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1Departments of Neurology, 2Ophthalmology, 3Otolaryngology-Head and Neck Surgery, and 4Neuroscience; The Johns Hopkins University School of Medicine, Baltimore, Maryland
Submitted 28 February 2007; accepted in final form 17 May 2007
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ABSTRACT |
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INTRODUCTION |
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Considerable evidence indicates that the 3-D calibration of the RVOR requires an intact cerebellum. First, humans with cerebellar degeneration demonstrate abnormal RVOR axes: the eyes rotate in a direction different from that of the head movement (Walker and Zee 2005
). Second, animals with vestibulocerebellar lesions are impaired in their ability to alter the axis (Schultheis and Robinson 1981) or amplitude (e.g., Blazquez et al. 2003; Lisberger et al. 1984; Nagao and Kitazawa 2003; Robinson 1976; Rambold et al. 2002) of the RVOR.
In the present study, we address another important question regarding the RVOR: does the cerebellum contribute to the relationship of the eye-velocity axis to the position of the eye in the orbit? For some eye movements, such as saccades (Ferman et al. 1987; Tweed and Vilis 1990), pursuit (Ferman et al. 1987; Haslwanter et al. 1991; Tweed et al. 1992), and the interaural translational VOR (TVOR) (Angelaki et al. 2003; Walker et al. 2004a), there is a torsional eye velocity that depends on orbital position, i.e., a tilt of the angular-velocity axis. This behavior is in accord with Listing's Law (LL), which defines the relationship of ocular torsion to the horizontal and vertical positions of the eye during fixation. In contrast, the RVOR demonstrates much less eye-position-dependent torsion; LL is violated (Crawford and Vilis 1991; Misslisch et al. 1994). The fact that the RVOR is more head-fixed (less dependent on eye position) has the theoretical advantage of more nearly stabilizing the entire visual image on the retina when the head is rotating.
Prior studies indicate that mechanical factors, e.g., orbital pulleys, the connective tissue sleeves that determine the pulling directions of the extraocular muscles (Demer et al. 1995), and neural innervation work together to determine the kinematic behavior of different types of eye movements, whether LL is obeyed (Ghasia and Angelaki 2005; Klier et al. 2006; Quaia and Optican 2003) or not (Smith and Crawford 1998). We hypothesized that the cerebellum might play a more specific role in the neural control of the kinematics of the RVOR given its various roles in the long-term calibration of eye movements, including the axis of the RVOR (Walker and Zee 2005). To test this hypothesis, we compared the orbital-position dependency of the RVOR in patients with cerebellar disease and normal subjects. Preliminary data from this study have been previously presented in abstract form (Walker et al. 2004b), and control data from chair rotations for normal subjects were included in a separate report (Tian et al. 2006).
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METHODS |
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We studied nine patients with cerebellar degeneration (ages: 29–79, 6 male) and seven normal subjects (ages: 30–60, 6 male). Most patients had sporadic cerebellar degeneration. Two had a genetically undefined familial ataxia. Seven patients were tested for chair rotations and all nine for head impulses.
Eye-movement recording
Eye movements were measured using the magnetic field search coil method. Each subject wore dual scleral coils in each eye (Skalar,Delft, the Netherlands). A similar custom-made dual coil was attached tightly to a bite bar made of dental impression material that was fit to each subject and was held firmly between the teeth during the experiment. For the chair rotations, the bite bar served to hold the head fixed in the same position relative to the axis of rotation. For head impulses, this coil was used to record three-axis head rotation while the head was free. Raw coil signals were filtered in hardware (90-Hz low-pass Butterworth), digitized (1,000 Hz), and saved on computer for later analysis.
Experimental paradigms
CHAIR ROTATIONS.
The subject sat in a motor-driven vestibular chair with the head upright and held steady by the bite bar. Each trial pair began with fixation of a laser target that was back-projected on a tangent screen (distance: 124 cm) in an otherwise nearly dark room. Target position on the screen was controlled by the computer through a pair of mirror galvanometers. The target was centered horizontally and was at one of three vertical positions: 0° (straight-ahead), 15° up, or 15° down. The chair accelerated (
200°/s2) randomly to the left or right to a plateau velocity of 40°/s. The rotation was continued for an additional 300 ms and then decelerated until it stopped. The total amplitude of each rotation was 20°. After the chair stopped, the target was moved in the direction of prior chair motion to re-center the eyes in the orbits horizontally, and a second trial brought the chair back to the center position. Approximately 10 trial pairs were performed for each initial rotation direction and each vertical eye position. For approximately half of the trials (randomly determined), the target was extinguished when the chair started to move and the rotation continued in darkness. For the other trials, the target remained on throughout the trial. Neither the presence nor absence of the target nor the predictability of the direction of rotation affected the kinematics of the response. Therefore all trials in the same direction and with the same vertical eye position were combined in the analysis.
HEAD IMPULSES.
Yaw head impulses were performed by one of the authors (M. Walker) while standing behind the subject. The subject's head was free to move, and the head coil was held firmly in the mouth by its attached bite bar. At the beginning of each trial, the head was centered in the fields by the examiner, using an on-line feedback monitor that displayed the instantaneous three-axis position of the head. The subject was instructed to look at an LED target that was 124 cm away and at one of the three vertical positions. The head was then rotated about the yaw axis randomly to the right or left (peak acceleration: 4,000–5,000°/s2, peak velocity: 150–200°/s) while the subject maintained fixation of the target, which remained illuminated. The feedback monitor was also used to detect and minimize roll and pitch components of the rotations.
Data analysis
The data were analyzed using custom programs developed in MATLAB (The Mathworks, Natick, MA). Raw coil data were converted to rotation vectors and to 3-D angular velocity vectors (Hepp 1990). Both head and eye velocities were determined in head-fixed coordinates (Walker and Zee 2005). An interactive program was used to select trials for analysis. For head impulses, trials containing quick phases, saccades, or blinks were excluded. For chair rotations, quick phases occurring during the rotation were marked, and those segments were excluded from the analysis. If a saccade occurred within the first 100 ms of the trial, the trial was excluded completely.
We grouped trials by the direction of rotation and the vertical position of the eyes. For chair rotations, we aligned the trials by determining the onset of chair motion using a velocity threshold (0.5°/s). The onset of head impulses was defined as the time at which the horizontal component of angular head velocity exceeded 5°/s.
For each data point, we determined the angular velocity axis for each eye in the sagittal (torsional-horizontal) plane. The instantaneous tilt angle was calculated as the arctangent of the ratio of the torsional to the horizontal component of eye velocity. A least-squares linear regression of this tilt angle to the instantaneous vertical position of the eye in the orbit yielded the tilt angle slope, which is a measure of the variation of the eye velocity axis with vertical eye position. To perform the regressions, data were separated into bins of 10-ms width, starting 50 ms from the onset of the trial and continuing for an additional 350 ms.
Rotation vectors can be expressed in a coordinate system that is aligned with the Listing primary position, i.e., in "Listing coordinates," when calculating the tilt angle slope. To do this, an accurate measurement of Listing's primary position is required. In some human subjects, however, it is difficult to determine primary positions precisely, due to the possibility of static torsional slip of the eye coils (Bergamin et al. 2004). In other experiments in our laboratory, we have addressed this problem using fixation paradigms in which frequent reference positions are taken (e.g., Steffen et al. 2000). Time constraints did not allow us to do this in the present study. Nonetheless, to investigate the possibility that not calculating the tilt angle slope in Listing's coordinates influenced our results, we calculated primary positions using the best available data (a square fixation paradigm with 20° target positions but without repeated reference positions throughout the collection period). The effect on the tilt angle slope and the difference between groups was negligible. Thus we left our data in standard head-fixed coordinates for the calculation of the tilt angle slope.
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RESULTS |
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Figure 1 shows responses of a representative normal subject and patient during head-fixed chair rotations. In the initial portion of the response, the response was close to head-fixed (there was very little torsion, regardless of vertical eye position). As the rotation proceeded, however, a torsional eye velocity appeared that was dependent on the vertical position: it was least for down gaze and greatest for up gaze. A similar behavior was seen in the patient, but the torsional velocities were larger.
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10°/s, the traces began to diverge (eye-position-dependent torsion and tilt angle slope started to increase). There was also an upward vertical component (upward velocities are negative) to the response, but this did not change with vertical eye position (right). Right eye data are shown, as our prior study (Walker and Zee 2005) showed that vertical eye velocities during yaw are greater in the abducting eye.
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), we determined the tilt angle slope as a function of time by aligning the trials at their onsets and dividing the data points into bins of 10-ms width. All data in each bin were subjected to a least-squares linear regression of tilt angle to vertical eye position. Representative results for a single interval (270–280 ms) are shown in Fig. 3 A. The slopes of these regressions are the tilt angle slopes. Note that the slope for the patient (0.63) is much greaterthan that of the normal subject (0.24). This difference was true for the groups as a whole (Fig. 3B).
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0.3, near the time when the chair velocity reached steady state. Patients also began with a relatively low tilt angle slope. However, it increased more rapidly with time and reached a higher maximum (0.5). Figure 4B shows that the difference in slopes between the two groups was highly significant throughout most of the response.
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Representative responses to yaw head impulses are shown in Fig. 5 for one normal subject and one patient. For both subjects, the axis of eye velocity varied as a function of the vertical position of the eyes in the orbits. When the eyes were looking up, the head and eye velocities were most closely aligned. When the eyes were looking down, there was a greater torsional eye velocity (the axis shifted downward), even though the axis of head velocity did not change. As for the head-fixed chair rotations, this shift of the eye velocity axis was much larger in the patient than in the normal subject.
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DISCUSSION |
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Two additional, and potentially related, aspects of eye-velocity kinematics did not require an intact cerebellum. First, in our cerebellar patients, as we have shown for normal subjects (Tian et al. 2006), the axis of eye velocity evolved over time during rotation of the head. Remarkably, at the onset of head rotation, eye velocity was nearly head-fixed, i.e., there was little eye-position-dependent torsion. Second, consistent with the combined results from prior studies (Misslisch and Tweed 2001; Palla et al. 1999; Thurtell et al. 1999; Tian et al. 2006; Walker et al. 2004a), the dynamics of the stimulus affected the kinematics of eye motion. In both patients and normal subjects, responses to head impulses were more head-fixed than responses to lower-acceleration chair rotations. We will discuss all these results in light of prior work regarding the kinematics of the RVOR, the possible relationship to LL, and the cerebellar contribution to control of the axis of eye rotation during head rotation.
Torsion, the RVOR, and LL
Misslisch et al. (1994) showed that the axis of the RVOR, in humans, depends on orbital position, but it does not obey LL. For low-frequency stimuli, the eye-velocity axis tilts 25% of the orthogonal gaze angle; this is half of what LL predicts (Tweed and Vilis 1987). Misslich et al. (1994) suggested that this represents a compromise between LL and the head-fixed axis of an ideal RVOR. Subsequent studies have suggested that many other variables, such as the frequency and/or acceleration of the stimulus, species, and the visual environment during head rotation, can influence the eye-velocity axis (e.g., Misslisch and Hess 2000; Palla et al. 1999; Thurtell et al. 1999; Tian et al. 2006; Walker et al. 2004a).
Here we focused on the temporal dependence of RVOR kinematics (Tian et al. 2006). Using transient stimuli, the RVOR axis evolved over time: the early response (from the point at which it could be reliably measured, 50 ms from the onset of chair rotation) is nearly head-fixed; thereafter eye-position-dependent torsion increases with time, reaching a plateau at about the time that steady-state head velocity is reached. Temporal dependence of RVOR kinematics was reported by Thurtell et al. (1999) but not by Crane et al. (2006).
The results of our studies and those of Thurtell et al. (1999) support the hypothesis that the early RVOR is close to head-fixed, i.e., the response axis is not modulated by orbital position. We show here that this property of the initial RVOR does not require an intact cerebellum, suggesting that it is mediated by elementary RVOR pathways within the brain stem.
Origin of eye-position-dependent torsion
What implications do our findings in the RVOR have for an understanding of the control of ocular torsion by the brain? Over the last two decades, a general consensus has emerged that ocular kinematics are determined by a combination of neural innervation and the mechanical constraints of the orbital pulleys, the connective tissue sleeves that determine the pulling directions on the globe of the extraocular muscles (Angelaki 2003; Angelaki and Hess 2004; Crawford et al. 2003; Demer 2006; Demer et al. 1995; Klier et al. 2003, 2006; Misslisch and Hess 2000; Misslisch and Tweed 2001; Quaia and Optican 2003; Smith and Crawford 1998). Important questions remain, however, regarding the interaction between 3-D neural signals and orbital mechanics, including which brain areas are important for the calibration of the neural component. Our data here in cerebellar patients do not address directly the mechanisms responsible for LL as the RVOR does not follow LL. They do, however, provide new and important information regarding the neural control of RVOR kinematics, and they show that the cerebellum plays a critical role in this process, particularly just after the initial response to head rotation (see also: Cerebellum and the axis of eye rotation during the RVOR).
The RVOR, unlike saccades and pursuit, is inherently 3-D (Tweed 1997). Semicircular canal afferents carry signals that encode 3-D angular head velocity. This alone, however, would not necessarily be sufficient to generate a head-fixed eye velocity. A recent study found that eye movements generated by direct abducens nerve stimulation follow the "half-angle rule," i.e., they obey LL (Klier et al. 2006). This suggests that the ocular pulleys confer a default orbital-position dependence to the pulling directions of the eye muscles and hence an eye-position-dependent torsion. To compensate for this imposed eye-position-dependent torsion, the RVOR would need to incorporate eye-position information itself into the eye muscle innervations. An innervation that was eye-position invariant, even though 3-D, would not suffice.
An important question then is how such eye-position compensation might be achieved by the RVOR. Originally it was suggested that the pulleys might move posteriorly in the orbit during head rotation (Demer et al. 2000; Thurtell et al. 1999, 2000), but this was shown unlikely to be feasible and at odds with other experimental data (Angelaki 2003; Crane et al. 2005; Misslisch and Tweed 2001). Alternatively, there might be a neurally generated torsional signal, dependent on eye position, that is sent to the cyclovertical eye muscles to counteract the effects of pulleys. Such a signal, however, has not been found on primary motor neurons during eye movements (Ghasia and Angelaki 2005). It is conceivable, however, that the eye-position dependence of the 3-D neural signal might not be readily seen in the responses of individual neurons (Smith and Crawford 2005). Clearly more information is needed to resolve the seeming discrepancies between neural recordings and the measured 3-D kinematics of eye movements during head rotation.
Cerebellum and the axis of eye rotation during the RVOR
A role for the cerebellum and its brain stem connections in the control of eye-position-dependent torsion (e.g., in the case of fixation, LL) is supported by several prior studies. The caudal nucleus reticularis tegmenti pontis (cNRTP), which projects to the cerebellum, is necessary for the correction of torsional errors that occur during saccades (Van Opstal et al. 1996). Moreover, spontaneous nystagmus in cerebellar disease violates LL (Glasauer et al. 2003; Straumann et al. 2000).
Our data indicate that the cerebellum also has a large effect on eye-position-dependent torsion in the RVOR, not on the initial eye-velocity axis but rather on its evolution over time. How might this happen? One possibility is that, similar to the role of the cNRTP for saccades, the brain monitors changes in torsional orientation of the eyes during the RVOR and imposes eye-position-dependent torsion to prevent the eyes from drifting too far from Listing's plane. The function of the cerebellum might then be to modulate this effect to achieve the compromise between the competing goals of keeping eye positions in LP (half-angle rule) and maintaining retinal stability of the visual image (head-fixed axis) (Misslisch et al. 1994). Without the cerebellum, there is no such compromise. Alternatively, the evolution of kinematics could reflect the activity of the velocity-to-position ocular motor neural integrator (Crawford 1994; Glasauer et al. 2003). Indeed the cerebellum and the flocculus and paraflocculus in particular play a key role in the function of the ocular motor integrator (Zee et al. 1981).
In conclusion, in spite of the uncertainty of neural mechanisms, our findings here strongly support the idea that the cerebellum is directly involved in the 3-D control of the RVOR in response to abrupt head rotations. Except perhaps for the very early portion of the response—the initial 50 ms or so, when the axis of eye rotation is close to head-fixed –the cerebellum controls the relationship of eye-velocity axis to the position of the eye in the orbit. This behavior complements the previously shown roles of the cerebellum in processing canal inputs to determine the 3-D axis of head rotation (Walker and Zee 2005) and controlling the axis of the RVOR in response to sustained, lower-frequency rotational stimuli (Angelaki and Hess 1995; Walker and Zee 1999; Wearne et al. 1998).
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GRANTS |
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ACKNOWLEDGMENTS |
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FOOTNOTES |
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Address for reprint requests and other correspondence: M. F. Walker, Dept. of Neurology, The Johns Hopkins University, 600 N. Wolfe St., Path 2-210, Baltimore, MD 21287 (E-mail: mwalker{at}dizzy.med.jhu.edu)
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ABSTRACT
INTRODUCTION
