ORL 40: 312-318 (1978)
Effect of Macular Ablation on Vertical Optokinetic Nystagmus in the Squirrel Monkey1 Makoto Igarashi, Masahim Takahashi, Takeshi Kubo, Joel K. Levy and Jerry L. Homick2 Department of Otorhinolaryngology and Communicative Sciences, Baylor College of Medicine, Houston, Tex.
Key Words. Vertical optokinetic nystagmus ■Maculat ablation • Squirrel monkey Abstract. After macular ablation in squirrel monkeys, a significant improvement of the slow-phase eye speed of vertical optokinetic nystagmus (VOKN) was found. This finding is in contrast to the result of our previous study in which horizontal optokinetic nystagmus (HOKN) was not improved following macular ablation. The different influence of macular ablation on HOKN and VOKN could be due to the directional characteristics of vestibular and visual interaction relative to the direction of gravity and to the difference in horizontal and vertical vestibulo-oculomotor neural pathways, including vestibular end-organs. The vertical directional dominance which was observed preoperatively was similarly observed in the postablative status; the upward slow-phase nystagmus was easier to provoke than the downward nystagmus by application of an identical stimulus.
It might be reasonable to speculate that in certain animal species horizontal eye movement (and head rotation) is necessary in order to compensate for the narrowed visual field in the case of frontally positioned eyes (compared to laterally positioned eyes), insofar as the animal’s living environment is widely spread over the horizontal terrestrial plane. The vestibular system of these animals is considered to function with maximal efficacy in the horizontal plane
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1 This study was partly supported by NASA contract NAS-9-14546, NINCDS grants NS 10940 and NS07237, and McFadden Trust Research Fund. Presented at the Research Forum meeting (AAO-ARO), Las Vegas, Nev., September 1978. 7 Neurophysiology Laboratory, Medical Sciences Division, NASA L.B. Johnson Space Center, Houston, Tex.
Effect of Macular Ablation
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for proper body equilibrium operation, posture maintenance and locomotion under ordinary gravity environment. It is reasonably suspected that optokinetic nystagmus which is an ocular pursuit activity can also be maximal in the horizontal plane. Previous investigations have dealt with all different aspects of the horizontal optokinetic nystagmus (HOKN); however, only a limited number of studies in experimental animals are available regarding the vertical optokinetic nystagmus (VOKN; Krieger and Bender, 1956; Collins et al., 1970; Collewijn and Noorduin, 1972a, b; Vital-Durand and Jeannerod, \91\\Takahashi and Igarashi, 1977). As far as the vestibular end-organ-oculomotor reactor linkage is con cerned, a difference exists neuroanatomically between the horizontal and the vertical oculomotor tracts. We have previously reported that in the squirrel monkey, the provocation of VOKN was more difficult when compared to that of the HOKN (Takahashi and Igarashi, 1977). When a ramp speed stimulus (0-200 °/sec speed with 1 °/sec2 angular acceleration) was applied, the saturation points to upward optokinetic stimulation and to downward stimulation were not equal; the latter was found to be lower than the former. In the present study, we surgically ablated the macular end-organ, which is the major gravitational receptor, and examined the effect on VOKN.
Methods
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9 healthy, young adult squirrel monkeys were used in this experiment. Their body weights ranged from 450 to 600 g. The apparatus used for optokinetic stimulus application was a cylinder, 60 cm in diameter, and 60 cm in height. The white interior was well illuminated and had 16 black stripes which were 1.5 cm wide and equally spaced. The animal was placed in a laboratory-built restrainer. Subdermal platinum needle electrodes were implanted at an equal distance above and below the monkey’s right eye. All tests were started 15 min after the injection of amphetamine (0.5 mg/kg). The vertical eye movement was recorded on a Beckman dynograph recorder through a DC amplifier. The test was performed in the upright position. The position of the animal’s head (visual plane) was adjusted to aim at the center of the stimulus cylinder. An eye speed calibration (upward direction and downward direction) was performed immediately before the test utilizing a 10°/sec constant-speed stimulus. For the optokinetic stimulus, a ramp speed of 0-200°/sec was used with a constant angular acceleration of l°/sec: . When the speed of the optokinetic stimulus reached 200°/sec the illumination was instantaneously eliminated in order to record the optokinetic after-nystagmus. The upward slow-phase stimulus was given first, followed by a minimum of 5 min rest period, and then the downward slow-phase stimulus was given. The slow-phase eye velocity was manually analyzed from the electronystagmographic recordings.
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Igarashi/Takahashi/Kubo/Levy/Homick 314
Effect of Macular Ablation
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The test was repeated once a week to establish a baseline. The bilateral utricular nerve section and saccular macula destruction were then performed. The interval between the bilateral operations was about 1 month. Starting about 2 weeks after each operation, tests were performed and a minimum of two measurements was done. Upon completion of the measurements the animals were sacrificed by means of transcardiac fixative perfusion and serial horizontal sections of the temporal bones were prepared in celloidin for light-micro scopic evaluation of the surgical lesions. 2 normal control monkeys were tested according to an identical repetitive test sequence for the same length of time.
Results
Fig. 1. Comparison of the average (n = 9) of the slow-phase eye speeds (ordinate) before (o) and after bilateral (two-staged; •) macular ablation, in the upward (a) and downward (b) stimulus conditions. A ramp speed of 0-200°/sec (abscissa) was applied with a constant angular acceleration of l°/sec2. Vertical bars represent the standard error of the means.
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Figures la, b demonstrate a comparison of the average of the slow-phase eye velocities, before and after bilateral macular ablation, in 9 monkeys. Postoperatively, a clear improvement in slow-phase eye speeds and saturation points was observed both in upward and downward stimulus conditions. The standard error of means slightly increased postoperatively. 2 control animals (with no operation) did not show any clear change. A three-factor analysis of variance was done (with repeated measures on all three factors: operation, stimulus direction and stimulus speed) on the slowphase eye speeds. The difference between pre- and postoperative VOKN was found to be significant. Overall significant differences (p
Effect of Macular Ablation on Vertical Optokinetic Nystagmus in the Squirrel Monkey1 Makoto Igarashi, Masahim Takahashi, Takeshi Kubo, Joel K. Levy and Jerry L. Homick2 Department of Otorhinolaryngology and Communicative Sciences, Baylor College of Medicine, Houston, Tex.
Key Words. Vertical optokinetic nystagmus ■Maculat ablation • Squirrel monkey Abstract. After macular ablation in squirrel monkeys, a significant improvement of the slow-phase eye speed of vertical optokinetic nystagmus (VOKN) was found. This finding is in contrast to the result of our previous study in which horizontal optokinetic nystagmus (HOKN) was not improved following macular ablation. The different influence of macular ablation on HOKN and VOKN could be due to the directional characteristics of vestibular and visual interaction relative to the direction of gravity and to the difference in horizontal and vertical vestibulo-oculomotor neural pathways, including vestibular end-organs. The vertical directional dominance which was observed preoperatively was similarly observed in the postablative status; the upward slow-phase nystagmus was easier to provoke than the downward nystagmus by application of an identical stimulus.
It might be reasonable to speculate that in certain animal species horizontal eye movement (and head rotation) is necessary in order to compensate for the narrowed visual field in the case of frontally positioned eyes (compared to laterally positioned eyes), insofar as the animal’s living environment is widely spread over the horizontal terrestrial plane. The vestibular system of these animals is considered to function with maximal efficacy in the horizontal plane
Downloaded by: Lund University Libraries 130.235.66.10 - 1/1/2019 7:48:00 PM
1 This study was partly supported by NASA contract NAS-9-14546, NINCDS grants NS 10940 and NS07237, and McFadden Trust Research Fund. Presented at the Research Forum meeting (AAO-ARO), Las Vegas, Nev., September 1978. 7 Neurophysiology Laboratory, Medical Sciences Division, NASA L.B. Johnson Space Center, Houston, Tex.
Effect of Macular Ablation
313
for proper body equilibrium operation, posture maintenance and locomotion under ordinary gravity environment. It is reasonably suspected that optokinetic nystagmus which is an ocular pursuit activity can also be maximal in the horizontal plane. Previous investigations have dealt with all different aspects of the horizontal optokinetic nystagmus (HOKN); however, only a limited number of studies in experimental animals are available regarding the vertical optokinetic nystagmus (VOKN; Krieger and Bender, 1956; Collins et al., 1970; Collewijn and Noorduin, 1972a, b; Vital-Durand and Jeannerod, \91\\Takahashi and Igarashi, 1977). As far as the vestibular end-organ-oculomotor reactor linkage is con cerned, a difference exists neuroanatomically between the horizontal and the vertical oculomotor tracts. We have previously reported that in the squirrel monkey, the provocation of VOKN was more difficult when compared to that of the HOKN (Takahashi and Igarashi, 1977). When a ramp speed stimulus (0-200 °/sec speed with 1 °/sec2 angular acceleration) was applied, the saturation points to upward optokinetic stimulation and to downward stimulation were not equal; the latter was found to be lower than the former. In the present study, we surgically ablated the macular end-organ, which is the major gravitational receptor, and examined the effect on VOKN.
Methods
Downloaded by: Lund University Libraries 130.235.66.10 - 1/1/2019 7:48:00 PM
9 healthy, young adult squirrel monkeys were used in this experiment. Their body weights ranged from 450 to 600 g. The apparatus used for optokinetic stimulus application was a cylinder, 60 cm in diameter, and 60 cm in height. The white interior was well illuminated and had 16 black stripes which were 1.5 cm wide and equally spaced. The animal was placed in a laboratory-built restrainer. Subdermal platinum needle electrodes were implanted at an equal distance above and below the monkey’s right eye. All tests were started 15 min after the injection of amphetamine (0.5 mg/kg). The vertical eye movement was recorded on a Beckman dynograph recorder through a DC amplifier. The test was performed in the upright position. The position of the animal’s head (visual plane) was adjusted to aim at the center of the stimulus cylinder. An eye speed calibration (upward direction and downward direction) was performed immediately before the test utilizing a 10°/sec constant-speed stimulus. For the optokinetic stimulus, a ramp speed of 0-200°/sec was used with a constant angular acceleration of l°/sec: . When the speed of the optokinetic stimulus reached 200°/sec the illumination was instantaneously eliminated in order to record the optokinetic after-nystagmus. The upward slow-phase stimulus was given first, followed by a minimum of 5 min rest period, and then the downward slow-phase stimulus was given. The slow-phase eye velocity was manually analyzed from the electronystagmographic recordings.
Downloaded by: Lund University Libraries 130.235.66.10 - 1/1/2019 7:48:00 PM
Igarashi/Takahashi/Kubo/Levy/Homick 314
Effect of Macular Ablation
315
The test was repeated once a week to establish a baseline. The bilateral utricular nerve section and saccular macula destruction were then performed. The interval between the bilateral operations was about 1 month. Starting about 2 weeks after each operation, tests were performed and a minimum of two measurements was done. Upon completion of the measurements the animals were sacrificed by means of transcardiac fixative perfusion and serial horizontal sections of the temporal bones were prepared in celloidin for light-micro scopic evaluation of the surgical lesions. 2 normal control monkeys were tested according to an identical repetitive test sequence for the same length of time.
Results
Fig. 1. Comparison of the average (n = 9) of the slow-phase eye speeds (ordinate) before (o) and after bilateral (two-staged; •) macular ablation, in the upward (a) and downward (b) stimulus conditions. A ramp speed of 0-200°/sec (abscissa) was applied with a constant angular acceleration of l°/sec2. Vertical bars represent the standard error of the means.
Downloaded by: Lund University Libraries 130.235.66.10 - 1/1/2019 7:48:00 PM
Figures la, b demonstrate a comparison of the average of the slow-phase eye velocities, before and after bilateral macular ablation, in 9 monkeys. Postoperatively, a clear improvement in slow-phase eye speeds and saturation points was observed both in upward and downward stimulus conditions. The standard error of means slightly increased postoperatively. 2 control animals (with no operation) did not show any clear change. A three-factor analysis of variance was done (with repeated measures on all three factors: operation, stimulus direction and stimulus speed) on the slowphase eye speeds. The difference between pre- and postoperative VOKN was found to be significant. Overall significant differences (p
