1Department of Surgery (Otolaryngology), University of Mississippi Medical Center, Jackson, Mississippi 39212; 2Regional Primate Research Center, 3Department of Physiology and Biophysics, and 4Department of Otolaryngology, Head and Neck Surgery, University of Washington, Seattle, Washington 98195; and 5Department of Neurology, Center for Sensorimotor Research, Ludwig Maximilians University, D81377 Munich, Germany
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ABSTRACT |
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Newlands, Shawn D., Leo Ling, James O. Phillips, Christoph Siebold, Larry Duckert, and Albert F. Fuchs. Short- and long-term consequences of canal plugging on gaze shifts in the rhesus monkey. I. Effects on gaze stabilization. To study the contribution of the vestibular system to the coordinated eye and head movements of a gaze shift, we plugged the lumens of just the horizontal (n = 2) or all six semicircular canals (n = 1) in monkeys trained to make horizontal head-unrestrained gaze shifts to visual targets. After the initial eye saccade of a gaze shift, normal monkeys exhibit a compensatory eye counterrotation that stabilizes gaze as the head movement continues. This counterrotation, which has a gain (eye velocity/head velocity) near one has been attributed to the vestibuloocular reflex (VOR). One day after horizontal canal plugging, the gain of the passive horizontal VOR at frequencies between 0.1 and 1.0 Hz was <0.10 in the horizontal-canal-plugged animals and zero in the all-canal-plugged animal. One day after surgery, counterrotation gain was ~0.3 in the animals with horizontal canals plugged and absent in the animal with all canals plugged. As the time after plugging increased, so too did counterrotation gain. In all three animals, counterrotation gain recovered to between 0.56 and 0.75 within 80-100 days. The initial loss of compensatory counterrotation after plugging resulted in a gaze shift that ended long after the eye saccade and just before the end of the head movement. With recovery, the length of time between the end of the eye saccade and the end of the gaze movement decreased. This shortening of the duration of reduced gain counterrotation occurred both because head movements ended sooner and counterrotation gain returned to 1.0 more rapidly relative to the end of the eye saccade. Eye counterrotation was not due to activation of pursuit eye movements as it persisted when gaze shifts were executed to extinguished targets. Also counterrotation was not due simply to activation of neck receptors because counterrotation persisted after head movements were arrested in midflight. We suggest that the neural signal that is used to cause counterrotation in the absence of vestibular input is an internal copy of the intended head movement.
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INTRODUCTION |
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Large gaze shifts are composed of rapid head and
saccadic eye movements. Once the eye saccade lands, the eye begins a
slow movement in the direction opposite to the head movement, i.e., a
counterrotation. The occurrence of a compensatory eye counterrotation once the target is acquired terminates the movement of the eye in space
and stabilizes gaze while the head continues to move. In fact,
stabilization of gaze requires either that eye counterrotation is
perfectly compensatory, i.e., has a gain (eye velocity/head velocity)
equal to one, or that the head movement has ended. For most large gaze
shifts in the primate, gaze is stabilized by a compensatory
counterrotation until the head movement stops. Thus the timing of the
initiation of the counterrotation, which appears coordinated with the
end of the eye saccade (Lefevre et al. 1992), effectively controls the termination of the gaze shift. Because the
counterrotation takes some time to increase to a gain of one, the gaze
control system must anticipate this delay and turn on the
counterrotation before the target is reached (Lefevre et al. 1992
).
In the normal animal, counterrotation depends on the vestibular system
because unexpectedly arresting the head movement stops the compensatory
eye movement (Bizzi et al. 1971) and removal of
vestibular input by bilateral labyrinthectomy results in an immediate
loss of counterrotation (Dichgans et al. 1973
). Thus complete bilateral labyrinthectomy initially produces hypermetric gaze
shifts, in part because compensatory counterrotation is eliminated. The
eye saccade ends near the target, but the head movement without the
compensatory counterrotation carries the gaze well past the target. In
time, counterrotation reappears and increases. Four months after
bilateral labyrinthectomy, counterrotation recovers to ~90% of its
previous amplitude, and gaze accuracy is restored (Dichgans et
al. 1973
). Recovery of counterrotation occurs despite the
persistent absence of a passive vestibuloocular reflex (VOR).
In labyrinthectomized animals, the time course and details of this
recovery have not been documented quantitatively. Furthermore, labyrinthectomy not only eliminates dynamic inputs during head turning
but also the robust tonic input to the vestibular nuclei due to the
high resting rate of vestibular afferents when the head is still
(Goldberg and Fernandez 1971). Therefore to eliminate this objection to labyrinthectomy, we plugged the canals bilaterally. The goals of our study are to document quantitatively the acute effect
of canal plugging on counterrotation, to quantify any recovery of
counterrotation after canal plugging, to investigate possible mechanisms underlying counterrotation recovery in the absence of
semicircular canal input, and to explore how disruption of the normal
relationship between the end of the saccadic eye movement and the end
of the gaze movement disrupts the termination of gaze shifts.
A preliminary report of this data has appeared in abstract form
(Newlands et al. 1996).
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METHODS |
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Gaze measurement and behavioral paradigms
Three Macaca mulatta monkeys, HC1, HC2, and
AC, were prepared for recording by implantation of a scleral
search coil under the insertions of the extraocular muscles
(Fuchs and Robinson 1966) and a metal post on the skull
to stabilize the head (Phillips et al. 1995
). The axis
of the head post was aligned with the C1-C2 joint. All surgery was performed under deep halothane inhalation anesthesia after induction with intramuscular ketamine (10 mg/kg).
To measure gaze position, we placed the animals in a chair, which in
turn was placed within alternating magnetic fields in spatial and
temporal quadrature. We measured gaze position (eye position in space)
to an accuracy of 1° over ±40° with an electromagnetic technique
(Robinson 1963). Gaze position was measured both with the head completely restrained and the head free to move about a
vertical axis. Head movements were constrained to rotate in the
horizontal stereotaxic plane by inserting the head post into a collar
attached to a potentiometer, which was fastened to a framework that
contained the field coils and held the chair. Head movement, as
measured by the potentiometer, was subtracted from gaze movement to
provide eye movement in the head. Throughout the text, "eye
movement" refers to eye movement with respect to the head.
Target movements were generated by sequential illumination of an array
of light-emitting diodes (LEDs), which faced the monkey at a distance
of 47 cm. Diodes were located between ±40° at 5° increments in dim
light. The monkeys were rewarded with applesauce for fixating a LED
target with an accuracy of 2° for 1-2 s. The LEDs were illuminated
in a pseudorandom order such that a mixture of gaze amplitudes with
different start and end positions resulted and also so that prediction
was eliminated (Bizzi et al. 1972). When the head was
fixed in space, we illuminated LEDs to a maximum of only ±30° from
straight ahead.
In some experiments, we eliminated all visual feedback during the gaze shift by turning the target LED off at the onset of the eye saccade while the animal was otherwise in total darkness. The LED was held off for 500 or 750 ms so that the target remained off during the entire eye counterrotation. Data were gathered using this "target extinguished" paradigm before plugging in HC2 and AC and on postplugging days 1, 3, 5, and 74 in HC1, days 1, 2, 4, 8, 12, and 21 in HC2, and on all postoperative days in AC.
Application of head and body movement stimuli
PASSIVE VOR TESTING.
To provide vestibular stimuli, we rotated the entire framework
including the monkey and the field coils about the interaural axis to
produce pitch or about a vertical axis midway between the two ears to
produce yaw. The monkeys' heads were secured to the framework through
the head post. The horizontal VOR (HVOR) was tested at frequencies of
0.1, 0.3, 0.5, 0.8, and 1.0 Hz with peak displacement held constant at
10°. The HVOR was tested both in the stereotaxic plane, in which the
gaze shifts were made, and with the nose pitched down 22° to rotate
the animal in a plane orthogonal to the vertical canals (Blanks
et al. 1985). The vertical VOR (VVOR) was tested at 0.3, 0.5, 0.8, and 1.0 Hz. All VOR testing was done in the dark. Monkeys were
kept alert by taps on the walls of the test chamber and by air puffs
blown unexpectedly on the back of their necks. The VOR was measured in
the dark approximately biweekly after canal plugging.
COR TESTING.
To test the cervicoocular reflex (COR), we fixed the animal's head in
space by means of a retractable arm and oscillated its body in yaw by
rotating the chair in which it sat. The body was rotated ±10° at
frequencies from 0.1 to 1.0 Hz. The coil frame moved with the chair, so
eye position was calculated by adding the chair position and eye
position signals. The validity of this method was verified by placing a
stationary test coil within the moving coil frame. COR gain was
calculated as (eye velocity/chair velocity).
ALTERING SENSORY INPUT DURING COUNTERROTATION. In monkey AC, we stopped the head movement at various times during eye counterrotation by means of the electromagnetic clutch attached to the head post. The application of the clutch was triggered by the initiation of the eye saccade with a delay adjusted by the experimenter. Trials were examined with the brake applied at various times, so that head stoppages were produced at all times of the eye counterrotation.
Data analysis
Analog voltages proportional to eye, head, gaze, chair, and target position, as well as signals indicating target illumination (or blanking) were converted to video signals with a Vetter PCM and recorded on video tape. The signals then were digitized off-line at 1 kHz with a Macintosh computer. Data were analyzed with the aid of interactive programs that displayed the data and automatically identified epochs for analysis.
ANALYSIS OF THE GAZE SHIFT. The start and end of the target step and the gaze, eye, and head movements of a gaze shift were identified by the computer using a velocity criterion of 20°/s, as were head-restrained saccades. The computer also identified the peak velocity of each movement. Each of these time points then was used to determine latencies and movement durations and was used as a reference for measurement of comparable velocities and positions of the other movement components. The results of this analysis could be displayed graphically or exported for further analysis using commercially available statistical and graphics packages.
As will be seen in a companion paper, gaze shifts after canal plugging were quite variable and often not directed at the target. Because the current paper deals specifically with the effects of canal plugging on eye counterrotation of targeted gaze shifts, we excluded from the analysis all gaze shifts that were not within 20% of the target amplitude.ANALYSIS OF THE COUNTERROTATION.
The period of counterrotation was taken as the interval between the end
of the eye saccade and either the termination of the gaze shift or the
occurrence of a correction saccade, whichever occurred first. We
considered the onset of counterrotation as the time when the eye began
rotating slowly in the direction opposite to the eye saccade. In the
normal animal, counterrotation usually begins immediately after the eye
saccade. On some trials, the eye holds its position (i.e., exhibited a
plateau) (Phillips et al. 1995) before counterrotation;
in those cases, counterrotation again was considered to begin when the
eye rotated slowly in a direction opposite to the eye saccade. The
inclusion of such trials did not materially effect our results since
gaze shifts with long plateaus were rare in these experiments.
ANALYSIS OF PASSIVE VOR GAIN.
Data from passive sinusoidal rotations was analyzed on a cycle by cycle
basis. Digitizing was done on a Macintosh II computer, which adjusted
the sampling rate to provide a constant number of samples (600) per
cycle. The computer identified and displayed individual cycles of head
and eye velocity and position, which then were desaccaded by one of the
investigators based on a visual inspection of the eye velocity trace.
All data during the saccade were removed from all subsequent analyses.
The program then fit a sine wave to each cycle excluding the desaccaded
segments by means of a least squares algorithm and provided the gain
and phase of the eye velocity relative to the velocity of the chair and therefore the head. Finally, after 10 cycles had been analyzed at
each frequency, the program determined, displayed, and saved the
average eye and head velocity data for all cycles.
Analysis of head movement frequencies
We calculated the frequency distribution of head movements during gaze shifts by estimating the power spectral density of sample head traces (e.g., a 35° head movement with a duration of ~700 ms). Records of average head movements were joined back to back and repeated to a length of 2.048 s and then subjected to a standard spectral analysis. This procedure eliminates the transients resulting from the discontinuity of the signal and improves the frequency resolution of the Fourier transform.
Surgical manipulations
CANAL PLUGGING. A postauricular incision exposed the mastoid cortex and a simple mastoidectomy was performed to reveal the semicircular canals. Each canal was individually entered, and the lumen of the canal was packed with fascia and bone dust. The defects then were sealed with bone wax. The wound was closed in two layers. In HC1, initially only the two horizontal canals were plugged, and then later all four vertical canals were plugged in a separate procedure. In HC2, only the horizontal canals were plugged. In AC, all six canals were plugged in one procedure. Immediately after canal plugging, the monkeys were placed in the dark overnight and tested the next day. Subsequently, the animals were housed with normal light/dark cycles.
DORSAL RHIZOTOMY. In one animal, bilateral cervical dorsal rhizotomy (C1-C3) was performed after all six canals were plugged. This procedure was performed via a dorsal approach with laminectomy of the cervical vertebrae to expose the spinal cord and dorsal roots and the dorsal roots were cut. The animal was allowed to survive only until the next day.
All experiments were carried out in strict accordance with the guidelines of the National Institutes of Health and the Society for Neuroscience and all surgical and behavioral protocols were approved by the Animal Care and Use Committee of the University of Washington. ![]() |
RESULTS |
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Normal counterrotation
As already described in several other studies, after the eye
saccade of a normal head-unrestrained gaze shift ends but before the
head movement is over, the eye counterrotates in the head (Fig.
1, preplug) so gaze remains stable in the
world. Stable gaze is the result of a compensatory eye counterrotation
the gain (/
) of which is near 1.0 throughout the head
movement. The technique for calculating eye counterrotation is
illustrated in Fig. 2. In Fig. 2,
instantaneous eye velocity 80 ms after the eye saccade is plotted
against the head velocity at that same time. Throughout this paper,
most often data at 80 ms are illustrated because this time is well
after the end of the eye saccade but well before the end of the head
movement. The slope of the linear regression determines the
counterrotation gain. For monkey HC1 (Fig. 2), the slope
(based on 375 gaze shifts) was 0.97 ± 0.03 (95% confidence
interval for the slope) whereas for monkey AC the slope was
1.00 ± 0.02 (201 gaze shifts; mean ± SD). All
calculations of counterrotation gain are based on an assortment of gaze
shifts between 20 and 80° unless otherwise noted.
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The preplugging counterrotation gains varied from one animal to another (Fig. 3), counterrotation gains in monkey HC1 tended to average <1.0, and consequently it exhibited occasional forward slides in gaze position after an eye saccade had ended. In contrast, counterrotation gains in monkey HC2 were greater than one, on average, and it exhibited occasional backward slides in gaze position after the eye saccade. Finally, counterrotation gains in monkey AC all were ~1.0 so its counterrotations produced the most stable gaze holding.
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For all pre- and post canal plugged gaze shifts that involved a head
movement (usually gaze shifts >25°) (Phillips et al. 1995), we first
considered whether counterrotation gain was related to either gaze or
target amplitude. In the late postplugging trials, counterrotation
gains tended to be slightly higher (by <15%) for smaller gaze and
head movements. This weak relation with head velocity is considered
later. Otherwise, counterrotation gain did not depend on whether gaze
shifts were centrifugal, centripetal, or across the primary direction
of gaze. Therefore we merged the data from all gaze shifts unless
otherwise noted.
With recovery, the length of time between the end of the eye saccade and the end of the gaze movement decreased. This shortening of counterrotation duration was due both to faster head movements and to an increased counterrotation gain.
Effects of canal plugging on the passive VOR
As expected, plugging of the semicircular canals produced a substantial reduction in the HVOR elicited by passive yaw rotations. One day after horizontal canal plugging, the gain of the HVOR was <0.10 at all frequencies (0.1-1.0 Hz) in both HC1 and HC2 whether their heads were in the normal upright stereotaxic position or were positioned so rotation occurred in the plane of the horizontal canals (Fig. 4A). In monkeys HC1 and HC2, horizontal canal plugging did not affect the pitch VOR, whose gain after plugging showed an average reduction from 0.84 to 0.81, which was not significant. Plugging of all canals in monkey AC produced postoperative HVOR gains <0.07 at all frequencies tested with the head in the stereotaxic position (Fig. 4A). Postoperative vertical VOR gains fell to <0.08 at all frequencies.
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In the two animals with only horizontal canals plugged, HVOR gain
increased with time. In HC2, who was last tested 73 days after horizontal canal plugging, the gain at 0.5 Hz increased to 0.21 with the head in the stereotaxic plane (Fig. 4A). The gain
increase was greater in HC1 because we followed him for 110 days by which time HVOR gain at 0.5 Hz was 0.45 with the head held in
the stereotaxic plane (Fig. 4A) and 0.27 with the head pitched 22° down (not shown). The highest HVOR gain in HC1
was 0.61 at 1.0 Hz (Fig. 4B). In this monkey, subsequent
vertical canal plugging at 121 days dramatically reduced the HVOR (Fig. 4A), which showed no evidence of recovery 50 days later
(not shown). In monkey AC, who had all canals plugged at
once, there was no significant recovery of either the HVOR (Fig.
4A) or VVOR (not shown) after 63 days (gains at all
frequencies
0.13).
It has been argued that the VOR at high frequencies survives canal plugging (R. D. Rabbitt, R. Boyle, and S. M. Highstein, unpublished observation). To determine whether the passive frequencies we tested were representative of those found in normal active head movements, we subjected representative head movements made by our monkeys to a fast Fourier transform (FFT). Less than 2% of the energy was at frequencies >2 Hz.
Acute effects of canal plugging on counterrotation gain
On postplug day 1, counterrotation velocities were well below normal in all animals (Fig. 1, acute postplug). Eighty milliseconds after the eye saccade, counterrotation gain for 39 gaze shifts was 0.27 ± 0.02 for monkey HC1 (Fig. 2, open squares) and 0.39 ± 0.02 for monkey HC2 for 141 gaze shifts (not shown). Counterrotation gain for 420 gaze shifts was essentially zero for monkey AC (Fig. 2). The values of counterrotation gain at 80 ms were similar to those measured at 40, 60, and 100 ms (Fig. 3). Counterrotation gain did not depend on either the amplitude of the head movement or the gaze movement. Because counterrotation gain was quite low, the gaze shift did not end until well after the eye saccade. In HC1, gaze shifts often were accomplished by multiple small eye movements with one large slow head movement. This pattern accounted for the lower number of accurate, typical shifts recorded in this animal.
Recovery of counterrotation
After plugging of either the horizontal canals or all canals, eye counterrotation gradually recovered (Fig. 1, late postplug). Some recovery of counterrotation gain was seen within 10 days of canal plugging in all three animals (Fig. 3). After 10 days, counterrotation gain remained relatively constant in monkey HC2 and continued to show a modest increase in monkeys HC1 and AC. In the two horizontal canal plugged animals, counterrotation gain was largest on the last days tested. In monkey HC1, counterrotation gain 80 ms after the eye saccade was 0.68 ± 0.01 (652 gaze shifts, Fig. 2) after 74 days, and in monkey HC1 it was 0.54 ± 0.01 (512 gaze shifts) after 47 days. After all canals had been plugged in monkey AC, the largest counterrotation gain at 80 ms was 0.60 ± 0.01 on day 49 (757 gaze shifts).
Source of counterrotation after canal plugging
After canal plugging, eye counterrotation could be the result of a variety of different sensory drives. These include visual, somatosensory from the neck, and vertical semicircular canal inputs. We now address each of these in turn.
ROLE OF DIRECT VISUAL FEEDBACK. To eliminate visual feedback, we turned off the target spot at the initiation of the eye saccade while the animal was otherwise in total darkness. Extinction of the target affected control saccades in different monkeys in different ways. In control experiments on HC2, eye counterrotation was the same whether the target was extinguished for 500 ms after initiation of the eye saccade or was left on continuously. In either case, eye counterrotation gain 80 ms after the eye saccade was 1.15 ± 0.01 (target on trials, 141 gaze shifts; target extinguished trials, 331 gaze shifts). In control experiments on AC, however, turning off the target caused a decrease in eye counterrotation gain before plugging. At 80 ms after the saccade, counterrotation gain was 1.00 ± 0.02 (201 gaze shifts) with the target spot on for the entire gaze shift and 0.89 ± 0.05 (140 gaze shifts) with the target light extinguished. Monkey HC1 was not tested with the target extinction paradigm.
For all three animals, counterrotation gains after canal plugging also were similar with the target light on or off. As seen in the data of Fig. 5 gathered 80 ms after the eye saccade, the slope of the regressions of eye velocity on head velocity are essentially identical whether the target was switched off (
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VERTICAL CANAL INPUT.
The role of the vertical canals in the recovery of horizontal
counterrotation was investigated by plugging them in monkey HC1, the horizontal canals of which had been plugged 110 days earlier and which already had recovered some eye counterrotation. The
day after we had plugged its remaining vertical canals, both the
passive HVOR and VVOR were reduced dramatically either with the nose
22° down or with the head in the stereotaxic position. Immediately
after vertical canal plugging, counterrotation gain 80 ms after the
saccade was reduced to 0.51 ± 0.02 based on 225 gaze shifts (Fig.
6, A and B, ),
and it ranged from 0.39 ± 0.02 to 0.59 ± 0.03 at 40 and 100 ms, respectively, after the eye saccade. Forty-seven days after
vertical canal plugging, horizontal counterrotation gains had improved
somewhat to 0.61 at 80 ms and to 0.41 ± 0.02 and 0.72 ± 0.02 at 40 and 100 ms, respectively, after the eye saccade (not shown).
Indeed counterrotation gains had almost returned to those seen with
only the horizontal canals plugged. Clearly other nonvestibular
mechanisms must contribute to the control of counterrotation.
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SOMATOSENSORY FEEDBACK.
One possible source of sensory information during eye counterrotation
is the afferent signal from cervical joint and neck muscle afferents.
We assessed the contribution of these sensory signals in two ways.
First, eye movements during trunk rotation under a stationary head
(i.e., the cervicoocular reflex, COR) were measured in all three
animals before and after canal plugging. The gain of the COR was not
consistent between animals, ranging from 0.17 to 0.35. Eye rotations
moved in phase with trunk rotation in all three animals. Over the
course of 50 days, two of the three monkeys exhibited a slight
increase in COR gain (Fig.
7A). Similar changes were seen
across all tested frequencies (0.1-1.0 Hz) of trunk rotation (Fig.
7B). Although such an improved COR would provide
compensatory eye counterrotation during gaze shifts with the head
unrestrained, COR recovery cannot explain a gradual recovery of
counterrotation in monkey AC because he exhibited none.
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EFFECT OF HEAD STOPPAGE ON COUNTERROTATION. A more direct measure of the contribution of any sensory signal to the counterrotation is to perturb the ongoing head movement and observe changes in eye counterrotation. We engaged an electromagnetic brake on some trials of monkey AC and a few trials in monkey HC2 to arrest the head movement completely in midflight. The time between the start of the eye saccade and the application of the brake was varied to produce arrests of the head movement during all portions of eye counterrotation. In all, hundreds of brakes were applied at various times during counterrotation. In none of these cases did application of the brake during counterrotation stop it. Small, transient perturbations in counterrotation, consisting of a brief deceleration and reacceleration, were noticeable, but they did not significantly alter the overall trajectory of the observed eye movement. We assume that they reflect a small influence of sensory signals from the neck or otolith organs. Despite stoppage of the head movement, eye counterrotation continued as is shown in Fig. 8.
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Termination of gaze shifts
By definition, the gaze movements ended when counterrotation gain reached 1.0. In our experiments, the interval between the end of the eye saccade and the end of the gaze shift, i.e., the duration of reduced gain counterrotation, increased immediately after plugging when counterrotation gain was low and shortened as counterrotation gain recovered (Fig. 9). However, the recovery of counterrotation gain to less than unity cannot account for the shortening. Part of the shortening can be attributed to a decrease of head movement duration, particularly in monkey HC1. However, the bulk of the remaining shortening must be due to a return of counterrotation gain to one, allowing termination of the gaze movement before termination of the head movement. We now consider the timing of the return of this fully compensatory counterrotation and whether head velocity and orbital eye position are instrumental in producing it.
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HEAD VELOCITY.
For a gaze movement to end before the head stops rotating, eye
counterrotation must match head velocity. To determine the head
velocities at which the gaze shift was terminated, we used gaze shifts
with a substantial head movement of 20°. The amplitudes of these
gaze shifts ranged from 40 to 80°.
ORBITAL POSITION.
Because the eye position at the end of the saccadic eye movement is
eccentric (Freedman and Sparks 1997), we considered the possibility that passive orbital properties contribute to the counterrotation from these eccentric orbital positions. To test this,
we compared head fixed saccades of 0-30° with the horizontal head-unrestrained gaze shifts. We found that in canal plugged animals
with the head fixed, there are small amplitude (generally <3°) and low peak velocity (generally <30°/s) postsaccadic
drifts back toward the origin of the saccade (Fig.
10C). The amplitude and
velocity of this drift are much smaller than those seen in the
horizontally head-unrestrained gaze shift counterrotations (Fig. 10,
A and B).
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DISCUSSION |
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The most striking finding of our study is the persistence of the eye counterrotation despite the absence of inputs from the semicircular canals. After only the horizontal canals were plugged in two monkeys, counterrotations already were present on the first test day after surgery. Furthermore, counterrotation gain increased with time to reach values between 0.51 and 0.75 (Fig. 3). After all canals were plugged in monkey AC, counterrotation gain initially dropped to zero; however, in only 2 or 3 days, counterrotations again were visible. In time, counterrotation gain in this monkey also improved to as much as 0.67.
In this DISCUSSION, we will consider the characteristics of the early, postplugging counterrotation, how the counterrotations improved with time, what mechanisms contributed to this recovery, and why a recovery of counterrotation is desirable for the task of shifting the direction of gaze. But first, we need to consider whether the canals indeed were inactivated functionally and whether they remained inactivated as counterrotation gain increased.
Our canal plugging eliminated the passive VOR
We are confident that our surgical intervention successfully
plugged the canals because passive yaw rotation in all three animals
and pitch rotation in the animal with all canals plugged produced
horizontal and vertical VOR gains of <0.07 at frequencies between 0.1 and 1.0 Hz (Fig. 4). However, it is still possible that the natural
head rotations produced in our behavioral situation consist of
frequency components that are higher than those we could test with our
passive vestibular stimulator and that those frequencies were spared
after canal plugging. Indeed, after the canals of the toadfish are
plugged, primary afferents still respond normally to 10-Hz rotations
(Rabbitt et al. 1999). Because the radius of the
horizontal canal in the rhesus monkey is smaller than that of the
toadfish (compare Blanks et al. 1985 with Rabbitt et al. 1999), one might expect a significant VOR in
canal-plugged rhesus monkeys at frequencies of ~5 Hz. A very recent
study published after our paper was accepted has shown that this is
indeed the case (Yakushin et al. 1998
). Because our
apparatus could produce yaw rotations at a maximum of only 1.0 Hz, we
could not test the passive VOR at this frequency in our animals.
To test whether the head movements of our monkeys had substantial high-frequency components that might account for the postplugging counterrotations, we performed a FFT on the averaged head movement in monkey AC 107 days after all his canals were plugged. This animal had relatively high velocity head movements after plugging and a robust counterrotation. We found that 99% of the energy of the head movement is at frequencies <3 Hz, suggesting that canal plugging is effective at the frequencies present in this task. Certainly if the plugged canals were still participating in the counterrotation, we would expect that stoppage of the head would halt the counterrotation but, as we saw in Fig. 8, this was not the case.
Counterrotation is related to head velocity
If our plugging was indeed effective, then eye counterrotation during natural gaze shifts in a lighted room must be coming from sources other than the peripheral vestibular apparatus. The first question, therefore, is whether the counterrotation is related to head movement at all or is just a "ballistic" return of eye position in the orbit. Figures 2 and 4 show that counterrotation velocity indeed exhibits a monotonic, even linear, increase with head velocity in monkeys HC1 and HC2 when measured at 80 ms after the end of the rapid gaze shift. Indeed there is a linear relation (average correlation coefficient = 0.8) between eye and head velocity at all times between 40 and 100 ms after the eye saccade is over. Finally a linear relation is a good description of counterrotation gain from just after the canal-plugging surgery until as long as the counterrotation was measured (from 71 to 110 days).
For monkey AC, the slope of the eye versus head velocity ratio begins at zero on the day after the surgery (Fig. 2). However, when counterrotations begin to appear, as soon as day 2 or 3, eye velocity is seen to increase monotonically with head velocity and a straight line fits the data quite well.
Now that we have satisfied ourselves that eye counterrotation velocity is dependent on head velocity even though there is no canal input, we ask how a counterrotation related to head velocity could be generated. For animals with only horizontal canals plugged, the possibilities included smooth eye movements caused by movement of the target spot on the retina, contributions from the intact vertical canals and eye movements generated by stimulation of the neck receptors. Here it also would be useful to consider whether eye movements attributable to any of these possible sources changed in parallel with the gradual improvement in counterrotation gain with time (Fig. 3).
Possible sources of eye counterrotation after canal plugging
VISUALLY ELICITED PURSUIT MOVEMENTS. Counterrotation gain was unaffected by whether the target light remained on or whether it was extinguished at the onset of the rapid gaze shift in the two animals tested (Fig. 4). This suggests that retinal slip cannot be solely responsible for driving the eye counterrotation.
CONTRIBUTION OF THE VERTICAL CANALS AFTER HORIZONTAL CANAL
PLUGGING.
In both animals with plugged horizontal canals, HVOR gain increased
with time after plugging. This recovery was seen even when the head was
tipped to align the horizontal canals with earth horizontal. This HVOR
recovery after plugging of the horizontal semicircular canals could
depend on signals from the vertical semicircular canals, which would be
sensitive to horizontal rotation even with the nose pitched down by
22° (Angelaki and Hess 1996). When the head is
completely free, the animal might choose to move its head so as to
maximize the vertical canal signal. Unfortunately, we could not test
this possibility as our animals were constrained to make horizontal
gaze shifts about a vertical axis.
INPUTS FROM NECK ACTIVATION. We investigated the role of cervical somatosensory pathways in counterrotation recovery in two ways: the COR was tested in all three monkeys and restricted dorsal roots were transected in one monkey.
The cervicoocular reflex was quite variable from trial to trial in a particular monkey and from one monkey to another. For example, both animals with only their horizontal canals plugged exhibited a long-term increase in COR gain, but the animal with all canals plugged showed a slight decrease in gain (Fig. 7). Furthermore, the animal (HC1) who underwent plugging of the vertical canals after the horizontal canals already had been plugged for 110 days, showed an increase in gain unlike the steady gain or slight decrease exhibited by monkey AC. Because eye rotations when the body was rotated under a stationary head moved in phase with the trunk rotation in all three animals, the COR, if it were consistent, would provide compensatory counterrotations for gaze shifts with the head unrestrained. Others have suggested that the COR helps substitute for the loss of vestibular inputs in labyrinthine-defective subjects. In monkeys, 3 mo after labyrinthectomy, the COR gain has increased from a value near 0 to ~0.3 (Dichgans et al. 1973Efference copy of head velocity?
The experiments in which we arrested the head movement in
midflight provide perhaps the most diagnostic test to evaluate
"sensory substitution" as a mechanism to compensate for the loss
of the vestibular input. Sudden stoppage of the head with the
electromechanical brake eliminated any sensory cue of head motion,
whether it was provided by a residual labyrinthine, somatosensory, or
visual signal. After head motion was stopped, the recovered
counterrotation persisted as was seen in Fig. 8, suggesting that an
internal copy of the intended head movement, i.e., an "efference
copy," is responsible for driving eye counterrotation. Others have
reported similar results in bilaterally labyrinthectomized monkeys
(Dichgans et al. 1973).
Because we previously had observed changes in counterrrotation after both cervical rhizotomy and vertical canal plugging, it is surprising that counterrotation continues when both those signals are altered during head perturbations. This finding seems to suggest that vertical canal signals and information from the neck are not used on-line to drive the counterrotation. Instead they seem to be important in setting the gain of the counterrotation based on errors in individual trials.
Our data allow us to suggest the nature of the efference copy signal. According to Fig. 3, the efference copy mechanism makes a low, constant gain, estimate of head velocity in the interval between 40 and 100 ms after the rapid eye component of the gaze shift ends. Sometime after 100 ms, the gaze movement ends. The gaze shift ends and the eye remains stable in space because counterrotation gain must have increased to 1.0. Counterrotation gain increases to 1.0 to end the gaze shift when the head is moving at relatively low velocities (Fig. 9). This pattern of a counterrotation gain that initially is low between 40 to 100 ms after the eye saccade (Fig. 3) and then later jumps to 1.0 at low head velocities is quite consistent from trial to trial in the same session for gaze shifts up to 80° in amplitude and peak head velocities as high as 300°/s. Although one animal did exhibit high-velocity counterrotations during the first and second weeks of recovery, the counterrotations did not match head velocity and therefore did not enhance gaze accuracy. This animal gradually abandoned these movements for a pattern like that described above (i.e., an initial constant gain of <1.0 followed by a gain of 1.0).
There are two reliable changes that occur with time after canal plugging. First, the low counterrotation gain in the first 100 ms after the eye saccade increases (Fig. 3). Second, there is a parallel increase in the head velocity at the end of the gaze shift (Fig. 9). If the time course of head velocity is relatively unaffected by adaptation, the second change could cause a decrease in the duration of the gaze shift (Fig. 9) by allowing the gaze shift to end earlier (i.e., at higher velocities) in the head trajectory. But why is there also a modest increase in counterrotation gain to ~0.6 when any gain <1.0 is inadequate to terminate the gaze shift?
We suggest that the two changes are interrelated. The gaze shift ends when counterrotation gain is "switched" to 1.0. Perhaps, this switch can be activated only after gaze velocities have been reduced to a certain low level. Low gaze velocities could be reached either by waiting until head velocities decay to a low level (which occurs early after canal plugging) or by increasing eye counterrotation gain (which occurs with time after canal plugging). Once low gaze velocity has been reached, a final estimate of the required eye counterrotation velocity can be made more accurately, and the gaze shift can be terminated. Therefore increasing counterrotation gain even to values <1.0, can hasten the end of the gaze shift, if the mechanism that halts the gaze shift is engaged only after a relatively low gaze velocity is attained.
There never is complete compensation for the loss of semicircular canal
input. The duration of the gaze shift remains long and the variability
of the gaze shift remains greater than normal. Thus recovery in this
system is limited, like other forms of plasticity in the
vestibulooculomotor system such as VOR recovery after labyrinthectomy (Fetter and Zee 1988, Maioli et al.
1983
), VOR gain plasticity (Angelaki and Hess
1998
; Miles and Fuller 1974
), and saccade
adaptation (Straube et al. 1997
).
The neural substrate of the counterrotation mechanisms remains unknown.
In three recent models of gaze control, a head velocity signal arises
from hypothetical head burst neurons (Phillips et al. 1995), from spinal afferents (Munoz and Guitton
1991
), or is unspecified (Galiana and Guitton
1992
). Where this head velocity signal might influence eye
movement also is a matter for speculation. Presumably, it may act
through the vestibular nucleus as does the semicircular canal input.
Indeed evidence in our lab and others (McCrea et al.
1996
; Phillips et al. 1996
; Roy and
Cullen 1998
) suggests that the discharge of possible VOR
interneurons is shifted away from head velocity during
head-unrestrained gaze shifts. Future experiments involving neural
recording in the vestibular nucleus during canal plugged gaze shifts
will be needed to resolve this issue.
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ACKNOWLEDGMENTS |
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We thank Dr. Michel Kliot of the Department of Neurological Surgery for performing the dorsal rhizotomy. We are grateful for the excellent support of the veterinary staff at the Regional Primate Research Center and for the superb editorial assistance of K. Elias.
This research was supported by National Institutes of Health Grants EY-00745 and RR-00166.
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FOOTNOTES |
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Address for reprint requests: S. D. Newlands, University of Mississippi Medical Center, Dept. of Surgery (Otolaryngology), 2500 N. State St., Jackson, MS 39212.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 28 September 1998; accepted in final form 27 January 1999.
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REFERENCES |
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