INTRODUCTION

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The angular vestibuloocular reflex (aVOR) stabilizes gaze by generating counter-rotation of the eyes in the orbit when the head is rotated in darkness. For precise visual fixation, the gain of the aVOR must be modified so that retinal slip, the difference between surround and eye velocity, is minimal. Retinal slip is critical for producing aVOR gain modification (Gonshor and Melvill Jones 1971; Miles and Fuller 1974), but other factors may also be important. Rotation in darkness with attention to an imagined head-fixed target can cause adaptive reduction in aVOR gains (Melvill Jones et al. 1984). Additionally, vestibular and visual stimuli in disparate planes can spatially adapt the aVOR so that the eyes move obliquely in darkness in response to pure horizontal or vertical stimuli (cross-axis adaptation) (Baker et al. 1986, 1987a,b; Harrison et al. 1986; Schultheis and Robinson 1981). Head position may also influence aVOR gain adaptation. The magnitude of the shift in the plane of the eye movements was greater during cross axis adaptation when it was tested in the head orientation in which the adaptation was induced (Baker et al. 1987a,b). A similar effect of head tilt on the gain of the horizontal aVOR has also been noted (Tan et al. 1992; Tiliket et al. 1993). Thus the direction of gravity relative to the head may be an important context for establishing the axes about which adaptation is expressed. The purpose of this study was to determine whether the position of the head relative to gravity, in which the aVOR gain was adapted, is an important context for maintaining the gain.

	METHODS

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Horizontal, vertical, and roll aVOR gains (eye velocity/head velocity) were tested in three cynomolgus monkeys (Macaca fascicularis) before and after adaptation. The experiments conformed to the Guide for the Care and Use of Laboratory Animals (National Research Council 1996) and were approved by the Institutional Animal Care and Use Committee. Monkeys sat with head fixed in a primate chair in a multi-axis vestibular stimulator (Yakushin et al. 1995, 1998, 2000). Animals were implanted with search coils (Robinson 1963) that measured eye movements in three dimensions. An optokinetic cylinder, 86 cm in diameter with vertical alternating 10° black and white stripes, surrounded the animal. Data were digitized at 600 Hz. To increase aVOR gain, animals were rotated with steps of velocity around an interaural axis with counter-phase drum rotation (Fig. 1A). Consequently the monkeys observed a visual surround that moved with a velocity of twice the head velocity (30 + 30°/s). Gain was decreased by in-phase rotation of the drum with animal rotation at 60°/s (Fig. 1B). The primate chair and optokinetic cylinder were mechanically coupled for the in-phase rotations.

View larger version (47K): [in this window] [in a new window]   Fig. 1. A: adaptation paradigm to increase the gain of the vertical angular vestibuloocular reflex (aVOR). Out-of-phase rotation of the animal and visual surround at the same velocity (30°/s) induced slow phases of eye velocity of 60°/s. B: adaptation paradigm to decrease the gain of the vertical aVOR. When animal was rotated together with the visual surrounding (60°/s), then the evoked aVOR was suppressed. C: stick figures showing the head orientations in which vertical aVOR gain was adapted. D-I: step responses of the aVOR when the animal was adapted upright (D and G), left side down (E and H), and right side down (F and I). Eye velocities induced by rotation before adaptation are shown in blue and after adaptation, in red. The stimulus velocity is shown in black. The direction of the stimulus was reversed to facilitate comparison. Increases in eye velocities were symmetrical after adaptation in the upright position (D and G). When the animal was adapted on side, increases in eye velocity were significant when the animal was tested with the same side down (E and I). There were no increases in eye velocity when the contralateral side was down (H and F).

Adaptation was induced by rotating the animals for 4 h in upright, left-side-down (LSD) or right-side-down (RSD) head positions (Fig. 1C). Gains of the aVOR were tested by rotation around a spatial vertical (interaural) axis with steps of velocity of 60°/s in darkness for 5 s in side-down positions. Rotation directions were alternated. After upward and downward rotation ten times in one side-down position, the head orientation was changed to the opposite side-down position and the test was repeated. Accelerations and decelerations during rotation were 300°/s². The system was underdamped to achieve these high accelerations. As a result, there was low-amplitude ringing at 10 Hz that decreased to zero over the first second after reaching peak velocity (Fig. 1, D-I). This 10-Hz ringing was reflected in eye velocities produced by the aVOR. The average head and eye velocities over the oscillation period were determined by fitting straight lines through the oscillations of the individual signals for 500 ms after acceleration reached a maximum. Gain was determined by computing the ratio (eye velocity)/(head velocity). It was presumed that activation of the semicircular canals was the same for LSD and RSD positions, but static activation of the otoliths and other tilt sensors depended on the tilt direction. Gain values obtained in a particular head orientation before and after adaptation were compared (t-test). During vertical aVOR gain adaptation, significant changes (P < 0.05) were observed only for vertical components of the aVOR, not for horizontal and roll components; the latter will not be considered further.

	RESULTS

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Before adaptation, pitch forward about a vertical interaural axis in the LSD (Fig. 1, D-F) or RSD (Fig. 1, G-I) positions, induced upward eye velocities that were close to stimulus velocities of 60°/s (Fig. 1, D-I, blue traces). After the aVOR gain had been increased with the animal in the upright position, eye velocities were changed symmetrically when the animal was tested LSD and RSD (red traces; Fig. 1, D and G). In contrast, when the aVOR gain was increased with the animal rotating in the LSD position, the gain increase was significant only when tested with the animal LSD (Fig. 1E), and there was no gain change in the RSD orientation (Fig. 1H). Similarly, when adapted in the RSD position, the gain was unchanged when the animal was LSD (Fig. 1F) but was significantly increased when the animal was RSD (Fig. 1I).

Gain increases and decreases were similar for upward and downward eye velocity in all three animals (Table 1 and Fig. 2), regardless of up-down gain asymmetries. Averaged gains before and after adaptation from the monkey shown in Fig. 1 (M98060), after it had been adapted in the upright position, were the same in the LSD and RSD positions (Fig. 2A). When gain was increased on the side position, however, changes were significant only when the animal was tested on the side in which the gain was adapted (LSD, Fig. 2B; RSD, Fig. 2C). Findings were similar when the gain was decreased during adaptation in upright (Fig. 2D) and on side positions (Fig. 2, E and F). There was a small decrease of the aVOR gain when the animal was tested contralateral side down (RSD, Fig. 2E; LSD, Fig. 2F).

View larger version (37K): [in this window] [in a new window]   Fig. 2. Vertical aVOR gain increase (A-C) and decrease (D-E) of M98060 following adaptation in upright (A and D), LSD (B and E), and RSD (C and F). See text for details. G-J: average changes in vertical aVOR gains across all tested animals. When the animals were adapted in upright position, gain changes were symmetrically increased (G) or decreased (I) when tested with the animals on either side. When the aVOR gains were adapted in an on-side position, increases (H) and decreases (J) were larger when the animals were tested with the ipsilateral side down.

Data for three animals were consistent with those from M98060 (Fig. 2, G-J). Increasing gain in the upright position caused symmetrical gain changes in the LSD and RSD positions (22 ± 10 and 21 ± 10%, respectively; P = 0.40, Fig. 2G). When the gain was increased in one on-side position, however, the increase with the ipsilateral side down was 42 ± 17%, compared with an increase with the contralateral side down of only 3 ± 5% (P = 3*10⁸, Fig. 2H). Similarly after gain decreases, gain changes were symmetrical after upright adaptation, at 24 ± 4 and 23 ± 2% for the LSD and RSD positions, respectively (P = 0.32, Fig. 2I). After aVOR gains were decreased in a side-down position, however, gain decreases were larger when that side was down, and there were smaller decreases in gain when the animals were tested with the contralateral side down (43 ± 16 and 15 ± 6%, P = 1*10⁵, respectively; Fig. 2J). Combining the results of gain increases and decreases, changes were 23 ± 7% in both side-down positions after adaptation while upright. In contrast, gain changes were 43 ± 16% with the ipsilateral side down and only 9 ± 8% with the contralateral side down after gain modification in an on-side position. Despite individual variation in absolute values among animals (Tables 1 and 2), the context specific differences in gains as a function of head position were present in every monkey in each experiment. It should be noted that the standard deviation about the modified gain value was the same as for the unmodified gain (0.044 vs. 0.046, P = 0.51). This implies that the modified gain was achieved as soon as the animal was placed in that head position and was maintained throughout the sequence of testing.

	DISCUSSION

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These findings show that the state of the vertical aVOR gain is dependent on the orientation of the head with regard to gravity in which it was adapted. Gain changes with the head oriented in the position in which it was adapted were always significantly greater than with the head in opposite orientation. When adaptation was performed with animals' upright, the gain changes were symmetrical when tested in either side down position. Since the same semicircular canals were activated in each head position in our study, adaptation in different canal planes could not have contributed to the results.

There are other contexts that affect the gain of the aVOR, such as eye position (Shelhamer et al. 1992; Tiliket et al. 1994) and imagined targets (Barr et al. 1976). Gain changes in the first condition is likely to occur in the velocity-to-position integrator where activity related to eye position is generated. In contrast, a likely place for the head position effect on gain adaptation is to take place is in the central vestibular system on neurons with otolith-canal convergence (Sato et al. 2000; Uchino et al. 2000; Yakushin et al. 1999; Zakir et al. 2000). Somatosensory inputs that sense tilt (Yates et al. 2000) could also contribute to the phenomenon. Regardless of the implementation, the finding that the altered gains were present on assuming a side-down position has significant implications for understanding motor performance in a terrestrial environment and in microgravity.