual cortex of the cat in the presence or absence of bodily tilt. Exp Brain Res 15: 113-132, 1972 2. Bisti G, Maffei L, Piccoli no M: Variations of the visual responses of the superior colliculus in relation to body roll. Science 175: 456-457, 1972 3. Schwartzkroin PA: The effect of body tilt on the directionality of units in cat visual cortex. Exp Neurol 36:498-501, 1972 4. Wood CC, Spear PD, Braun JJ: Direction specific defects in the horizontal optokinetic nystagmus following removal of visual cortex in the cat. Brain Res 60:231-237, 1973 5. Henriksson NC, Fernandez C, Kohut RI: The caloric test in the cat. Acta Otolaryngol (Stockh) 53:21-32, 1961 6. Crampton GH: Effects of visual experience on vestibular nystagmus habituation in the cat. Acta Otolaryngol (Stockh) 55:516526 7. Silverstein H: The cortical influence on the vestibular apparatus. Arch Otolaryngol 76: 158-166, 1962 8. Takemori S, Cohen B: Visual suppression of vestibular nystagmus in rhesus monkeys. Brain Res 72:203-212, 1974 9. Aschan G, Bergstedt M, Stanle J: Nystagmography. Recording of nystagmus in clinical neuro-otological examinations. Acta Otolaryngol (Stockh) [Suppl 129] 1956 10. McCabe BF: Vestibular suppression in figure skaters. Trans Am Acad Ophthalmol Otolaryngol 64:264-269, 1960 11. Jongkees LBW, Philipzoon AJ: Electronystagmography. Acta Otolaryngol (Stockh) [SuppI189:1-111] 1964 12. Mahoney JL, Harlan WL, Bickford RG: Visual and other factors influencing caloric nystagmus in normal subjects. Arch Otolaryngol 66:46-53, 1957
13. Collins WE, Guedry FE, Posner JB: Control of caloric nystagmus by manipulating arousal and visual fixation distance. Ann Otol Rhinol Laryngol 71: 187-202, 1962 14. Naito T, Tatsurni T, Matsunage T, et al: The effect of eye-closure upon nystagmus. Acta Otolaryngol (Stockh) [Suppl 179 :72-85] 1956 15. Sokolouski A: The influence of mental activity and visual fixation upon caloric-induced nystagmus in normal subjects. Acta Otolaryngol (Stockh) 61:209-220, 1966 16. Hart CW: Ocular fixation and the caloric test. Laryngoscope 77 :2103-2113, 1967 17. Colavita FA: Auditory cortical lesions and visual pattern discrimination in cat. Brain Res 39:437-447, 1972 18. Winans SS: Visual cues used by normal and visual-decorticate cats to discriminate figures of equal luminous flux. J Comp Physiol Psychol 74:167-178, 1971 19. Sprague JM, Meikle TH Jr: The role of the superior colliculus in visually guided behavior. Exp Neurol 11:115-146, 1965 20. Meyers RE: Visual deficits after lesions of brain stem tegmentum in cats. Arch Neurol 11 :73-90, 1964 21. Pasik T, Pasik P, Bender M: The superior colliculi and eye movements. Arch Neural 15:420-436, 1966 22. Spiegel EA, Scala NP: Effects of quadrigeminal lesions upon labyrinthine nystagmus. Confinia Neural 7 :68-76, 1946 23. Proctor LR: Experimental observations on postural nystagmus. III. Lesions of the colliculi. Ann Otol Rhinol Laryngol 71 :891-912, 1962 24. Fukuda 1. Highstein SM, Ito M: Cerebellar inhibitory control of the vestibulo-ocular reflex investigated in rabbit IIIrd nucleus. Exp Brain Res 14:511-526, 1952 25. Takemori S: Visual suppression of ves-
Downloaded from aor.sagepub.com at Bobst Library, New York University on May 14, 2015
INHIBITION OF LABYRINTHINE NYSTAGMUS tibular nystagmus after cerebellar lesions. Ann Otol Rhinol Laryngol 84:318-326, 1975 26. Mackawa K, Simpson JL: Climbing fiber response evoked in vestibulocerebellum of rabbit from visual system. J Neurophysiol 36: 649-666, 1973 27. Ito M, Nisimaru N, Yamamoto M: Specific neural connections for the cerebellar cortical vestibulo-ocular reflexes. Brain Res 60: 238-243, 1973 28. Lisberger SG, Fuchs AF: Response of flocculus cells to adequate vestibular stimulation in the alert monkey: Fixation versus compensatory eye movements. Brain Res 69 :347353, 1974 29. Takemori S, Cohen B: Loss of visual suppression of vestibular nystagmus after flocculus lesions. Brain Res 72:213-224, 1974 30. Spiegel EA, Aronson L: The interaction of cortical and labyrinthine impulses to ocular
423
muscle movements. Am J Physiol109:693-703, 1934 31. Wycis HT, Spiegel EA: Influence of cortical areas upon vestibulo-ocular reflex arc. Fed Proc 4:79-80, 1945 32. Arslan M, Molinari GA: Modifications of the activity of the vestibular nuclei in the cat following stimulation of the temporal lobe. Acta Otolaryngol (Stockh) 59:338-344, 1965 33. Pompeiano 0, Walberg F: Descending connections to the vestibular nuclei: An experimental study of the cat. J Comp Neurol 108: 455-503, 1957 34. Gildenberg PL, Hassler R: Influence of stimulation of the cerebral cortex on vestibular nuclei units in the cats. Exp Brain Res 14: 77-94, 1971 35. DiGiorgio AM, Manni E: Anatomical and functional relationship of the cerebral nystagmogenic area to some subcortical centers. Arch Ital BioI 101 :48-58, 1963
REPRINTS - Emil P. Liebman, MD, Dept. of Otorhinology, Temple University, Health Sciences Center, Philadelphia, PA 19140.
PROFESSOR OF SURGERY/OTOLARYNGOLOGY University of California at San Diego Qualifications include: 1) Eligible for certification of the American Board of Otolaryngology; 2) Medical licensure in California; 3) Special skills and experience in neurotologic surgery; 4) Experience and skill in teaching at undergraduate and postgraduate levels; 5) Experience and skill in administration in an academic environment. Salary related to academic rank of appointment within the established salary schedule of the UCSD Clinical Departments Compensation and Incentive Plan. UCSD is an Equal Opportunity!Affirmative Action Employer. Contact: Alan M. Nahum, MD, Head, Division of Otolaryngology, University Hospital (H-895), 225 West Dickinson, San Diego, CA 92093.
Downloaded from aor.sagepub.com at Bobst Library, New York University on May 14, 2015
