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The Journal of Neuroscience, February 15, 1999, 19(4):1524-1531
Optokinetic and Vestibular Stimulation Determines the Spatial Orientation of Negative Optokinetic Afternystagmus in the Rabbit
Vito E. Pettorossi1, Pierangelo Errico2, Aldo Ferraresi2, and Neal H. Barmack3 1 Institute of Human Physiology, University of Perugia, I-06100 Italy, 2 Institute of Human Physiology of Catholic University, Rome, I-06100 Italy, and 3 Neurological Sciences Institute, Oregon Health Sciences University, Portland, Oregon 97201-3098
ABSTRACT
Top
Abstract
Introduction
Prolonged binocular optokinetic stimulation (OKS) in the rabbit induces a high-velocity negative optokinetic afternystagmus (OKAN II) that persists for several hours. We have taken advantage of this uniform nystagmus to study how changes in static head orientation in the pitch plane might influence the orientation of the nystagmus. After horizontal OKS, the rotation axis of the OKAN II remained almost constant in space as it was kept aligned with the gravity vector when the head was pitched by as much as 80° up and 35° down. Moreover, during reorientation, slow-phase eye velocity decreased according to the head pitch angle.
Thereafter, we analyzed the space orientation of OKAN II after optokinetic stimulation during which the head and/or the OKS were pitched upward and downward. The rotation axis of OKAN II did not remain aligned with an earth vertical axis nor a head vertical axis, but it tended to be aligned with that of the OKS respace. The slow-phase eye velocity of OKAN II was also affected by the head pitch angle during OKS, because maximal OKAN II velocity occurred at the same head pitch angle as that during optokinetic stimulation.
We suggest that OKAN II is coded in gravity-centered rather than in head-centered coordinates, but that this coordinate system may be influenced by optokinetic and vestibular stimulation. Moreover, the velocity attenuation of OKAN II seems to depend on the mismatch between the space-centered nystagmus rotation axis orientation and that of the "remembered" head-centered optokinetic pathway activated by OKS.
Key words: optokinetic afternystagmus; eye movement; inertial coordinates; head position; optokinetic stimulus; slow-phase eye velocity
INTRODUCTION
Most of reflexive eye movements shows spatial constancy. In monkeys, optokinetic afternystagmus (OKAN) tends to align with the gravitational axis after off-vertical axis stimulation (Dai et al., 1991
), and the rotation axis of the horizontal postrotatory nystagmus (PRN) remains fixed in space when the head is tilted (Merfeld et al., 1993
To accomplish the transformation from head-centered to space-centered coordinates, information about head position in space is required. The otolith signal could be the most important input responsible for aligning optokinetic afternystagmus or postrotatory nystagmus with the direction of the gravity vector, because it provides information about static head position in space. However, the alignment of the reflexive eye responses may not be simply influenced by the otolithic signal, but other sensory information may be also important in modifying the response orientation, inducing a change in the internal reference frame. In the previous experiments, the issue of a possible modification of the nystagmus orientation was not studied. The possible influence of nonvestibular sensory input in modifying response orientation can be addressed by using prolonged, binocular optokinetic stimulations. This would induce a plastic changes in the visuovestibular circuitry, which may affect the internal reference frame.
In the present paper, we investigated how optokinetic and gravitational stimulation influenced the nystagmus reference frame of rabbits. We used prolonged (24-48 hr) binocular optokinetic stimulation to establish a constant velocity nystagmus, termed negative optokinetic afternystagmus (OKAN II). The slow phase of OKAN II is opposite to the direction of the optokinetic stimulus and may reflect an adaptive process aimed at counteracting a persistent unidirectional retinal stimulation (Malcolm and Melvill-Jones, 1970
After establishing OKAN II, we measured the rotation axis of its slow phase during different perturbations of the head about the interaural axis (pitch). Thereafter, we investigated the effect of different rotation angles of the optokinetic drum combined with different head pitch angles on the OKAN II orientation to ascertain whether the nystagmus would be always oriented in the horizontal plane of the earth or would change its orientation according to the plane of optokinetic stimulation.
MATERIALS AND METHODS Subjects. Thirteen pigmented rabbits were anesthetized with ketamine hydrochloride (50 mg/kg), xylazine (6 mg/Kg), and acepromazine maleate (1.2 mg/kg) to fix two stainless steel screws to the calvarium aligned in a stereotaxic apparatus so that the lambda suture was 1.5 mm above the bregma suture (0° stereotaxic).
Optokinetic stimulation. Rabbits were placed in a restrainer at the center of a contour-rich patterned optokinetic drum (diameter of 110 cm, height of 115 cm). The direction of optokinetic stimulation (OKS) was in the posteroanterior direction [posterior (P)
anterior (A)] with respect to the left eye. The head of the rabbit was fixed to the apparatus by a spring-loaded flexible coupling. This coupling attached to the implanted head screws. This device prevented lateral head displacement, permitting only small phasic sagittal movements, so that the imposed head position was maintained throughout the optokinetic stimulation. The body of the rabbit was encased in foam rubber and fixed with elastic straps to a plastic tube aligned with the longitudinal axis of the rate table. The method of restraint caused no pressure on any part of the body.
Rabbits received optokinetic stimulation for 48 hr at 5°/sec of drum velocity to evoke OKAN II with a relative constant velocity (Barmack and Nelson, 1987
Head and stimulus orientation during conditioning procedure. The spring-loaded flexible coupling that attached the head to the restrainer was positioned at an angle of 12° in the posteroanterior direction. This angle aligned the horizontal semicircular canals so that they were orthogonal to the direction of gravity (0° pitch angle) (Barmack, 1987
Eye movement recording. After 48 hr of optokinetic stimulation, the rabbits were placed in the dark, and the head was attached to a rigid restraining bar pitched downward 12° in the posteroanterior direction. Eye movements were measured by infrared light projection technique. The right eye was topically anesthetized with proparacaine hydrochloride, and a small suction cup (diameter of 3 mm, weight of 135 mg) bearing a light-emitting diode (LED) was attached to the right eye so that the axis of light was aligned with the visual axis (Barmack and Nelson, 1987
The eye position was expressed as a rotation vector E = tan (
/2) u [where u is the unity vector, and
was calculated [
Average SPEV of both horizontal and vertical components was computed from multiple intersaccadic samples taken at 5 msec intervals. Averaged values were used, because under some stimulus conditions, slow phases were curvilinear rather than constant velocity. This was especially true after large changes in head pitch angles. Usually, 20-30 consecutive slow-phase velocities values were averaged when their variability was <5% (~15 sec after a step change in head position was completed). Single slow-phase velocity values were used only for describing the time course of changes in slow-phase velocity immediately after a step change in head position.
A first-order exponential decay (y = y0 + Ae
(x
Statistical evaluation. Statistical evaluations were performed by using a t test, and a difference was considered statistically significant at p < 0.05. The goodness fit was established by
2 for sine function and by correlation coefficient (R) for exponential decay, 1- and 2°-order polynomials. The fit was obtained by minimizing the mean square error between the data and the curve (Levenberg-Marquardt algorithm).
RESULTS Rotation axis of OKAN II remains fixed in space during changes in head pitch angle
Four rabbits received 48 hr of horizontal optokinetic stimulation (P
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Figure 1. Shift in rotation axis of OKAN II induced by change in head pitch angle. A, Example of eye position record during OKAN II in which horizontal eye position is plotted against vertical eye position. Eye movements during OKAN II were restricted to a horizontal plane when the head pitch angle was maintained at 0° (1, head pitch of 0°). When the head was pitched up (2, 45° CCW), the plane of eye movements shifted by approximately the same angle in CW direction to maintain the axis of eye movement vertical in space. B, Example of horizontal and vertical eye movements as a function of time. The top two traces represent horizontal and vertical eye position. The bottom two traces represent horizontal and vertical eye velocity. The middle trace represents head pitch angle.
The reorientation had a gain (angle of OKAN II rotation axis rehead vertical-head pitch angle) close to 1 within a range of pitch angle of ~35° CW and 80° CCW (Fig. 2). Beyond this range, the reorientation showed a progressive reduction. The nystagmus reorientation over the whole range of pitch angles was fitted by a sinusoid. This sinusoid showed a phase shift of ~20° in CCW direction of head pitch angle and a vertical shift of ~22° in CW direction of rotation axis angle (Fig. 2, Table 1). The reorientation gains were not affected by the absolute value of the velocity of the nystagmus. The gains were similar in all the animals, although there were large differences in nystagmus velocity, ranging from 15 to 50°/sec. The gains were not changed when the head was pitched slowly (0.2°/sec) or when it was pitched abruptly (40°/sec). In other words, the gain of OKAN II reorientation appeared to be dependent on activation of the otolithic receptors but not the vertical semicircular canals.
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Figure 2. OKAN II rotation axis and velocity of slow phase are dependent on head pitch angle. A, In four rabbits, the rotation axis of OKAN II was measured while the head pitch angle was systematically varied. Each data point represents the mean of 20 consecutive slow-phase values. Data points were fitted with a sinusoid whose width comprises a 95% confidence interval (
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Table 1. Change in the rotation axis and slow-phase eye velocity of OKAN II Beyond 90° of pitch, the reorientation values deviated from a sinusoidal function, primarily in downward direction, because the nystagmus orientation did not decrease as much as the sine function predicted (Fig. 2). The nystagmus had an abrupt inversion, because the vertical component changed direction within a few degrees of head pitch (Figs. 2, 3). This inversion occurred at 150 ± 11° in CW direction of head pitch. The rotation axis at the center of maximal nystagmus reorientation and that at the inversion point were displaced from the earth vertical by approximately the same amount (20-30°) in CCW direction.
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Figure 3. Abrupt shift in rotation axis of OKAN II induced by a small change in head pitch angle near supine orientation. When the head pitch angle changed by small increments near the angle of 135-150° (CW direction), there was a large change in the axis of rotation of OKAN II of nearly 90°. A, The head pitch angle was changed from 124 (1) to 138 (2) and then to 150° (3). Note that the axis of rotation of OKAN II changed abruptly when the head pitch angle changed from 138 to 150°. B, Examples of horizontal and vertical eye movements as a function of time. The top two traces represent horizontal and vertical eye position. The bottom two traces represent horizontal and vertical eye velocity. The middle trace represents head pitch angle.
Changes in the OKAN II rotation axis occurred over a time course of <3 sec after a step pitch displacement. The time constants of these changes varied between 0.5 and 1.2 sec (Fig. 4).
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Figure 4. Step change in head pitch angle induces a change in OKAN II rotation axis and a decrease in slow-phase velocity. Step changes in head pitch angle in both the CW (A) and CCW (B) directions from an initial horizontal head position (head pitch of 0°) caused both a decrease in absolute OKAN II slow-phase velocity (dashed line) and a change in its horizontal (open squares) and vertical (open circles) velocity components. The 45° step in either direction was executed within 1 sec, as indicated by the obliquely shaded bars in A and B. The rotation axis of the nystagmus is indicated by the filled diamonds. Note that the change in the nystagmus rotation axis after a step change in the CW direction (A) is substantially completed before there is a decrease in slow-phase velocity.
In addition to the relative change in the vertical and horizontal velocity components, reorientation was accompanied by a reduction of the absolute SPEV. The time constant of this decay was longer than the reorientation time constant, having a value of ~1.5 sec in the CCW direction and 5.2 sec in the CW direction. In CW head pitch, nystagmus decay in slow-phase velocity began when 70% of the reorientation was already completed. When the animals were pitched back to the 0° position, the return of the slow-phase velocity to the value observed at 0° pitch angle was much slower.
OKAN II slow-phase velocity had the maximal value at 0° pitch angle and decreased progressively when the rabbits were pitched upward and downward (Fig. 2). At 90° (nose up), OKAN II slow-phase velocity was reduced by 90% of its maximal value at 0°. This decrease in OKAN II slow-phase velocity was greater in CCW head pitch than in CW pitch. A second-order polynomial fitting curve, evaluated within ±90°, showed a peak value of 8 ± 4° shifted toward head pitch down (Fig. 2, Table 1).
OKAN II induced by oblique optokinetic stimulation at 0° head pitch angle
Three rabbits received oblique OKS in upward direction (P
20°). The rotation axis of the OKAN II was inclined ~12° in CW direction (Fig. 5). For both downward and upward stimulation, the sine curves fitting the orientation values over the whole range of head pitch angles were also shifted by almost the same amount in CCW and CW direction, respectively, as shown by their vertical shift (Fig. 5, Table 1), although there was no significant phase shift and no change in the inversion points. In addition, measurements of eye velocity indicated that the peak velocity for OKAN II evoked under both stimulus condition was almost the same (Fig. 5, Table 1).
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Figure 5. The OKAN II rotation axis is shifted by a change in the axis of rotation of the optokinetic stimulus when the head is maintained in a fixed horizontal orientation. A rabbit received optokinetic stimulation at two different angles with respect to the head: a downward oblique stimulation for the left eye (head pitch of 0°, OKS of
OKAN II induced by horizontal optokinetic stimulation at different head pitch angles
Three animals received horizontal OKS with the head pitched 20° in CCW and CW directions (head pitch of ±20°, OKS of 0°). These stimulus combinations provided oblique OKS in retinal coordinates but horizontal OKS in space coordinates. Subsequently, OKAN II had rotation axis close to the earth vertical and tended to remain in earth vertical when the angle of head pitch was changed. In other words, OKAN II had the same characteristics as the OKAN II evoked by 0° OKS at 0° head pitch angle (Fig. 6). No differences were observed for the inversion point. The slow phase of the OKAN II was not changed in either CCW or CW directions, as shown by the fitted sinusoid in Figure 6 and Table 1. However, the pitch angle of the head at which the maximal OKAN II slow-phase velocity occurred corresponded to the pitch angle of the head during optokinetic stimulation. If the head was pitched CW (head pitch of
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Figure 6. SPEV of OKAN II is modified by a change in the head position maintained during the optokinetic stimulation. A rabbit received horizontal optokinetic stimulation at two different head pitch angles: head pitch of
OKAN II induced by combined inclination of optokinetic stimulation and head position
Three rabbits received oblique optokinetic stimulation (35°; P
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Figure 7. The rotation axis of OKAN II is shifted by a change in both the optokinetic rotation axis and the head position. A rabbit received oblique optokinetic stimulation (left eye) at head pitch angle with the same inclination: head pitch of +35°, OKS of +35° (right drawing); and horizontal stimulation: head pitch of 0°, OKS of 0° (left drawing). A, OKAN II rotation axis was plotted against head orientation, and data points were fitted with a sinusoid whose width comprises a 95% confidence interval. For the head pitch of +35°, OKS of 0°, data points are filled squares, fitted with a dark gray sinusoid, and for head pitch of 0°, OKS of 0°, data points are open squares, fitted with a light gray sinusoid. After oblique head and stimulus inclination, the OKAN II rotation axis was shifted in CCW direction. B, The oblique head and stimulus inclination alters the head pitch angle (head pitch of 0°) at which the velocity of OKAN II was maximal. These velocities were fitted with a second-order polynomial for head pitch of +35°, OKS of +35° (filled circles, solid line) and head pitch of 0°, OKS of 0° (open circles, dashed line). C, The data illustrated in A are plotted over a more restricted range and fitted with linear regression lines. Data obtained after head pitch of +35°, OKS of +35° stimulation are represented as filled squares and fitted with a solid line, and data after head pitch of 0°, OKS of 0° stimulation as open squares and fitted with a dashed line.
DISCUSSION Spatial constancy of OKAN II
We found that, in the rabbit, OKAN II showed spatial constancy, as do the cervico-ocular reflex (Pettorossi et al., 1987
Although the gain of the OKAN II reorientation approaches that observed in the monkey during PRN (Angelaki and Hess, 1994
Another difference between eye movements of the monkey and rabbit may be related to the contribution of the tonic torsional reflex, which has an higher gain in the rabbit (Van der Steen and Collewijn, 1984
The curve of the shift of the OKAN II plane within the orbit had sinusoidal shape over the whole range of pitch angles and was fitted by sine function. This may reflect the responses of the otolithic afferents to a full cycle pitch of the head, as previously determined for both cat (Loe et al., 1973
OKAN II orientation depends on the OKS orientation respace
A second finding of this study concerns the space orientation of the OKAN II rotation axis. In contrast with previous studies showing the rotation axis of OKAN and PRN to be aligned with the gravity vector (Harris, 1987
It has been proposed that nystagmus reorientation reflects characteristics of an internal reference frame for spatial orientation (Dai et al., 1991
Changes in OKAN II slow-phase velocity induced by head pitch
The absolute value of the OKAN II SPEV was also modified systematically by the head pitch, with a longer time constant than that of the nystagmus reorientation. The velocity was usually reduced when the head was tilted and came back when the head was tilted back, but there was a large difference in the velocity rising and falling timing. Decrease in nystagmus velocity may be attributable to an active inhibitory process, whereas the velocity increase may be a result of the inhibition removal and of the slower nystagmus velocity building up.
The change in slow-phase velocity at different head pitch angles resembles the change in velocity of PRN and OKAN I observed previously by others (Waespe et al., 1985
We suggest that the head pitch-induced change in velocity is related to the mismatch between the plane of activated retinal pathway coded in head-centered coordinates and the plane of OKAN II coded in a space-centered frame. In fact, when the OKS is horizontal and the head is pitched up or down, the peak velocity is shifted similarly in upward and downward direction so that maximal velocity occurs when the space-centered and head-centered planes coincided. The velocity dependence on the mismatch between the two planes implies also that the head-centered plane is stored in the CNS. Prolonged optokinetic stimulation induces long-lasting plastic changes along the optokinetic pathway to keep memory of optokinetic stimulus velocity. These "storage sites" include the retina (Liu et al., 1998
It is likely that the structures involved in the comparison between space-centered and head-centered responses include the nodulus and the ventral uvula. In studies on primates, this part of caudal vermis appears to be necessary for both spatial constancy and head tilt-induced velocity attenuation of the nystagmus (Waespe et al., 1985
In conclusion, our results indicate that the plane of OKAN II is coded in space-centered coordinates, and it is influenced by the plane of the OKS respace. The SPEV of OKAN II is also affected by the OKS orientation, and it is maximal when the plane of OKAN II coincides with the plane of the activated retinal pathway, coded in head-centered coordinates.
FOOTNOTES Received May 19, 1998; revised Nov. 30, 1998; accepted Dec. 7, 1998.
This research was supported in part by the Consiglio Nazionale delle Ricerche, the Ministero dell'Universitá e della Ricerca Scientifica e Tecnologica, and the National Eye Institute.
Correspondence should be addressed to Vito Enrico Pettorossi, Istituto di Fisiologia Umana, Universitá di Perugia, Via del Giochetto, I-06100 Perugia, Italy.
REFERENCES
- Angelaki DE, Hess BJM (1994) Inertial representation of angular motion in the vestibular system of Rhesus monkeys. I. Vestibulo-ocular reflex. J Neurophysiol 71:1222-1249
[Abstract/Free Full Text] .- Angelaki DE, Hess BJM (1995) Inertial representation of angular motion in the vestibular system of Rhesus monkeys. II. Otolith-controlled transformation that depends on intact cerebellar Nodulus. J Neurophysiol 73:1729-1751
[Abstract/Free Full Text] .- Angelaki DE, Hess BJM, Suzuki J (1995) Differential processing of semicircular canal signals in the vestibulo-ocular reflex. J Neurosci 15:7201-7216[Abstract].
- Barmack NH (1987) The influence of gravity on horizontal and vertical vestibulo-ocular and optokinetic reflexes in the rabbit. Brain Res 424:89-98[Medline].
- Barmack NH, Errico P (1993) Optokinetically evoked expression of corticotropin-releasing factor in inferior olivary neurons of rabbits. J Neurosci 13:4647-4659[Abstract].
- Barmack NH, Nelson BJ (1987) Influence of long-term optokinetic stimulation on eye movements of the rabbit. Brain Res 437:111-120[Web of Science][Medline].
- Brandt T, Dichgans J, Buhele W (1974) Motion habituation: inverted self-motion perception and optokinetic afternystagmus. Exp Brain Res 21:337-352[Web of Science][Medline].
- Buttner UW, Waespe W, Henn V (1976) Duration and direction of optokinetic after-nystagmus as a function of stimulus exposure time in the monkey. Arch Psychiatr Nervenkr 222:281-291[Medline].
- Dai MJ, Raphan T, Cohen B (1991) Spatial orientation of the vestibular system. Dependence of optokinetic after-nystagmus on gravity. J Neurophysiol 66:1422-1439
[Abstract/Free Full Text] .- Errico P, Ferraresi A, Barmack NH, Pettorossi VE (1996) Role of cerebellar uvula-nodulus in the control of head orientation-specific eye velocity in the rabbit. Ann NY Acad Sci 781:614-618[Web of Science][Medline].
- Fernandez C, Goldberg JM, Abend W (1972) Response to static tilts of peripheral neurons innervating otolith organs of the squirrel monkey. J Neurophysiol 35:978-987
[Free Full Text] .- Fetter M, Heimberger J, Black R, Hermann W, Sievering F, Dichgans J (1996a) Otolith-semicircular canal interaction during postrotatory nystagmus in humans. Exp Brain Res 108:463-472[Web of Science][Medline].
- Fetter M, Pfaff G, Heimberger J, Haslwanter T (1996b) 3D optokinetic responses in humans are not influenced by the gravito-inertial force vector. Soc Neurosci Abstr 434:1095.
- Gizzi M, Raphan T, Rudolph S, Cohen B (1994) Orientation of human optokinetic nystagmus to gravity: a model-based approach. Exp Brain Res 99:347-360[Web of Science][Medline].
- Guedry FE (1965) Orientation of the rotation axis relative to gravity: its influence on nystagmus and sense of rotation. Acta Otolaryngol (Stockh) 60:30-48.
- Harris LR (1987) Vestibular and optokinetic eye movements evoked in the cat by rotation about a tilted axis. Exp Brain Res 66:522-532[Web of Science][Medline].
- Haustein W (1989) Considerations on Listing's law and primary position by means of matrix description of eye position control. Biol Cybern 60:411-420[Web of Science][Medline].
- Koenig E, Dichgans J (1981) Aftereffects of vestibular and optokinetic stimulation and their interaction. Ann NY Acad Sci 374:434-445[Medline].
- Leigh RJ, Robinson DA, Zee DS (1981) A hypothetical explanation for periodic alternating nystagmus: instability in the optokinetic vestibular system. Ann NY Acad Sci 374:619-635[Web of Science][Medline].
- Liu H, Qian ZY, Barmack NH (1998) Endogenous diazepam ligand in rabbit retina induced by long-term optokinetic stimulation and detected by differential display. Soc Neurosci Abstr 24:1024.
- Loe PR, Tomko DL, Werner G (1973) The neural signal of angular head position in primary afferent vestibular nerve axons. J Physiol (Lond) 230:29-50.
- Maioli C (1988) Optokinetic nystagmus: modeling the velocity storage mechanism. J Neurosci 8:821-832[Abstract].
- Malcolm R, Melvill-Jones G (1970) A quantitative study of vestibular adaptation in humans. Acta Otolaryngol (Stockh) 70:126-135[Medline].
- Merfeld DM, Young LR, Paige GD, Tomko DL (1993) Three dimensional eye movements of squirrel monkeys following postrotatory tilt. J Vestib Res 3:123-139[Medline].
- Pettorossi VE, Errico P, Ferraresi A, Fedeli R (1987) Vestibular contribution to the orientation of cervico-ocular reflex in rabbit. Brain Res 403:58-65[Medline].
- Pettorossi VE, Errico P, Ferraresi A (1997) Difference in quick phases induced by horizontal and vertical vestibular stimulations: role of the otolithic input. J Vestib Res 7:89-99[Web of Science][Medline].
- Raphan T, Cohen B (1988) Organizational principles of velocity storage in three dimensions. The effect of gravity on cross-coupling of optokinetic after-nystagmus. Ann NY Acad Sci 545:74-92[Medline].
- Savitzky A, Golay MJE (1964) Smoothing and differentiation of data by simplified least square procedure. Anal Chem 36:1627-1639.
- Soodak RE, Simpson JI (1988) The accessory optic system of rabbit. I. Basic visual response properties. J Neurophysiol 60:2037-2054
[Abstract/Free Full Text] .- Van der Steen J, Collewijn H (1984) Ocular stability in the horizontal, frontal and sagittal planes in the rabbit. Exp Brain Res 56:263-274[Web of Science][Medline].
- Waespe W, Henn V (1978) Reciprocal changes in primary and secondary optokinetic after-nystagmus produced by repetitive optokinetic stimulation in the monkey. Arch Psychiatr Nervenkr 225:23-30[Medline].
- Waespe W, Cohen B, Raphan T (1985) Dynamic modification of the vestibulo-ocular reflex by the nodulus and uvula. Science 228:199-202
[Abstract/Free Full Text] .- Wearne S, Raphan T, Cohen B (1997) Contribution of vestibular commissural pathways to spatial orientation of the angular vestibuloocular reflex. J Neurophysiol 78:1193-1197
[Abstract/Free Full Text] .- Wearne S, Raphan T, Cohen B (1998) Control of spatial orientation of the angular vestibuloocular reflex by the nodulus and uvula. J Neurophysiol 79:2690-2715
[Abstract/Free Full Text] .
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