 |
INTRODUCTION |
The vestibuloocular reflex (VOR) functions to maintain visual acuity during head movements. By generating compensatory eye movements, which are ideally equivalent in velocity but opposite to the spatial direction of a head movement, the VOR minimizes retinal image slip and thereby stabilizes visual images on the retina. An important characteristic of the VOR is that it operates in an "open loop" fashion, i.e., the elicited eye movements are not sensed by the labyrinthine receptors that generate them. Therefore, there must exist other mechanisms that control and adjust VOR gain to optimize gaze stabilization. Errors in VOR calibration result in retinal image slip, which activates adaptive mechanisms to modify central VOR circuits.
Adaptation of VOR response gain has been demonstrated in several species including man (Berthoz et al. 1981
; Demer et al. 1989
; Gauthier and Robinson 1975
; Gonshor and Melvill Jones 1976a
,b
; Paige and Sargent 1991
), monkeys (Bello et al. 1991
; Miles and Eighmy 1980
; Miles and Fuller 1974
), cats (Godaux et al. 1983
; Keller and Precht 1979
; Melvill Jones and Davies 1976
; Robinson 1976
; Snyder and King 1988
), rabbits (Collewijn and Grootendorst 1979
; Ito et al. 1974
), rats (Tempia et al. 1991
), and fish (Pastor et al. 1992
; Schairer and Bennett 1981
). Most of these studies have investigated horizontal VOR gain adaptation after exposure to enhanced, reduced, or direction-reversed visual surround motion produced either by optical devices or by coupling altered visual surround motion with head movement. In each case, the gain of the VOR was modified (increased or decreased) in such a way as to reduce or eliminate retinal image slip during head movements.
Not only must the speed of the compensatory eye movement be correct, but also the axis of eye rotation must be aligned with that of the head movement to keep the line of sight stationary in space. Human studies investigating adaptive responses after exposure to an optically induced tilt have revealed changes in both spatial orientation perception (Ebenholtz 1966
; Mack and Rock 1968
; Mikaelian and Held 1964
; Morant and Beller 1965
) and eye movement direction (Callan and Ebenholtz 1982
). Changes in the direction of the VOR recorded in the dark (using electrooculography) have also been observed in cats after exposure to combined vestibular and optokinetic stimulation about orthogonal axes (Baker et al. 1986
, 1987
; Harrison et al. 1986
; Schultheis and Robinson 1981
). Recently, Fukushima et al. (1996)
demonstrated cross-axis adaptation using orthogonal pursuit rather than full-field optokinetic stimuli. All these studies have concentrated on vertical and horizontal eye movements using adaptation protocols at a single stimulus frequency.
The present study was aimed at providing a thorough quantitative description of the three-dimensional properties of the primate VOR after 2 h of exposure to spatially orthogonal visual and vestibular environments. Thus rotation of the head, as transduced by the vestibular system, was along one direction (e.g., the pitch plane), while rotation of the visual surround was along a noncomplementary orthogonal direction (e.g., the horizontal plane). Four different spatial combinations of the visual/vestibular stimuli (torsional VOR + vertical OKN, torsional VOR + horizontal OKN, vertical VOR + horizontal OKN, and horizontal VOR + vertical OKN) at two different frequencies were applied to evaluate the spatiotemporal properties of the adapted VOR.
Most natural head movements, particularly those including pitch and roll components, involve dynamic changes in the orientation relative to gravity. In addition to the semicircular canals, these head movements also activate the otolith system. Even though there is little or no contribution to VOR gain during angular head movements at frequencies >0.05 Hz in intact rhesus monkeys (Angelaki and Hess 1996b
), dynamic activation of the otolith-ocular system could still alter adapted VOR responses. In fact, the response characteristics of both the orienting (i.e., head position-dependent otolith-ocular responses such as those described as counterrolling or counterpitching during roll or pitch tilts, respectively) and inertial (i.e., head velocity-dependent otolith-ocular responses associated with activation of velocity storage) systems are spatially and temporally appropriate tosupplement semicircular canal VORs and to contribute to adapted responses. An additional goal of this study was to examine the otolith contribution to the adapted VOR in both intact and canal-plugged animals by applying head movements about earth-horizontal axes during the adapting stimulus sequences.
 |
METHODS |
Animal preparation and eye movement recording
Seven rhesus monkeys were chronically prepared with skull bolts to restrain the head during experiments and implanted with a dual search coil for three-dimensional eye movement recordings using the magnetic search coil technique. Of these, five animals were used for control responses. In addition, data were also collected from five animals after selective semicircular canals were inactivated by plugging. The lateral canals were plugged in two (LC) animals, the right anterior/left posterior canals were plugged in another two (RALP) animals, and all canals were plugged in the fifth animal. Details for these procedures have been described previously (Angelaki and Hess 1994
-1996a
-c
; Angelaki et al. 1996a
). The efficacy of canal-plugging has been histologically verified (e.g., see Fig. 1 in Angelaki et al. 1996a
). All surgeries were performed under intubation anesthesia, and animal treatment and handling was in accordance with the National Institutes of Health guidelines.

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| FIG. 1.
Adaptation protocol using pitch head oscillations phase-locked to horizontal oscillations of the visual surround. A: schematic diagram of stimulus conditions during adaptation. B: eye movement responses during pitch head oscillations at 0.5 Hz (±18°) in complete darkness before (left) and after (right) 2 h of adaptation to simultaneous oscillations of the head in the pitch plane and of the visual surround (optokinetic drum) in the earth-horizontal plane. Horizontal, vertical, and torsional eye position: Ehor, Ever, Etor; Horizontal, vertical, and torsional eye velocity (fast phases removed): hor, ver, tor); head stimulus velocity: stm.
|
|
The search coil consisted of a dual coil assembly with two serially interconnected miniature coils that were attached at diagonal points along the circumference of a large conventional three-turn coil (Hess 1990
). Calibration of the search coil signals was performed in two stages, one before implantation and the second daily before each experimental protocol by requiring the monkeys to fixate three light-emitting diodes (LEDs) separated by 20° along a parasagittal plane through the respective eye (Hess et al. 1992
; see also Angelaki and Hess 1996a
,b
).
The voltage signals of the coil assembly, as well as position and velocity signals of the turntable were digitized at a rate of 833 Hz (Cambridge Electronics Device 1401) and stored on the hard disk of a PC for off-line analyses. Three-dimensional eye positions were expressed in head-centered Cartesian coordinates as rotation vectors E (using straight ahead as reference position) (Haustein 1989
). The eye angular velocity vector,
, was computed from the eye position vector, E, according to the equation
= 2(dE/dt + E × dE/dt)/(1 + |E|2) (Hepp 1990
). Eye position and angular velocity vectors were expressed relative to a right-handed, head-fixed coordinate system as defined by the orientation of the magnetic fields relative to the animal in the standard 15° nose-down position. For the majority of experimental protocols, eye position and velocity were decomposed into horizontal, vertical, and torsional components. Thus a vertical eye position (velocity) was the component of the eye position vector E (angular velocity vector
) along the interaural axis, whereas torsional and horizontal eye positions (velocities) were the respective vector components along the nasooccipital and vertical head axes (which were rotated relative to the stereotaxic coordinates in the pitch plane through an angle of 15° nose-up). Positive directions were defined as clockwise (i.e., rotation of the upper pole of the eye toward the right ear), downward, and leftward, respectively (see sketches of monkey heads in Fig. 1). In selected experiments (for example, in RALP VOR + horizontal OKN adaptation experiments performed in animals with the right anterior/left posterior canals inactivated), eye velocity was decomposed into horizontal, right-anterior/left posterior, and left anterior/right posterior canal components (
hor,
ralp, and
larp) obtained by rotating the horizontal, vertical, and torsional components (
hor,
ver, and
tor) through 45° about the yaw axis.
Experimental setup
For experiments, the monkeys were seated in a primate chair with their heads restrained in a position such that the horizontal stereotaxic plane was tilted 15° nose-down. In this head position, the vertical semicircular canals were approximately perpendicular and the lateral semicircular canals approximately parallel to the earth-horizontal plane. The monkeys were placed in a primate chair that was secured inside a motorized three-dimensional turntable that could deliver both earth-vertical and -horizontal axis rotations about the yaw, pitch, and roll axes. The turntable was surrounded completely by a light-tight sphere (80 cm radius) covered with a random dot pattern such that eye movements could be studied in complete darkness (when the lights inside the sphere were off). This sphere also could be oscillated independently such that horizontal or vertical (but not torsional) optokinetic optic flow could be generated (with the lights inside the sphere on).
Due to the gimbaled structure of the three-dimensional turntable and optokinetic sphere, animals were rotated inside the optokinetic sphere the movement of which always was fixed relative to space (i.e., either space-vertical or space-horizontal), independently of the instantaneous position of the animal during head oscillation. As a result, the optic flow components experienced by the animals during adaptation were not purely horizontal or purely vertical but rather consisted of a more complex optic flow pattern, which can be described as follows: consider the situation of pitch head oscillations (about an earth-horizontal axis) in the presence of horizontal optokinetic stimulation (Fig. 1A, about an earth-vertical axis). Let us also assume that the optokinetic stimulus velocity is described by the equation:
okn(t) = A
sin
t. Similarly, the vestibular stimulus velocity is described by the equation:
vest(t) = d
/dt = d(
B cos
t)/dt = B
sin
t, where
(t) =
B cos
t describes head position as a function of time,
= 2
f is the angular frequency, A is peak drum displacement, and B is peak head displacement.
In the moving, head-fixed coordinate system of the animal, the experienced optic flow pattern exhibits two velocity components: one in the yaw plane (rotation about the z axis) and the second in the roll plane [rotation about the x (torsional) axis], as follows
|
(1a)
|
|
(1b)
|
For small angles B, Eq. 1, a and b, can be approximated by
|
(2a)
|
|
(2b)
|
Equation 2, a and b, suggests that the optic flow experienced by the animals during adaptation has two components, both along axes orthogonal to the vestibular stimulus (which in this example is along the y axis). The largest optic flow component is at the fundamental frequency along the described optokinetic stimulus axis, i.e., horizontal for hOKN condition (Eq. 2b). The second optic flow component is at double the frequency of the imposed vestibular and optokinetic stimuli and occurs along the third spatial axis, i.e., torsional for the vVOR + hOKN condition. For 0.5 Hz, ±18°, the second harmonic optic flow component was only 15.7% of the fundamental. For 0.05 Hz, ±60°, the second harmonic optic flow component was 52% of the fundamental.
Adapting procedures and test protocols
Before experimental sessions, animals were given a small dose of d-amphetamine (1.5 mg orally) to maintain a constant level of alertness. Monkeys were subjected to 2 h of simultaneous vestibular and optokinetic oscillations at each of two frequencies: 0.5 Hz (±18° for both vestibular and optokinetic stimuli) or 0.05 Hz (±60° for vestibular and ± 180° for optokinetic stimuli). In two animals, all possible combinations of vestibular and optokinetic stimuli were tested. That is, a total of four combinations were delivered, i.e., horizontal vestibular coupled to vertical optokinetic stimulation (hVOR + vOKN); vertical vestibular coupled to horizontal optokinetic stimulation (vVOR + hOKN); torsional vestibular stimulation coupled to horizontal optokinetic stimulation (tVOR + hOKN); and torsional vestibular stimulation coupled to vertical optokinetic stimulation (tVOR + vOKN) at two different frequencies (0.5 and 0.05 Hz). For each combination and frequency, two separate adapting protocols were applied: one with the axis of rotation oriented earth-vertical (such that dynamic otolith stimulation was minimal to test the properties of semicircular canal adaptation) and the other with the axis of rotation oriented earth-horizontal (such that the adaptive effects of activating both the semicircular canal and otolith systems could be tested). Therefore, a total of 16 adaptation protocols were tested in each of the two intact animals that were adapted under all conditions. In the remaining animals, selected adapting protocols were delivered such that a total of two to five intact animals were tested for each of the 16 stimulus combinations. In the LC and RALP canal-plugged animals, several adaptation protocols were employed whereby the missing canal plane coincided with the head movement plane or the optokinetic stimulus plane or it was orthogonal to both. Due to the large data volume and because no difference was observed with other adapting stimulus sequences, the canal-plugging data presented here will only focus on the adapting protocols where head movement occurred in the plane of the plugged canals. That is, in LC-plugged animals, only the hVOR + vOKN adapting condition will be described. In the RALP-plugged animals, a slightly altered adapting condition was used: ralp VOR + hOKN, whereby the head oscillated in the RALP (half-way between pitch and roll) planes. The fifth animal with all canals plugged was only tested with OVAR (but not EVA) adaptation protocols.
During adaptation, and approximately every 15 min during each adapting session, the lights were turned off, animals were given a period of rest for ~1 min, and the VOR in the dark was tested at the adapting frequency, amplitude, and axis orientation (i.e., earth-vertical for EVA or earth-horizontal for OVAR adaptation protocols) to monitor the time course of adaptation. After completion of the 2 h of adaptation, the VOR was tested in the dark using sinusoidal oscillations at 0.01 (±900°), 0.02 (±450°), 0.05 (±90° and ± 180°), 0.1 (±90°), 0.2 (±45°), 0.5 (±18°), and 1 Hz (±5°). For each EVA and OVAR adapting condition, the VOR was tested with the axis of rotation both earth-vertical and -horizontal. Because the changes in VOR observed with adapting protocols where the axis of rotation was earth-horizontal also reflected the adaptive states of the otolith signals, these protocols were optimized to address specifically the role of otolith system changes in the adapted VOR. Thus in addition to the main protocol described above, the VOR after 0.05 Hz OVAR adaptation was also studied in selected animals with the following stimuli: sinusoidal oscillations where peak amplitude was kept constant at 60° while frequency varied and sinusoidal oscillations at the adapting frequency with different peak amplitudes (10, 20, 30, 60, 90, and 180°).
As explained in more detail elsewhere (Angelaki and Hess 1996b
), two different otolith-ocular reflexes are activated during earth-horizontal axis oscillations: responses phase-locked to head velocity that arise from activation of the inertial (velocity storage) system and responses phase-locked to head position relative to gravity (translational and orienting responses; the former are primarily horizontal, whereas the latter are torsional and vertical eye movements traditionally described as counterrolling and counterpitching). With peak-to-peak oscillation amplitudes less than a whole revolution, the head position- and head velocity-dependent responses are indistinguishable. With peak-to-peak oscillation amplitudes that exceed a whole revolution in space, however, the two waveforms can be dissociated such that fitting of slow phase velocity responses reflects exclusively the contribution of the inertialsystem.1
Data analyses
Raw eye movement measurements were converted off-line into eye position vectors using pre- and postimplantation (daily, before each experimental protocol) calibration values. The horizontal, vertical, and torsional components of the calibrated eye position vectors then were differentiated with a polynomial filter (Savitzky and Golay 1964) and mathematically processed to compute angular eye velocity,
, as described earlier. Subsequently, the fast phases of nystagmus were identified and removed based on time and amplitude windows set for the second derivative of the eye velocity vector amplitude. The identified fast phases were displayed visually on a plot of the eye position components to interactively correct potential misidentifications.
Gain and phase values were computed for each stimulus cycle by fitting a sinusoidal function (sum of 1st and 2nd harmonic) to each component of the desaccaded eye velocity vector using a nonlinear least squares algorithm based on the Levenberg-Marquardt method. Gains for both the first and the second harmonic response components were expressed as a ratio of the amplitude of each slow phase eye velocity component over peak head velocity. For 0.5-Hz adaptation, peak head and peak drum oscillation amplitudes were identical. Thus the reported orthogonal response gains tested at the adapting frequency also reflect gains relative to those required for ideal adaptation. For 0.05-Hz adaptation, peak drum oscillation amplitude was three times that of vestibular stimulation. Therefore reported gains have to be appropriately adjusted (i.e., multiplied by 1/3) to reflect values relative to ideal adaptation. Phase was expressed as the difference (in degrees) between peak eye velocity and peak head velocity. Ten cycles were used for gain and phase estimation at frequencies >0.05 Hz. At the lowest stimulus frequencies, a total of six (0.05 and 0.02 Hz) or three cycles (0.01 Hz) were analyzed. For each experimental run, the median, mean, and SD values of the gain and phase fits were stored for further processing. Analysis of variance was used to detect statistically significant differences in the data.
 |
RESULTS |
General characteristics in intact animals
Similarly to what has been reported previously in cats (Baker et al. 1986
; Harrison et al. 1986
; Schultheis and Robinson 1981
), optokinetic stimulation about an axis orthogonal to that of head rotation resulted in changes of the spatial characteristics of the primate VOR. Examples of pitch VOR before and after adaptation in the presence of horizontal OKN stimulation have been plotted in Fig. 1B. Before adaptation, pitch VOR in complete darkness elicited purely vertical slow phase eye velocity (Fig. 1B, left). After 2 h of pitch head movements in the presence of horizontal optic flow, VOR responses exhibited a large horizontal slow phase velocity component when tested in complete darkness (Fig. 1B, right).
In all 16 combinations of visual/vestibular stimuli, animals could adaptively change the direction of the elicited eye movements by generating an orthogonal component collinear with the direction of optokinetic stimulation. In no case did the gain and phase of the main response component in intact animals change after adaptation. Average data for the orthogonal response elicited before and after 2 h of adaptation for all labyrinthine-intact animals have been included in Table 1 separately for each adapting condition. The gain of the orthogonal component when tested at the adapting frequency in an animal that was tested in all conditions has been plotted in Fig. 2 as a function of time during adaptation. For all testing during adaptation, the axis of rotation remained earth-vertical for EVA adaptation and earth-horizontal for OVAR adaptation. With an adapting frequency of 0.5 Hz, orthogonal gains after 2 h of either EVA or OVAR adaptation reached values that were ~40-70% of head velocity (Fig. 2, left; see also Table 1).

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| FIG. 2.
Time course of orthogonal slow phase velocity changes at the adaptingfrequency during cross-axis adaptation: changes in the gain of the elicited orthogonal response component (normalized to 0 at the start of adaptation) were plotted as a function of time during adaptation for all 16 different adaptation protocols (1 animal). tVOR + vOKN: roll head movements in the presence of vertical optokinetic stimulation ( ); tVOR + hOKN: roll head movements in the presence of horizontal optokinetic stimulation ( ); vVOR + hOKN: pitch head movements in the presence of horizontal optokinetic stimulation ( ); hVOR + vOKN: yaw head movements in the presence of vertical optokinetic stimulation ( ). EVA, earth-vertical axis head rotations; OVAR, earth-horizontal axis head rotations. Axis of rotation during testing was identical to that during adaptation (i.e., earth-vertical for EVA adaptation and earth-horizontal for OVAR adaptation).
|
|
Results were quite different, however, when the adaptation was performed at a low stimulus frequency (0.05 Hz; Fig. 2, right; see also Table 1). First, head oscillations about an earth-vertical axis during adaptation resulted in orthogonal response gains that reached lower values than those obtained at 0.5 Hz (Fig. 2, top). Because peak drum oscillation amplitude was three times that of head oscillation amplitude during adaptation, gain values of 20-40% suggest adaptive changes that only account for ~10% of ideal adaptation responses. Second, with a low-frequency adapting sequence, orthogonal responses were different after EVA and OVAR adaptation. Contrary to the small orthogonal response gains acquired with low-frequency EVA adaptation protocols, adapted response gains were generally large when the head rotated about an earth-horizontal axis during adaptation (Fig. 2 right, top vs. bottom traces). Finally, for the OVAR adapting sequences, peak orthogonal response gain seemed to depend on the particular visual/vestibular combination, being the largest for tVOR + hOKN and the smallest for tVOR + vOKN (Table 1).
The magnitude of the orthogonal response component (when tested at the adapting frequency) after 2 h of OVAR adaptation in animals with intact labyrinths has been plotted versus the equivalent values after EVA adaptation in Fig. 3A (each symbol corresponds to a pair of EVA-OVAR adaptation protocols under different conditions in different animals). Data acquired after adaptation at 0.5 Hz fell along the line of unity ratio, indicating that orthogonal response gains were similar in magnitude and independent of the head orientation relative to gravity [F(1,18) = 0.19, P > 0.05; see Fig. 3A, solid symbols]. Data acquired at 0.05 Hz, however, were scattered in the top half of the plot, suggesting that OVAR adaptation at 0.05 Hz was consistently more efficient than EVA adaptation in changing the spatial direction of VOR slow phase velocity [F(1,20) = 85.7, P < 0.05; see Fig. 3A, open symbols]. Inspection of the vertical distribution of the data further supports the observation that orthogonal response gains at 0.05 Hz depended on the particular visual/vestibular condition, being largest after horizontal OKN in the presence of vertical plane rotations [F(3,11) = 8.3, P < 0.05]. Equivalent data from LC and RALP canal-plugged animals (limited to head oscillation in the plane of the plugged canals) have been plotted in Fig. 3B. In the following paragraphs, these observations are characterized in more detail for each adaptation protocol, first in intact and subsequently in canal-plugged animals.

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| FIG. 3.
Relationship between magnitude of adaptive changes when the axis of head rotation during adaptation was EVA and OVAR: orthogonal response gain obtained at the adapting frequency in complete darkness 2 h after EVA adaptation was plotted vs. orthogonal response gain after OVAR adaptation. A: data in animals with intact labyrinths. B: data in animals after plugging of the right anterior/left posterior canals (ralp VOR + hOKN) or of both lateral canals (hVOR + vOKN). Open symbols, data at 0.05 Hz; solid symbols, data at 0.5 Hz; ···, unity line slope. Adaptation protocols as specified (see also Fig. 2). Axis of rotation during testing was identical to that during adaptation (i.e., earth-vertical for EVA adaptation and earth-horizontal for OVAR adaptation).
|
|
Dynamic properties of orthogonal component
After 2 h of adaptation to simultaneous yaw head oscillations combined with vertical optokinetic stimulation at 0.5 Hz, vertical (orthogonal) response gains elicited during yaw rotation in complete darkness were largest at high frequencies and progressively decreased at frequencies lower than the adapting frequency. Vertical response phase also depended on frequency (Fig. 4, each symbol shows data from a different animal): it was consistently ~0° at the adapting frequency of 0.5 Hz, but phase leads and lags were introduced at lower and higher frequencies, respectively. Horizontal slow phase eye velocity gain and dynamics were indistinguishable from those before adaptation (Fig. 4, dotted lines).

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| FIG. 4.
Frequency response of main ( hor) and orthogonal ( ver) response component after 2 h of hVOR + vOKN EVA adaptation at 0.5 Hz: gain and phase values from 4 different animals are plotted as a function of frequency. ···, average horizontal VOR values from 7 rhesus monkeys (data from Fig. 7, Angelaki and Hess 1996b ). Axis of rotation during testing was identical to that during adaptation (i.e., earth-vertical).
|
|
Similar results were also observed for the other three adaptation conditions (tVOR + hOKN, vVOR + hOKN, and tVOR + vOKN). Because the dynamics of the orthogonal response component after 0.5-Hz EVA adaptation were qualitatively similar, gain and phase from all four adaptation protocols (i.e., tVOR + vOKN, tVOR + hOKN, vVOR + hOKN, and hVOR + vOKN; all at 0.5 Hz with head oscillations about an earth-vertical axis) have been combined (in 2 conditions, the orthogonal response component was horizontal, whereas in the other 2 conditions, the orthogonal response component was vertical). To better evaluate the frequency dependence of orthogonal responses in this and subsequent figures, gains have been normalized to unity at the adapting frequency before averages were computed. Mean data values (±SD) from all animals have been plotted in Fig. 5 (open circles with error bars). Because there was no change in the main response component, only the gain and phase of the orthogonal components have been plotted in this and subsequent figures.

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| FIG. 5.
Dynamic properties of the orthogonal response component after 0.5-Hz EVA adaptation: mean ± SD of gain and phase values for earth-horizontal ( ) and earth-vertical ( ) axis rotations in the adapted animals have been plotted as a function of frequency. Data from all 4 different adapting conditions (tVOR + vOKN, tVOR + hOKN, vVOR + hOKN, and hVOR + vOKN) were included in the average (n = 13). Gains were normalized to a value of unity at 0.5 Hz before averages were calculated. ···, average horizontal and vertical VOR gain and phase values from 7 rhesus monkeys (data during earth-vertical axis rotations normalized at 0.5 Hz and replotted from Fig. 7, Angelaki and Hess 1996b ).
|
|
For comparison with the adapted VOR dynamics, the mean gain and phase values of horizontal and vertical VORs in intact animals have been included as dotted lines in this and subsequent plots (normalized to a gain of unity at 0.5 Hz; data obtained from 7 animals, as in Angelaki and Hess 1996b
). A comparison with such normalized control data shows that the dynamics of the horizontal or vertical orthogonal response component were, in general, different from those of the horizontal or vertical VORs. For example, after earth-vertical axis adaptation at 0.5 Hz, gain declined with frequency with a larger slope than that of either horizontal or vertical VORs (Fig. 5). In addition, a characteristic phase lag was always present when the adapted VOR was tested at 1.1 Hz (the highest frequency tested here; Fig. 5, open symbols). When tested with earth-horizontal instead of earth-vertical axis oscillations, the dynamics of the orthogonal response component were characterized by smaller low frequency phase leads (Fig. 5, solid symbols), similarly as in primate horizontal, vertical, and torsional VORs (Angelaki and Hess 1996b
).
Similar observations characterized the dynamic properties of the orthogonal components when the 0.5-Hz head oscillations during adaptation were about an earth-horizontal axis. Mean data values (± SD) from all animals (after normalizing gains to unity at 0.5 Hz) were plotted separately for responses obtained from earth-horizontal and earth-vertical axis rotations (Fig. 6; solid and open circles, respectively). Similarly as after earth-vertical axis adaptation, gains decreased at frequencies away from the adapting frequency and phase lags were observed at 1.1 Hz. The adapted orthogonal components exhibited the characteristic low-frequency differences in response phase when the axis of rotation was earth-vertical compared with earth-horizontal.

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| FIG. 6.
Dynamic properties of the orthogonal response component after 0.5-Hz OVAR adaptation: mean ± SD of gain and phase values for earth-horizontal ( ) and earth-vertical ( ) axis rotations in the adapted animals have been plotted as a function of frequency. Data from all 4 different adapting conditions (tVOR + vOKN, tVOR + hOKN, vVOR + hOKN, and hVOR + vOKN) have been included in the average (n = 13). Gains have been normalized to a value of unity at 0.5 Hz before averages were calculated. ···, average horizontal and vertical VOR gain and phase values from 7 rhesus monkeys (data during earth-horizontal axis rotation normalized at 0.5 Hz and replotted from Fig. 7, Angelaki and Hess 1996b ).
|
|
Interestingly, when animals adapted at a low frequency (0.05 Hz), results were different. In particular, we observed two different types of dynamic responses after low-frequency EVA adaptation: one, associated with the tVOR + hOKN adaptation protocols, and a different one associated with all the other tested protocols. Average data from all animals and all protocols except the tVOR + hOKN adaptation condition are illustrated in Fig. 7 (solid circles). Gains (normalized to a unity value at 0.05 Hz) were relatively independent of testing frequency. In fact, the gain and phase dependence on frequency was similar as those of horizontal and vertical VORs (compare solid circles with dotted lines in Fig. 7). Nevertheless, nonzero phase lags also characterized the orthogonal component during 1.1-Hz oscillations. In contrast, the dynamic properties of the orthogonal component were different for the tVOR + hOKN condition [F(3,42) = 32.8, P < 0.05; see Fig. 7, open squares]. The orthogonal component was large only when tested at the adapting frequency, and gains fell off sharply at lower and higher frequencies. In addition, response phase was strongly dependent on frequency: at low frequencies, large phase leads were present. At frequencies above the adapting frequency, orthogonal responses strongly lagged the stimulus.

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| FIG. 7.
Dynamic properties of the orthogonal response component after 0.05-Hz EVA adaptation. , means ± SD of gain and phase values for tVOR + hOKN adaptation (n = 4); , means ± SD of gain and phase values for 3 adapting conditions (tVOR + vOKN, vVOR + hOKN, and hVOR + vOKN; n = 8). Gains have been normalized to a value of unity at 0.05 Hz before averages were calculated. ···, average horizontal and vertical VOR gain and phase values from 7 rhesus monkeys (data during earth-vertical axis rotations normalized at 0.05 Hz and replotted from Fig. 7, Angelaki and Hess 1996b ).
|
|
As mentioned above, animals adapted differently to orthogonal vestibular and optokinetic stimuli at low frequencies when the axis of rotation was earth-vertical and -horizontal. Figures 8-10 illustrate the dynamic properties of the orthogonal component generated after 0.05 Hz OVAR adaptation. Even though differences in gain among the four different adaptation conditions are not apparent in the following plots (because gain data have been normalized to unity at 0.05 Hz, ± 180° before averages were calculated), relative differences in response gain will also be summarized (for unnormalized orthogonal gain values, see also Table 1).

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| FIG. 8.
Dynamic properties of orthogonal response component after 0.05-Hz OVAR adaptation for 2 different adapting conditions, tVOR + hOKN (left) and vVOR + hOKN (right). Mean ± SD gain and phase of horizontal slow phase velocity elicited during earth-horizontal ( ) and earth-vertical ( ) axis roll (left) or pitch (right) oscillations in the adapted animals (n = 3 and n = 3, respectively). Before averages were computed, all gains were normalized relative to those during earth-horizontal axis rotation at 0.05 Hz, ±180°. For frequencies 0.05 Hz, peak oscillation amplitude was 90°. For frequencies 0.05, Hz peak oscillation amplitude was 180°. ···, average horizontal VOR gain and phase values from 7 rhesus monkeys (data during earth-horizontal axis rotations normalized at 0.05 Hz and replotted from Fig. 7, Angelaki and Hess 1996b ).
|
|
Roll and pitch head movements in the presence of horizontal optic flow and the animal centered in upright position induced the largest adaptive changes in the VOR. Interestingly, the dynamics of the orthogonal (horizontal) response component were similar for both adapting conditions(tVOR + hOKN and vVOR + hOKN; Fig. 8). Examination of the normalized orthogonal response component during earth-horizontal axis oscillations suggested two discrete "modes" (Fig. 8, solid symbols). As outlined in METHODS, tests with frequencies of
0.05 Hz routinely were performed at peak oscillation amplitudes of
90° (±5, ±18, ±45, ±90, and ±90° for 1.1, 0.5, 0.2, 0.1, and 0.05 Hz, respectively), resulting in a sinusoidal motion where head angular velocity and position in space (i.e., relative to gravity) traced out similar waveforms (90° out of phase relative to each other). For test frequencies of
0.05 Hz (0.05-Hz data values were obtained for both stimulus conditions; see METHODS), peak-to-peak oscillation amplitude either comprised or exceeded a single revolution in space (±180, ±450, and ± 900° for 0.05, 0.02, and 0.01 Hz, respectively). Under these test conditions, the angular head velocity stimulus sensed by the vestibular system maintains its sinusoidal waveform at the frequency of stimulation, however, the gravity (head-position-sensitive) stimulus sensed by the otolith system exhibits a much more complex waveform at a varying frequency that is a function of instantaneous angular velocity (for a more detailed explanation of these stimuli, see Angelaki and Hess 1996b
). During the former set of stimuli (i.e., peak oscillation amplitudes of
90°), two distinct otolith-ocular reflexes, the inertial (velocity-storage) and orienting (counterrolling and counterpitching) responses, are both co-activated and, along with the semicircular-canal-ocular reflex, generate the observed head-velocity-dependent modulation in slow phase eye velocity. With the latter stimuli where the waveform of head angular velocity and that of head position relative to gravity are different (i.e., when peak oscillation amplitudes are
180°), only inertial otolith-ocular responses combine with the semicircular canal-ocular signals to generate the head velocity-dependent modulation in slow phase eye velocity that has been analyzed here.1
The fact that small-amplitude head oscillations (similar to those during adaptation) were characterized by orthogonal (horizontal) response components that were 5-10 times larger than those elicited during large amplitude head oscillations at a similar frequency [i.e., compare 0.05-Hz data in Fig. 8; F(1,7) = 10.1; P < 0.05] suggests that it is the orienting and not the inertial aspect of the otolith-ocular system that is responsible for these adaptive changes. Indeed, low-frequency inertial response gains were indistinguishable from those during earth-vertical axis oscillation testing [F(1,22) = 0.53, P > 0.05; compare solid circles with open symbols at the three lowest frequencies in Fig. 8].
The standard experimental protocol tested in all animals involved different peak amplitudes for different frequencies. To further examine the frequency and amplitude selectivity of the adapted responses to the 0.05 Hz OVAR conditions, specific protocols were applied in selected animals (Fig. 9). For example, the otolith contribution to the adapted responses was largest at low frequencies (even lower than 0.05 Hz), as evident when oscillation amplitudes were kept constant at 60° (Fig. 9A). Furthermore, for oscillations with peak amplitudes
90°, orthogonal response gains were independent of stimulus amplitude (Fig. 9B). As already mentioned, when peak-to-peak oscillation amplitude exceeded a single revolution and the fitted slow phase velocity reflected only inertial but not orienting responses, orthogonal response amplitude was significantly smaller.

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| FIG. 9.
Dependence of orthogonal response gain on frequency and peak oscillation amplitude after 0.05-Hz OVAR tVOR + hOKN adaptation. A: orthogonal response gain as a function of frequency during earth-horizontal axis rotation with peak oscillation amplitude of 60°. B: orthogonal response gain during 0.05-Hz earth-horizontal axis oscillations as a function of peak oscillation amplitude. Data from 1 (B) or 2 animals (A, and ).
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Results obtained from the tVOR + vOKN low-frequency OVAR adaptation protocol were different from the other adapting conditions (Fig. 10, left). Orthogonal (vertical) response gains were indistinguishable for earth-vertical and-horizontal axis testing [F(1,11) = 1.8, P > 0.05; see Fig. 10, open vs. solid circles]. Moreover, response gains were similar for small- and large-amplitude earth-horizontal axis oscillations. Therefore, it would appear that the otolith-ocular system does not contribute to the adaptive changes under this condition. Indeed, as already shown in Fig. 3A (open circles), orthogonal response gains after 2 h of tVOR + vOKN EVA and tVOR + vOKN OVAR adaptation protocols were similar, with data points falling close to the unity slope line. These results suggest that the presence of a gravity component along the interaural axis (as during roll oscillations) can adaptively change the direction of the elicited eye movement only from torsional to horizontal but not to vertical.

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| FIG. 10.
Dynamic properties of the orthogonal response component after 0.05-Hz OVAR adaptation for 2 different adapting conditions, tVOR + vOKN (left) and hVOR + vOKN (right). Mean ± SD of gain and phase of vertical slow phase velocity that is elicited during earth-horizontal ( ) and earth-vertical ( ) axis roll (left) or yaw (right) oscillations in the adapted animals (n = 3 and n = 4, respectively). Before averages were computed, all gains were normalized relative to those during earth-horizontal axis rotation at 0.05 Hz, ±180°. For frequencies 0.05 Hz, peak oscillation amplitude was 90°. For frequencies 0.05 Hz, peak oscillation amplitude was 180°. ···, average vertical VOR gain and phase values from 7 rhesus monkeys (data during earth-horizontal axis rotations normalized at 0.05 Hz and replotted from Fig. 7, Angelaki and Hess 1996b ).
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Again, a different picture emerged from the fourth low-frequency adaptation protocol (hVOR + vOKN): first, the otolith-ocular system did contribute to adaptation, as suggested by earth-vertical axis gains that were lower than earth-horizontal axis gains during sinusoidal testing after the 0.05-Hz OVAR protocol [F(1,41) = 33.2, P < 0.05; see Fig. 10, right; compare open with solid symbols) and by absolute gains during 0.05-Hz OVAR adaptation that were more than double those acquired after 0.05-Hz EVA adaptation [F(1,5) = 53.4, P < 0.05; see Fig. 3A, down triangles]. The otolith adaptive properties, however, do reflect a different organization for these vertical orthogonal components from that observed for the horizontal orthogonal response component elicited after adaptation with the tVOR + hOKN and vVOR + hOKN conditions: even though a difference between responses gains tested with small- and large-amplitude 0.05-Hz oscillations also was present, it was smaller. Moreover, response phase lagged head velocity during small-amplitude earth-horizontal axis oscillation testing.
Second harmonic response component
Oscillation of the optokinetic drum about an axis that was space-fixed simultaneously with head movements about a nested orthogonal axis resulted in a complex optic flow pattern (with respect to the animal) with higher harmonic components in addition to the fundamental oscillation frequency. Among these higher harmonics, the largest one was a second harmonic optic flow component about an axis that was mutually orthogonal to both the axis of head movement and the optokinetic stimulus axis. This second harmonic optic flow component was small at 0.5 Hz, ±18° (~15.7% of the fundamental) but much larger at 0.05 Hz, ±60° (~52% of the fundamental). To investigate whether the spatial organization of the adapted VOR reflected the contribution of this second harmonic optic flow component, we included a second harmonic term to the sinusoidal function, which was fitted to slow phase eye velocity. Gains of second harmonic responses are illustrated in Fig. 11, A and B, as a function of time during adaptation for two different animals. There was no second harmonic response in the adapted VOR after EVA adaptation (Fig. 11, A and B, top). This suggests that semicircular canal-ocular pathways can adaptively change their spatial organization only in response to an optic flow component at the same frequency as that of head oscillation.

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| FIG. 11.
Time course of adaptation of 2nd harmonic response component. A and B: gain of the 2nd harmonic response component (orthogonal to both the plane of head oscillation and the plane of optokinetic stimulation) elicited during 0.05-Hz oscillations in complete darkness and plotted against time of adaptation for 2 different animals. Data after 0.05-Hz EVA (top) and 0.05-Hz OVAR (bottom) adaptation were illustrated separately for tVOR + vOKN ( ), tVOR + hOKN ( ), vVOR + hOKN ( ), and hVOR + vOKN ( ). Axis of rotation during testing was identical to that during adaptation (i.e., earth-vertical for EVA adaptation and earth-horizontal for OVAR adaptation).
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Interestingly, however, there was a large second harmonic response component about the appropriate spatial axis when the axis of head oscillation during adaptation was earth-horizontal (see Fig. 14 for an example in a canal-plugged animal). The generation of these second harmonic VOR components followed a similar time course as those of the fundamental component (compare Fig. 11 with Fig. 2), and their gains, when tested at the adapting frequency and axis orientation in complete darkness after 2 h of adaptation, were roughly proportional to a similar eye movement component that was generated in the light during adaptation (Fig. 12A; see also Fig. 14, right). Moreover, different adapting conditions resulted in different second harmonic amplitudes: the largest second harmonic responses were observed after tVOR + hOKN and tVOR + vOKN adaptation, when the second harmonic component was vertical and horizontal, respectively (Fig. 11 and 12, A and B). The smallest second harmonic responses were observed after vVOR + hOKN and hVOR + vOKN adaptation, when the second harmonic component in both cases was torsional.

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| FIG. 14.
Low-frequency adaptation in an animal with all semicircular canals plugged. Horizontal ( hor), vertical ( ver), and torsional ( tor) slow phase eye velocity (fast phases removed) before adaptation (A) and after 2 h of 0.05-Hz OVAR tVOR + hOKN adaptation (B). Responses plotted either in complete darkness (left) or in the light during the combined stimulation (right).
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| FIG. 12.
Dynamic properties of 2nd harmonic response component. A: response gain tested at the adapting frequency in complete darkness has been plotted vs. gain in light 2 h after 0.05-Hz OVAR adaptation. B: mean response gain (±SD) obtained from responses to earth-horizontal axisoscillations after 0.05-Hz OVAR adaptation plotted as a function of frequency. Different adaptation protocols: tVOR + vOKN ( ), tVOR + hOKN ( ), vVOR + hOKN ( ), and hVOR + vOKN ( ); ···, average gain values during earth-vertical axis testing.
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The gain of these second harmonic components was amplitude and frequency specific, similarly to that of the orthogonal component at the frequency of head oscillation (Fig. 12B). In addition, no such second harmonic response was observed when the VOR was tested about an earth-vertical axis after 0.05-Hz OVAR adaptation (Fig. 12B, dotted lines). These observations, as well as the fact that these second harmonic components were similar in canal-plugged animals (Fig. 14), suggest that the otolith-ocular system is capable of adapting to the presence of retinal slip induced by noncomplementary optic flow stimulation at a different frequency from that of the head movement.
Responses in animals with plugged semicircular canals
VOR adaptation was also tested in five animals after both lateral canals (LC animals) or the right anterior/left posterior canals (RALP animals) or all six semicircular canals were inactivated by plugging (3 of these animals have also been used for control responses; the other 2 were only tested after plugging). Adaptive protocols during rotation in the intact canal planes yielded results that were indistinguishable from controls. The following presentation focuses on responses after adaptation obtained during head movements in the plane of plugged canals.
The time course of changes in the gain of the orthogonal response component for a LC and a RALP animal have been plotted in Fig. 13 (open symbols: data before plugging; gray and black symbols: data 2 and 7 mo after plugging). Similar results were also obtained in the other animals. Adaptation was absent, and the amplitude of the orthogonal response component was minuscule for EVA adaptation (for both the 0.5- and 0.05-Hz protocols; Fig. 13, top), as well as for both the EVA and OVAR 0.5-Hz adapting protocols (Fig. 13, bottom left). In contrast, large orthogonal response gains were found after 0.05-Hz OVAR adaptation protocols, further supporting the conclusion that the adapted responses in intact animals originate mainly from otolith rather than semicircular canal system activation. An example of roll head movements about an earth-horizontal axis at 0.05 Hz before and after 0.05-Hz tVOR + hOKN OVAR adaptation in the all canal-plugged animal is illustrated in Fig. 14, A and B. After 2 h of adaptation, both a horizontal response component at the frequency of head oscillation and a vertical response component at double the frequency of head oscillation are evident during roll head oscillations in complete darkness (Fig. 14B, left). For comparison, data during tVOR + hOKN stimulation in the light were also displayed both within the first 5 and the last 5 min of combined stimulation (Fig. 14, A and B, right).

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| FIG. 13.
Cross-axis adaptation in animals after inactivation of both lateral semicircular canals (hVOR + vOKN, LC animal; circles) and of the right anterior/left posterior canals (ralp VOR + hOKN, RALP animal; squares). Gain changes (data normalized to 0 at the beginning of adaptation) of the orthogonal response component elicited during oscillations in complete darkness at the adapting frequency and plotted as a function of time of adaptation before, as well as 2 and 7 mo after plugging (open, gray, and black symbols, respectively). Axis of rotation during testing was identical to that during adaptation (i.e., earth-vertical for EVA adaptation and earth-horizontal for OVAR adaptation). Control data were not available for the LC animal for 0.05-Hz EVA adaptation. Notice the different scale for 0.05-Hz, OVAR.
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An interesting result in canal-plugged animals that was not observed in animals with intact labyrinths was the presence of gain increases in the main response component as a function of time during adaptation (compare torsional response components in Fig. 14, A and B, left; compare also open with gray and black symbols in Fig. 15). These increases in main response gain were small for 0.5-Hz adaptation but relatively large in the low-frequency adapting sequences. No such increases were observed during earth-vertical axis adaptation, suggesting that it is the otolith system that is responsible for these changes.

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| FIG. 15.
Gain changes of main response component tested at the adapting frequency in animals after inactivation of both lateral canals (hVOR + vOKN, LC animal; circles) or of the right anterior/left posterior canals (ralp VOR + hOKN, RALP animal; squares). Data (normalized to 0 at the start of adaptation) before, as well as 2 and 7 mo after, plugging (open, gray, and black symbols, respectively). Axis of rotation during testing was identical to that during adaptation (i.e., earth-vertical for EVA adaptation and earth-horizontal for OVAR adaptation). An increase in gain of the main response component as a function of time during adaptation was only observed during OVAR adaptation.
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The dynamics of the adapted VOR in the plugged animals after 0.05-Hz OVAR adaptation were characterized by properties similar to those of intact animals (Figs. 8-10): orthogonal response gains (for both the 1st and 2nd harmonic) were largest during low-frequency, small-amplitude head oscillations and minimal during low-frequency, large-amplitude head oscillations. These results complement responses in intact animals and suggest that otolith system adaptation was primarily responsible for the low-frequency OVAR responses obtained in these experiments.
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DISCUSSION |
We have examined the properties of spatial adaptation of the VOR in three dimensions. Two different adaptation frequencies (0.5 and 0.05 Hz) were used to represent bandwidths in which VOR properties are determined by either the absence or presence of the inertial (velocity storage) properties (e.g., Angelaki and Hess 1996b
). Four different combinations of orthogonal visual/vestibular protocols were tested (tVOR + vOKN, tVOR + hOKN, vVOR + hOKN, and hVOR + vOKN). The axis of rotation during adaptation and testing was either earth-vertical or -horizontal. With earth-vertical axis rotations, we specifically tested the adaptive properties of the VOR that are determined largely by semicircular canal activation. With earth-horizontal axis rotations, we examined the adaptive properties of the system when both semicircular canal and otolith receptors (animals with intact labyrinths) or otolith receptors alone (canal-plugged animals) are activated dynamically. We have found characteristic differences in the spatial adaptation of the VOR based on these 16 different adapting protocols. The following paragraphs summarize our main results and discuss some of the possible underlying mechanisms.
VOR spatial adaptation at 0.5 Hz
Adapted responses at 0.5 Hz were independent of the orientation of the axis of rotation during adaptation (i.e., earth-vertical or -horizontal). For all tested conditions, orthogonal response gains reached values as large as 30-70% of head velocity (and consequently, that required for ideal adaptation) when tested at the adapting frequency 2 h after adaptation (Fig. 2, left, and Fig. 3, solid symbols; see also Table 1). These changes were acquired with an approximately exponential time course. Similar time courses of hVOR + vOKN adaptation have also been reported previously in cats and humans (Harrison et al. 1986
; Khater et al. 1990
).
The gain of the orthogonal response components was frequency specific for both earth-vertical and -horizontal axis protocols (Figs. 5 and 6). In the cat, hVOR + vOKN adaptation at a single frequency also resulted in strongly frequency-specific orthogonal response gains (Harrison et al. 1986
; Powell et al. 1991
). Parallel to this frequency-dependent gain behavior, phase leads were present at frequencies below the adapting frequency, whereas phase lags were introduced at frequencies above the adapting frequency. In contrast to the results in cats, a much broader frequency selectivity without any significant phase leads or lags at frequencies away from the adapting frequency has been reported under identical experimental conditions in human subjects (Khater et al. 1990
). Our results in rhesus monkeys are rather similar to those previously reported in cats and unlike those in humans: EVA adaptation at 0.5 Hz (a frequency similar to the 0.25-Hz stimuli used in these previous studies) resulted in frequency-specific changes with associated phase leads or lags for frequencies lower or higher, respectively, than the adapting frequency.
VOR spatial adaptation at 0.05 Hz
With low-frequency adaptation sequences and the axis of rotation earth-vertical, adapted responses were small for all animals and all conditions tested. Because OKN amplitude was three times that of head oscillation amplitude, gains of 20-40% suggest only a 10% efficacy in adaptation. In addition, the small orthogonal responses generated after tVOR + vOKN, vVOR + hOKN, and hVOR + vOKN adaptation were relatively independent of testing frequency. In contrast, orthogonal responses were strongly tuned to the adapting frequency after tVOR + hOKN EVA 0.05-Hz adaptation (Fig. 7).
When the axis of head motion was earth-horizontal during the low-frequency adaptation protocols, several interesting observations were made: first, adaptation was large, with orthogonal response components often exceeding head velocity. Because the OKN stimulus amplitude during 0.05-Hz adaptation was three times that of head oscillations, orthogonal gains of 90-120% would correspond only to 30-40% of the ideal adaptation gain. Second, the temporal properties of the adapted orthogonal component were dependent on the particular visual/vestibular stimulus combination during training. The largest coupling was observed after tVOR + hOKN or vVOR + hOKN adaptation. On the other extreme, small adaptive changes were observed after tVOR + vOKN adaptation. Third, adapted responses were strongly amplitude and frequency selective, suggesting a rather specific role of otolith system in cross-axis adaptation. Fourth, after 0.05-Hz OVAR adaptation, the VOR acquired spatially specific responses not only at the frequency of head oscillation but also at other frequencies of optic flow stimulation.
The properties of the adapted VOR after 0.05-Hz OVAR protocols are most likely related to the adaptive plasticity of the otolith-ocular system. The following facts support this conclusion. 1) Quantitative characteristics of the adapted VOR were very different for 0.05-Hz OVAR compared with EVA adaptation. 2) For 0.05-Hz OVAR adaptation, orthogonal responses during earth-vertical axis oscillations were small compared with the equivalent responses during earth-horizontal axis oscillations (Figs. 8 and 10, compare open with solid symbols). 3) Similar properties were also observed after 0.05-Hz OVAR adaptation in animals with inactivated semicircular canals by plugging (Figs. 13 and 14).
Adaptive properties of the otolith-ocular system: can the inertial, orienting, and translational otolith-ocular VOR responses adapt?
In previous work, we have argued that the otolith-ocular system can best be characterized in the context of the following three aspects (Angelaki and Hess 1996a
,b
): 1) translational VORs, i.e., primarily horizontal responses compensatory to translational motion (Paige 1989
; Paige and Tomko 1991a
,b
; Schwarz and Miles 1991
; Schwarz et al. 1989
; Snyder and King 1992
; Viirre et al. 1986
); 2) orienting responses, i.e., torsional and vertical eye movements during roll and pitch head tilts, respectively. These reflexes are responsible for ocular counterrolling during roll tilts and counterpitching during pitch tilts (Diamond et al. 1979
; Hannen et al. 1966
; Kellogg 1965
; Lichtenberg et al. 1982
; Paige and Tomko 1991a
). Both the translational VORs and the orienting otolith-ocular reflexes are elicited in response to distinct linear acceleration stimuli along specific directions. As a consequence, they are generated during both linear motions and angular movements relative to gravity (i.e., tilts and off-vertical axis rotations). 3) The third aspect is inertial responses, which are elicited only during angular motion and never during linear head movements. These responses comprise a number of observations characterizing low-frequency VOR responses (associated with "velocity storage") (e.g., Angelaki and Hess 1994
-1996b
). Whenever there is a rotation about an off-vertical axis, there is a spatially specific dynamic activation of primary otolith afferents based on which the central otolith system computes head angular velocity (Angelaki 1992a
,b
; Hain 1986
; Hess 1992
; Schnabolk and Raphan 1992
). These central otolith-born head velocity signals drive the steady-state slow phase velocity component ("bias") during constant-velocity head rotation and are manifest as an enhancement of low-frequency VOR dynamics during sinusoidal oscillations about off-vertical axes (Angelaki and Hess 1996b
).
The inertial aspects of the otolith-ocular system can be separated easily from the first two response categories by either rotating animals at constant velocity or by sinusoidally oscillating animals with peak amplitudes that exceed a single revolution of the head in space (Angelaki and Hess 1996b
). During these two stimulus conditions, the waveform of the head position (i.e., gravity)-dependent responses is different from that of inertial, velocity-dependent responses. Using head oscillations with peak amplitudes <90 or >180°, we have shown here evidence that it is the orienting, head position-dependent otolith system that adapts to spatially mismatched visual and vestibular stimuli. Indeed, even though orthogonal response gains were large and relatively independent of peak oscillation amplitude when the latter did not exceed 90°, they were small and indistinguishable from earth-vertical axis responses during earth-horizontal axis oscillations with peak amplitude >180° (Figs. 8-10). Therefore, the head velocity-dependent inertial responses seem to have a negligible contribution to the orthogonal response gains during adaptation.
Our data thus show that orienting otolith-ocular reflexes do adapt in response to altered, spatially mismatched visual/vestibular stimulus conditions. For example, duringtVOR + hOKN and vVOR + hOKN adaptation, the presence of a gravitational (linear acceleration) component along the interaural and nasooccipital axis, respectively, is coupled to the presence of a horizontal optic flow (and thus, retinal slip) component. As a consequence, the orienting otolith-ocular system, which, in normal animals, is responsible for ocular counterrolling and counterpitching, adaptively changes the direction of the elicited eye movement accordingly. A similar plasticity in the orienting (but not inertial) responses during pitch and roll head movements also has been observed during recovery after selective semicircular canal plugging (Angelaki et al. 1996b
). These results suggest that even though orienting responses contribute little to slow phase eye velocity in the intact, normal primate VOR (Angelaki and Hess 1996a
,b
), they are characterized by a large ability to adaptively change their amplitude and/or eye movement direction in response to altered visuo-motor demands.
Despite this plasticity with respect to horizontal response components, the otolith system seems unable to direct the elicited eye movement toward vertical during roll oscillations, as suggested by the results after tVOR + vOKN adaptation: first, orthogonal response gains were relatively similar for EVA and OVAR adaptation (Figs. 2 and 3). Second, earth-vertical and -horizontal axis testing after OVAR adaptation resulted in similar orthogonal response gain and phase (Fig. 10, left). Perhaps, the presence of a linear acceleration (or gravity) component along the interaural (but not naso-occipital) axis during roll tilts prevents generation of vertical slow phase velocity, which usually is associated with pitch tilts (and gravity components along the naso-occipital axis).
Although the changes seen after tVOR + hOKN and vVOR + hOKN OVAR adaptation could be explained by a spatially specific organization of orienting otolith-ocular responses, a slightly different situation emerged for hVOR + vOKN adaptation. Despite the fact that the otolith system contributes clearly to the adapted VOR (Fig. 10, right, compare earth-vertical with -horizontal responses), quantitative properties of the orthogonal response gain and phase were different compared with those after tVOR + hOKN and vVOR + hOKN adaptation. First, there was little difference in orthogonal response gain for small (<90°, f
0.05 Hz) versus large (>180°, f
0.05 Hz) oscillation amplitudes. Second, responses were smaller for earth-vertical than earth-horizontal axis rotations. Finally, small oscillation amplitude responses (<90°, f
0.05 Hz) were characterized by relatively large phase lags, which were present in none of the other adapting conditions.
It has been shown previously that static head position relative to gravity is important in cross-axis adaptation. For example, changes in VOR direction generalizes to body orientations as large as 90° from the orientation during adaptation, but with a reduced gain (Baker et al. 1987
). Moreover, it also has been shown that VOR can hold simultaneously two opposing adaptive states, the expression of which are contingent on body orientation (Baker et al. 1987
). Experiments during pitch oscillations with the cats centered in upright position (i.e., earth-horizontal axis rotations) in the presence of horizontal optokinetic stimulation at 0.25 Hz, ±12° suggested otolith-mediated adaptive changes at low frequencies (Baker et al. 1986
, 1987
). Because the VOR was tested with small-amplitude head oscillations after adaptation, these observations most likely reflect changes in the orienting components of the otolith-ocular system, as in the present experiments.
Adaptive changes in the orienting components of the otolith-ocular reflexes have also been observed during space flight. Ocular counterrolling, for example, has been reported to decrease to zero in microgravity and increase beyond normal values in hypergravity (Hofstetter-Degen et al. 1993
). Furthermore, ocular counterrolling has been reported to be decreased for the first few days on return to earth, even though the quantitative details differ (Arrott and Young 1986
; Dai et al. 1994
; Hofstetter-Degen et al. 1993
; Vogel and Kass 1986
; Yakovleva et al. 1982
).
Finally, a novel observation of the present studies that deserves further investigation is the system's ability to adaptively change VOR spatial organization even at a different frequency from that of the imposed head movement. Interestingly, this ability seemed to be limited to the otolith-ocular system, as suggested by the absence of a second harmonic 1) in the adapted VOR after earth-vertical axis adaptation (Fig. 11) and 2) in the VOR elicited during earth-vertical axis oscillations after 0.05-Hz OVAR adaptation (Fig. 12B, dotted lines). Furthermore, there are second harmonic components of similar properties in the adapted VOR of canal-plugged animals (Fig. 14). These results demonstrate a large adaptive plasticity of the orienting and perhaps translational components of the otolith-ocular system and a significant otolith contribution to primate angular VOR in response to altered visuo-motor requirements.