ORL 41: 100-106 (1979)
Eye Movements Associated with Eye Closure 1. Normal Subjects Setsuko Takemori' Department of Neurotology, Toranomon Hospital, Tokyo
Key Words. Eye closure ■Eye bail ■Elevation • Adduction Abstract. Eye movements associated with eye closure were studied in 36 normal adults, and they were recorded by DC amplifiers of ENG. (1) Eyes moved 64 ± 17° upward and were adducted 15 ± 7° when eyes were closed. (2) The vertical eye position was held upwards in 33 persons and slightly turned down in 3 persons. (3) The superior rectus and inferior oblique muscles worked together during eye closure.
Introduction
Bell (1) discovered the well-known phenomenon of upward eye rotation with eye closure. Visual conditions such as eyes closed, eyes covered or eyes open in darkness are used to evoke nystagmus in routine vestibular function tests. Ohm (6) reported that vestibular nystagmus was inhibited by eye closure. Thus, eye closure has a strong influence on vestibular nystagmus (5) and this causes eye ball elevation (7-9). The purpose of this study is to clarify the eye movements associated with eye closure.
Methods
Horizontal and vertical eye movements of 36 normal adults were recorded by DC amplifiers of electronystagmography (ENG) and were differentiated to obtain velocity measures using silver plate electrodes.
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1 Electromyograms of external eye muscles were taken by Prof. Dr. T. Maruo (Depart ment of Ophthalmology, Teikyo University School of Medicine).
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Horizontal and vertical eye movements were recorded with eyes closed and with eyes open in darkness. 3-5 eye closures were performed. The period of closing eyes was from 3 to 10 sec because the turning down of vertical eye position usually started 2 -5 sec after closing eyes. F.lectromyograms were recorded from external eye muscles by using needle electrodes. The needle electrodes were inserted into the superior rectus, medial rectus and inferior oblique muscles.
Results
Eye Movements Associated with Eye Closure (fig. 1). Eye closure resulted in a 64 ± 17° eye ball elevation and a 15 ± 7° adduction. The vertical eye position was held upward during eye closure in 33 persons (fig. 1A), and turned down slightly in 3 persons (fig. IB). These two types of vertical eye position were seen in normal persons.
Fig. 1. Eye movements associated with eye closure. Eyes were elevated and adducted when eyes were closed. The eye position was held upwards during eye closure in 33 persons (A) and slightly turned down in 3 persons (B). The top traces are paper speed (1 mark/sec), the second and third traces are DC-recordings of the vertical and horizontal eye movements of the right eye. The calibrations represent 10°. These are the same in figure 5.
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Eye Muscle Recordings during Eye Closure. While eyes were closed, the superior rectus strongly contracted and inferior oblique muscles showed slightly increased activities. The medial rectus muscle showed no increase in activity.
Takemori
102
( rt e y e )
Fig. 3. Eye movements with eyes closed. When eyes moved upwards or downwards with eyes closed, only fluctuation around vertical eye position appeared.
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Fig. 2. Reproducibility of eye movements. The same types of eye movements appeared upon successive eye closure. The top trace is the paper speed (1 mark/sec), the second and third traces are DC recordings of the vertical and horizontal eye movements. The bottom trace is horizontal eye velocities. The calibrations represent 10° for eye movements and 20°/sec for eye velocity. These are the same in figure 3.
Eye Movements Associated with Eye Closure
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Fig. 4. Eye lid movements and vertical eye movements. Eye lid movements affected the vertical eye movements during eye closure (arrow). DC recordings of the vertical (a), and horizontal (c) eye movements, and the vertical (b) and horizontal (d) eye velocities are shown.
Effect o f Vertical Eye Movements on Upward Eye Elevation Associated with Eye Closure (fig. 3). While eyes were closed, the subjects were required to move their eyes upwards or downwards. These movements during eye closure resulted in only upward and downward fluctuating vertical eye movements; the upward baseline of eye elevation was maintained during eye closure.
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Reproducibility o f Eye Movements Associated with Eye Closure (fig. 2). The subjects were required to close their eyes 5—10 times. The type of vertical and horizontal eye movements associated with eye closure was the same on each trial.
Takemori
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Fig. 5. Eye closure, wink and blink. A Eye closure. B Stronger eye closure. C Eye closure and stronger eye closure. D Wink and blink. * Closing eyes; ** opening eyes.
Effect o f Eye Lids on Eye Movements Associated with Eye Closure (fig. 4). Eye lid movements only affected the vertical eye movement during eye closure, however the upward eye elevation was maintained while the eyes were closed.
Consciousness and Eye Movements during Eye Closure. The eyes were fixed on the center position during general anesthesia regardless of closure.
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Eye Closure, Wink and Blink (fig. 5). Eye closure resulted in eye ball elevation and adduction. Stronger eye closure produced larger eye ball elevation and adduction. Winking resulted in the same eye ball elevation and adduction as eye closure, however the eye ball returned to the initial eye position immedi ately. Blinking eye movements produced quick, low amplitude eye ball eleva tions and adductions.
Eye Movements Associated with Eye Closure
105
Discussion
When eyes were closed, the eye balls were elevated and were adducted. The superior rectus and inferior oblique muscles worked together during eye closure. This result indicates that these upward and inward eye movements associated with eye closure are controlled by the oculomotor nerves and nuclei. Electrical stimulation of the superior semicircular ampullary nerve produces strong con traction of the ipsilateral superior rectus and contralateral inferior oblique muscles, that is the ipsilateral eye moves upwards and the contralateral eye rotates (2). The excitatory vestibulo-ocular reflex pathways in rabbits have been found to extend from the anterior semicircular canal through the oculomotor nucleus and ending at the superior rectus muscle (ipsilateral) or at the inferior oblique muscle (contralateral) (3). Thus, the upward eye ball elevation may be influenced by the structures of this pathway from the anterior canal to the oculomotor nucleus. The eye movements associated with eye closure are highly consistent across eye closure manipulations. The eye ball elevation was maintained during eye closure in normal subjects. The eye lid movements and upward or downward eye movements produced only fluctuating movements on upward eye position during eye closure. Sudden turning down of the eye ball during eye closure was never found in normal subjects. Stronger eye closure caused larger eye ball elevation. Winking was associated with smaller eye ball elevations and sudden turning down of the eye ball, that is, when eyes were open slightly or widely, the vertical eye position immediately returned to the initial eye position.
Conclusion
When eyes were closed, eye balls moved 64 ± 17° upwards and 15 ± 7° in wards in 36 normal adults. The vertical eye position was held upwards during eye closure in 33 persons and slightly turned down in 3 persons. The superior rectus and inferior oblique muscles worked together during eye closure.
1
Bell, C.: On the motions of the eyes, in illustration of the uses of the muscles and nerves of the orbit. Phil. Trans. R. Soc. I l l : 166 186 (1823).
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References
Takemori
3
4
5 6 7 8 9
Cohen, B.; Suzuki, J., and Bender, M.B.: Eye movement from semicircular canal nerve stimulation in the cat. Annls Oto-lar. 73: 153-169 (1964). Ito, M.; Nisimura, N., and Yamamoto, M.: Pathways for the vestibulo-ocular reflex exitation arising from semicircular canals of rabbits. Expl Brain Res. 24: 257-271 (1976). Ito, M.; Nisimura, N., and Yamamoto, M.: Postsynaptic inhibition of oculomotor neurons involved in vestibulo-ocular reflexes arising from semicircular canals of rabbits. Expl Brain Res. 24: 273-283 (1976). Naito, T.; Tatsumi, T.; Matsunaga, T., and Matsunaga, T.: The effect of eye closure upon nystagmus Acta oto-lar., suppl. 179, pp. 72-85 (1963). Ohm, J.: Über den Einfluss des Sehens auf den vestibulären Drehnystagmus und Nachnystagmus. Z. Hals- Nasen- Ohrenheilk. 16: 521- 540 (1926). Takemori, S.: Eye closure and nystagmus. Equil. Res. 38: 46 -4 8 (1978). Takemori, S.; Moriyama, H., and Totsuka, G.: The mechanism of eye closure inhibition of caloric nystagmus. Proc. Barany Soc. Meet, (in press). Tjernström, Ö.: Nystagmus inhibition as an effect of eye closure. Acta oto-lar. 75: 408-418 (1973).
Received: January 31, 1979; accepted: February 12, 1979 Dr. Setsuko Takemori, Neurotology, Toranomon Hospital, Toranomon 2-2-2, Minato-Ku, Tokyo 107 (Japan)
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Eye Movements Associated with Eye Closure 1. Normal Subjects Setsuko Takemori' Department of Neurotology, Toranomon Hospital, Tokyo
Key Words. Eye closure ■Eye bail ■Elevation • Adduction Abstract. Eye movements associated with eye closure were studied in 36 normal adults, and they were recorded by DC amplifiers of ENG. (1) Eyes moved 64 ± 17° upward and were adducted 15 ± 7° when eyes were closed. (2) The vertical eye position was held upwards in 33 persons and slightly turned down in 3 persons. (3) The superior rectus and inferior oblique muscles worked together during eye closure.
Introduction
Bell (1) discovered the well-known phenomenon of upward eye rotation with eye closure. Visual conditions such as eyes closed, eyes covered or eyes open in darkness are used to evoke nystagmus in routine vestibular function tests. Ohm (6) reported that vestibular nystagmus was inhibited by eye closure. Thus, eye closure has a strong influence on vestibular nystagmus (5) and this causes eye ball elevation (7-9). The purpose of this study is to clarify the eye movements associated with eye closure.
Methods
Horizontal and vertical eye movements of 36 normal adults were recorded by DC amplifiers of electronystagmography (ENG) and were differentiated to obtain velocity measures using silver plate electrodes.
Downloaded by: Univ. of California Santa Barbara 128.111.121.42 - 3/5/2018 11:56:10 PM
1 Electromyograms of external eye muscles were taken by Prof. Dr. T. Maruo (Depart ment of Ophthalmology, Teikyo University School of Medicine).
Eye Movements Associated with Eye Closure
101
Horizontal and vertical eye movements were recorded with eyes closed and with eyes open in darkness. 3-5 eye closures were performed. The period of closing eyes was from 3 to 10 sec because the turning down of vertical eye position usually started 2 -5 sec after closing eyes. F.lectromyograms were recorded from external eye muscles by using needle electrodes. The needle electrodes were inserted into the superior rectus, medial rectus and inferior oblique muscles.
Results
Eye Movements Associated with Eye Closure (fig. 1). Eye closure resulted in a 64 ± 17° eye ball elevation and a 15 ± 7° adduction. The vertical eye position was held upward during eye closure in 33 persons (fig. 1A), and turned down slightly in 3 persons (fig. IB). These two types of vertical eye position were seen in normal persons.
Fig. 1. Eye movements associated with eye closure. Eyes were elevated and adducted when eyes were closed. The eye position was held upwards during eye closure in 33 persons (A) and slightly turned down in 3 persons (B). The top traces are paper speed (1 mark/sec), the second and third traces are DC-recordings of the vertical and horizontal eye movements of the right eye. The calibrations represent 10°. These are the same in figure 5.
Downloaded by: Univ. of California Santa Barbara 128.111.121.42 - 3/5/2018 11:56:10 PM
Eye Muscle Recordings during Eye Closure. While eyes were closed, the superior rectus strongly contracted and inferior oblique muscles showed slightly increased activities. The medial rectus muscle showed no increase in activity.
Takemori
102
( rt e y e )
Fig. 3. Eye movements with eyes closed. When eyes moved upwards or downwards with eyes closed, only fluctuation around vertical eye position appeared.
Downloaded by: Univ. of California Santa Barbara 128.111.121.42 - 3/5/2018 11:56:10 PM
Fig. 2. Reproducibility of eye movements. The same types of eye movements appeared upon successive eye closure. The top trace is the paper speed (1 mark/sec), the second and third traces are DC recordings of the vertical and horizontal eye movements. The bottom trace is horizontal eye velocities. The calibrations represent 10° for eye movements and 20°/sec for eye velocity. These are the same in figure 3.
Eye Movements Associated with Eye Closure
103
Fig. 4. Eye lid movements and vertical eye movements. Eye lid movements affected the vertical eye movements during eye closure (arrow). DC recordings of the vertical (a), and horizontal (c) eye movements, and the vertical (b) and horizontal (d) eye velocities are shown.
Effect o f Vertical Eye Movements on Upward Eye Elevation Associated with Eye Closure (fig. 3). While eyes were closed, the subjects were required to move their eyes upwards or downwards. These movements during eye closure resulted in only upward and downward fluctuating vertical eye movements; the upward baseline of eye elevation was maintained during eye closure.
Downloaded by: Univ. of California Santa Barbara 128.111.121.42 - 3/5/2018 11:56:10 PM
Reproducibility o f Eye Movements Associated with Eye Closure (fig. 2). The subjects were required to close their eyes 5—10 times. The type of vertical and horizontal eye movements associated with eye closure was the same on each trial.
Takemori
104
Fig. 5. Eye closure, wink and blink. A Eye closure. B Stronger eye closure. C Eye closure and stronger eye closure. D Wink and blink. * Closing eyes; ** opening eyes.
Effect o f Eye Lids on Eye Movements Associated with Eye Closure (fig. 4). Eye lid movements only affected the vertical eye movement during eye closure, however the upward eye elevation was maintained while the eyes were closed.
Consciousness and Eye Movements during Eye Closure. The eyes were fixed on the center position during general anesthesia regardless of closure.
Downloaded by: Univ. of California Santa Barbara 128.111.121.42 - 3/5/2018 11:56:10 PM
Eye Closure, Wink and Blink (fig. 5). Eye closure resulted in eye ball elevation and adduction. Stronger eye closure produced larger eye ball elevation and adduction. Winking resulted in the same eye ball elevation and adduction as eye closure, however the eye ball returned to the initial eye position immedi ately. Blinking eye movements produced quick, low amplitude eye ball eleva tions and adductions.
Eye Movements Associated with Eye Closure
105
Discussion
When eyes were closed, the eye balls were elevated and were adducted. The superior rectus and inferior oblique muscles worked together during eye closure. This result indicates that these upward and inward eye movements associated with eye closure are controlled by the oculomotor nerves and nuclei. Electrical stimulation of the superior semicircular ampullary nerve produces strong con traction of the ipsilateral superior rectus and contralateral inferior oblique muscles, that is the ipsilateral eye moves upwards and the contralateral eye rotates (2). The excitatory vestibulo-ocular reflex pathways in rabbits have been found to extend from the anterior semicircular canal through the oculomotor nucleus and ending at the superior rectus muscle (ipsilateral) or at the inferior oblique muscle (contralateral) (3). Thus, the upward eye ball elevation may be influenced by the structures of this pathway from the anterior canal to the oculomotor nucleus. The eye movements associated with eye closure are highly consistent across eye closure manipulations. The eye ball elevation was maintained during eye closure in normal subjects. The eye lid movements and upward or downward eye movements produced only fluctuating movements on upward eye position during eye closure. Sudden turning down of the eye ball during eye closure was never found in normal subjects. Stronger eye closure caused larger eye ball elevation. Winking was associated with smaller eye ball elevations and sudden turning down of the eye ball, that is, when eyes were open slightly or widely, the vertical eye position immediately returned to the initial eye position.
Conclusion
When eyes were closed, eye balls moved 64 ± 17° upwards and 15 ± 7° in wards in 36 normal adults. The vertical eye position was held upwards during eye closure in 33 persons and slightly turned down in 3 persons. The superior rectus and inferior oblique muscles worked together during eye closure.
1
Bell, C.: On the motions of the eyes, in illustration of the uses of the muscles and nerves of the orbit. Phil. Trans. R. Soc. I l l : 166 186 (1823).
Downloaded by: Univ. of California Santa Barbara 128.111.121.42 - 3/5/2018 11:56:10 PM
References
Takemori
3
4
5 6 7 8 9
Cohen, B.; Suzuki, J., and Bender, M.B.: Eye movement from semicircular canal nerve stimulation in the cat. Annls Oto-lar. 73: 153-169 (1964). Ito, M.; Nisimura, N., and Yamamoto, M.: Pathways for the vestibulo-ocular reflex exitation arising from semicircular canals of rabbits. Expl Brain Res. 24: 257-271 (1976). Ito, M.; Nisimura, N., and Yamamoto, M.: Postsynaptic inhibition of oculomotor neurons involved in vestibulo-ocular reflexes arising from semicircular canals of rabbits. Expl Brain Res. 24: 273-283 (1976). Naito, T.; Tatsumi, T.; Matsunaga, T., and Matsunaga, T.: The effect of eye closure upon nystagmus Acta oto-lar., suppl. 179, pp. 72-85 (1963). Ohm, J.: Über den Einfluss des Sehens auf den vestibulären Drehnystagmus und Nachnystagmus. Z. Hals- Nasen- Ohrenheilk. 16: 521- 540 (1926). Takemori, S.: Eye closure and nystagmus. Equil. Res. 38: 46 -4 8 (1978). Takemori, S.; Moriyama, H., and Totsuka, G.: The mechanism of eye closure inhibition of caloric nystagmus. Proc. Barany Soc. Meet, (in press). Tjernström, Ö.: Nystagmus inhibition as an effect of eye closure. Acta oto-lar. 75: 408-418 (1973).
Received: January 31, 1979; accepted: February 12, 1979 Dr. Setsuko Takemori, Neurotology, Toranomon Hospital, Toranomon 2-2-2, Minato-Ku, Tokyo 107 (Japan)
Downloaded by: Univ. of California Santa Barbara 128.111.121.42 - 3/5/2018 11:56:10 PM
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