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The Journal of Neurophysiology Vol. 87 No. 5 May 2002, pp. 2337-2357
Copyright ©2002 by the American Physiological Society
Aerospace Medical Research Unit, Department of Physiology, McGill University, Montreal, Quebec H3G 1Y6, Canada
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ABSTRACT |
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Roy, Jefferson E. and Kathleen E. Cullen. Vestibuloocular Reflex Signal Modulation During Voluntary and Passive Head Movements. J. Neurophysiol. 87: 2337-2357, 2002. The vestibuloocular reflex (VOR) effectively stabilizes the visual world on the retina over the wide range of head movements generated during daily activities by producing an eye movement of equal and opposite amplitude to the motion of the head. Although an intact VOR is essential for stabilizing gaze during walking and running, it can be counterproductive during certain voluntary behaviors. For example, primates use rapid coordinated movements of the eyes and head (gaze shifts) to redirect the visual axis from one target of interest to another. During these self-generated head movements, a fully functional VOR would generate an eye-movement command in the direction opposite to that of the intended shift in gaze. Here, we have investigated how the VOR pathways process vestibular information across a wide range of behaviors in which head movements were either externally applied and/or self-generated and in which the gaze goal was systematically varied (i.e., stabilize vs. redirect). VOR interneurons [i.e., type I position-vestibular-pause (PVP) neurons] were characterized during head-restrained passive whole-body rotation, passive head-on-body rotation, active eye-head gaze shifts, active eye-head gaze pursuit, self-generated whole-body motion, and active head-on-body motion made while the monkey was passively rotated. We found that regardless of the stimulation condition, type I PVP neuron responses to head motion were comparable whenever the monkey stabilized its gaze. In contrast, whenever the monkey redirected its gaze, type I PVP neurons were significantly less responsive to head velocity. We also performed a comparable analysis of type II PVP neurons, which are likely to contribute indirectly to the VOR, and found that they generally behaved in a quantitatively similar manner. Thus our findings support the hypothesis that the activity of the VOR pathways is reduced "on-line" whenever the current behavioral goal is to redirect gaze. By characterizing neuronal responses during a variety of experimental conditions, we were also able to determine which inputs contribute to the differential processing of head-velocity information by PVP neurons. We show that neither neck proprioceptive inputs, an efference copy of neck motor commands nor the monkey's knowledge of its self-motion influence the activity of PVP neurons per se. Rather we propose that efference copies of oculomotor/gaze commands are responsible for the behaviorally dependent modulation of PVP neurons (and by extension for modulation of the status of the VOR) during gaze redirection.
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INTRODUCTION |
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The vestibular system
is classically associated with detecting the motion of the
head-in-space to generate the reflexes that are
crucial for our daily activities, such as stabilizing gaze (gaze = eye-in-head + head-in-space) via the vestibuloocular reflex (VOR)
during walking and running (Grossman et al. 1988
, 1989
). During passive whole-body rotation in head-restrained animals, vestibular afferents originating in the semicircular canals encode the
angular velocity of the head-in-space (Goldberg and Fernandez 1971
). These vestibular afferents, in turn, project to
second-order neurons within the vestibular nuclei, which encode angular
head velocity during the compensatory eye movements generated by the VOR (Cullen and McCrea 1993
; McCrea et al.
1987
; Scudder and Fuchs 1992
). However, in
addition to input from the vestibular nerve, the vestibular nuclei
receive projections from many structures that could influence their
discharge. For example, neurons within oculomotor/gaze control
pathways, such as the saccadic burst neurons in the paramedian pontine
reticular formation, send direct projections to the vestibular nuclei
(Sasaki and Shimazu 1981
). Furthermore, neck
muscle spindle afferents are known to influence the activity of
vestibular nuclei neurons in decerebrate animals (Anastasopoulos and Mergner 1982
; Boyle and Pompeiano 1981
;
Fuller 1988
; Wilson et al. 1990
) via a
disynaptic pathway (Sato et al. 1997
). Moreover, cortical areas, which have been implicated in more cognitive aspects of
vestibular function including the perception of spatial orientation, the ability to navigate (in the absence of visual cues), and gaze control, project to the vestibular nuclei (for review, see
Fukushima 1997
). Thus given the convergence of multiple
inputs to the vestibular nuclei, it is natural to ask how the signals
carried by these inputs are integrated during our daily activities.
Here we have focused on the behavior of a distinct population of
vestibular nuclei neurons termed position-vestibular-pause (PVP)
neurons during horizontal head rotations. Type I PVP neurons are
thought to constitute most of the intermediate leg of the direct VOR
pathway; they receive a strong monosynaptic connection from the
ipsilateral semicircular canal afferents and, in turn, project directly
to the extraocular motoneurons (Cullen and McCrea 1993
; McCrea et al. 1987
; Scudder and
Fuchs 1992
). These neurons derive their name from the signals
they carry during head-restrained oculomotor and vestibular paradigms:
their firing rates increase when the eyes move to more contralaterally
directed positions; during slow phase vestibular
nystagmus, these neurons are sensitive to ipsilateral head rotations
(i.e., a type I response); and their discharges cease
(pause) for ipsilaterally directed saccades and vestibular
quick phases. Type II PVP neurons have oppositely directed eye- and
head-motion sensitivities to those of type I PVP neurons, and their
role in the processing of vestibular information is less well
understood. Nevertheless, in general, they behave in a quantitatively
similar manner to type I PVP neurons during head-restrained rotations
and eye movements (Scudder and Fuchs 1992
).
The first goal of this study was to address the general question of whether the PVP neuron responses to active and/or passive movements are modified in a manner that depends on the animal's current behavioral goal. For example, the response of PVP neurons might be selectively attenuated for gaze redirection versus stabilization, consistent with their role in mediating the VOR. Alternatively, it is also possible that PVP neurons might differentially encode head velocity during self-generated versus passively applied head-in-space rotations and/or during rotation of the head and body together in space versus rotation of the head relative to an earth-stationary body.
On the one hand, there is already much evidence to suggest that type I
PVP neurons differentially encode head-velocity during gaze redirection
versus gaze stabilization. First, while type I PVP neurons encode head
velocity during the compensatory slow phase component of the VOR evoked
by passive whole-body rotation, they pause or cease firing during
vestibular quick phases where gaze is redirected (Cullen and
McCrea 1993
; Fuchs and Kimm 1975
; Keller
and Daniels 1975
; Keller and Kamath 1975
;
Lisberger et al. 1994a
,b
; McConville et al.
1996
; McCrea et al. 1987
; Miles 1975
; Roy and Cullen 1998
; Scudder and
Fuchs 1992
; Tomlinson and Robinson 1984
).
Second, when gaze is voluntarily redirected using coordinated eye-head
gaze shifts, the head-velocity signal carried by type I PVP neurons is
significantly attenuated as compared with passive whole-body rotation
(Cullen and McCrea 1993
; McCrea et al.
1996
; Roy and Cullen 1998
) in an
amplitude-dependent manner (Roy and Cullen 1998
). Third,
type I PVP neuron responses are attenuated by ~30% as compared with
passive rotation in the dark when monkeys suppress their VOR (and
therefore redirect their gaze to move with the head in space) during
passive whole-body rotation by tracking a target that moves with the
head (Cullen and McCrea 1993
; McCrea et al.
1996
; Roy and Cullen 1998
; Scudder and
Fuchs 1992
).
On the other hand, whether PVP neurons differentially encode
head-velocity during self-generated versus passively applied rotations
of the head-in-space is less clear. It has been proposed that an
enhanced sensitivity of the VOR pathways during active head movements
might increase VOR responses in humans as compared with passive head
motion when the goal is to stabilize gaze (Demer et al.
1993
; Jell et al. 1988
). However, this
behavioral observation remains to be confirmed at the neural level. We
have previously shown (Roy and Cullen 1998
) that type I
PVP neuron discharges in the rhesus monkey are similar during the VOR
elicited by passive whole-body rotation and during the active head
movements made in the time interval that immediately follows a gaze
shift. In this interval, an ocular counter roll compensates for the
residual active head motion such that the monkey's axis of gaze is
stable relative to space. Gdowski and McCrea (1999)
also
reported that the majority of PVP neurons in squirrel monkeys encode
head-in-space motion during simultaneous active and passive head
motion. However, they emphasized that 35% of the neurons were better
related to the passive component of the motion than to the total
head-in-space motion during this same paradigm. While this latter
result is actually the opposite of what would be expected if the
efficacy of the VOR was, in fact, enhanced during active head
movements, its interpretation is limited given that the gaze goal of
the monkeys was not reported.
The second goal of the present study was to determine the neural
mechanism(s) that contribute to the differential processing of
head-velocity information by PVP neurons. For example, during gaze
shifts, there are several possible mechanisms that could modulate PVP
neuron discharges. It is likely that inputs from the brain stem
saccadic burst generator to the vestibular nuclei could function to
suppress PVP neuron responses during voluntary combined eye-head gaze
shifts (Roy and Cullen 1998
). Specifically, burst
neurons in the paramedian pontine reticular formation project to type
II neurons in the vestibular nucleus (Sasaki and Shimazu 1981
), which in turn send an inhibitory projection to type I
PVP neurons (Nakao et al. 1982
). This pathway almost
certainly provides a powerful inhibitory drive to type I PVP neurons
during rapid gaze shifts. It is also possible that inhibitory inputs
from neck proprioceptors contribute to the attenuation of PVP neuron
discharges. Studies in anesthetized animals have shown that the
activation of neck proprioceptors can influence the activity of
vestibular nuclei neurons (Anastasopoulos and Mergner
1982
; Boyle and Pompeiano 1981
; Fuller
1988
; Wilson et al. 1990
). Furthermore, McCrea
and colleagues recently reported that most if not all secondary
vestibular neurons (including type I PVP neurons) in squirrel monkey
are sensitive to passive neck rotation (Gdowski and McCrea 1999
,
2000
; McCrea et al. 1996
). Finally, a signal
related to the voluntary head motion itself, such as an efferent copy
of the motor command to the neck musculature (McCrea et al.
1996
) or a cortically derived signal representing the monkey's
self-generated head motion, could influence the responses of PVP neurons.
To determine how PVP neurons process head-velocity information across a wide variety of behaviors and to understand the mechanisms that underlie the observed differential processing, we devised a sequence of paradigms in which the gaze goal was systematically varied for externally applied and/or self-generated head movements. We first characterized the discharges of PVP neurons in the head-restrained condition during passive whole-body rotation when gaze was stable (VOR) and when gaze was redirected (VOR cancellation paradigm). The neuronal discharges were then recorded during different gaze control tasks while the monkey experienced passive rotations of its head-on-body, generated voluntary head-on-body movements to orient to novel targets or track a slowly moving target, was passively rotated while simultaneously generating active head movements, and voluntarily "drove" its head and body together relative to space. We found that, during active and/or passive head movements, type I PVP neurons robustly encoded head velocity whenever monkeys stabilized their gaze relative to space, and were similarly attenuated during gaze-redirection tasks. Furthermore, the responses of type II PVP neurons were quantitatively comparable to those of type I PVP neurons during most behavioral conditions. Our results support the hypothesis that an efference copy of the brain stem oculomotor/gaze commands to redirect the visual axis in space underlies the "on-line" reduction in VOR pathway modulation when the VOR is functionally inappropriate.
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METHODS |
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Three rhesus monkeys (Macaca mulatta) were prepared for chronic extracellular recording using aseptic surgical techniques. All experimental protocols were approved by the McGill University Animal Care Committee and were in compliance with the guidelines of the Canadian Council on Animal Care.
Surgical procedures
The surgical techniques were similar to those previously
described by Roy and Cullen (2001)
. Briefly, an 18- to
19-mm-diam eye coil (3 loops of Teflon-coated stainless steel wire) was
implanted in the right eye behind the conjunctiva. In addition, a
dental acrylic implant was fastened to each animal's skull using
stainless steel screws. The implant held in place a stainless steel
post used to restrain the animal's head, and a stainless steel
recording chamber that was positioned to access the medial vestibular
nucleus (posterior and lateral angles of 30°). During the surgery
isoflurane gas was utilized to initiate (2-3%) and maintain
(0.8-1.5%) anesthesia. After the surgery, buprenorphine (0.01 mg/kg
im) was utilized for postoperative analgesia, and monkeys were allowed
to recover for 2 wk before commencing experimental sessions.
Data acquisition
At the onset of each experiment, the monkey sat comfortably in a
primate chair, which was placed on a vestibular turntable. With the
monkey initially head-restrained, extracellular single-unit activity
was recorded using enamel-insulated tungsten microelectrodes (7-10
M
impedance, Frederick-Haer) as has been described elsewhere (Roy and Cullen 2001
). The abducens nucleus, which was
identified based on its stereotypical discharge patterns during eye
movements (Cullen et al. 1993
; Sylvestre and
Cullen 1999
), was located and used as a landmark to determine
the location of the medial and lateral vestibular nuclei. Gaze and head
position were measured using the magnetic search coil technique
(Fuchs and Robinson 1966
), and turntable velocity was
measured using an angular velocity sensor (Watson). Unit activity,
horizontal and vertical gaze and head positions, target position, and
table velocity were recorded on DAT tape for later playback. Action
potentials were discriminated during playback using a windowing circuit
(BAK) that was manually set to generate a pulse coincident with the
rising phase of each action potential. Gaze position, head
position, target position, and table velocity signals were
low-pass filtered at 250 Hz (8 pole Bessel filter) and sampled at 1,000 Hz.
Behavioral paradigms
Using juice as a reward, monkeys were trained to follow a target
light (HeNe laser) that was projected, via a system of two galvanometer
controlled mirrors, onto a cylindrical screen located 60 cm away from
the monkey's head. Eye-motion sensitivities to saccades and ocular
fixation were characterized by having the head-restrained monkey attend
to a target that stepped between horizontal positions over a range of
±30°. To determine neuronal eye-motion sensitivities during smooth
pursuit, head-restrained monkeys tracked sinusoidal (0.5 Hz, 80°/s
peak velocity) target motion in the horizontal plane. Head-velocity
sensitivities to passive whole body rotation (0.5 Hz, 80°/s peak
velocity) were tested by rotating monkeys about an earth vertical axis
in the dark [passive whole-body rotation (pWBR)] and while they
cancelled their VOR by fixating a target that moved with the vestibular turntable (pWBRc). Target and turntable motion, and on-line data displays were controlled by a UNIX-based real-time data-acquisition system (REX) (Hayes et al. 1982
).
After a neuron was fully characterized in the head-restrained condition, the monkey's head was slowly and carefully released to maintain isolation. Once released, the monkey was able to rotate its head through the natural range of motion in the yaw (horizontal), pitch (vertical), and roll (torsional) axes. The response of the same neuron was then recorded during the voluntary head movements made during combined eye-head gaze shifts (15-65° in amplitude) and during combined eye-head gaze pursuit of a sinusoidal target (0.5 Hz, 80°/s peak velocity). In addition, neuronal responses to combined passive and active head motion were recorded while head-unrestrained monkeys were passively rotated (0.5 Hz., 80°/s peak) and allowed to simultaneously generate voluntary head-on-body movements. A subset of neurons was tested during a "driving paradigm" in which the monkey moved its head and body together in space. During this paradigm, head-restrained monkeys manually manipulated a steering wheel to control the initiation of the movement as well as the rotational velocity of the turntable on which they were seated. The goal of the monkey was to align a chair mounted target with a moving laser target.
Finally, the influences of dynamic and static neck proprioceptive inputs on neural discharges were investigated. Two different paradigms were used to dynamically activate the neck afferents. First, the experimenter manually rotated the monkey's head to induce rapid motion of the head relative to a stationary body. Second, the monkey's head was held stationary relative to the earth while its body was passively rotated at 0.1, 0.2, 0.5, 1, 1.5, and 2 Hz at 20°/s peak velocity and 0.2, 0.5, 1, 1.5, and 2 Hz at 40°/s peak velocity. The gain of the cervicoocular reflex induced during the rotations was calculated as the resultant desaccaded eye velocity divided by the turntable velocity. To test for the influence of static neck afferent activation, the monkey's body was held at different static positions relative to its earth-stationary head, and the mean firing rate was calculated. During this testing, the torque produced by the monkey against the head-restraint was measured using a reaction torque transducer (Sensotec).
Analysis of neuron discharges
Before analysis, recorded gaze and head-position signals were
digitally filtered at 125 Hz. Eye position was calculated from the
difference between gaze and head-position signals. Gaze, eye, and
head-position signals were digitally differentiated to produce velocity
signals. The neural discharge was represented using a spike density
function in which a Gaussian function was convolved with the spike
train (SD of 5 ms for saccades and gaze shifts and 10 ms for remainder
of the paradigms) (Cullen et al. 1996
). Saccade and gaze
shift onsets and offsets were defined using a ±20°/s gaze velocity
criterion. Subsequent analysis was performed using custom algorithms
(Matlab, Mathworks).
To quantify a neuron's response to eye movement, we analyzed periods
of steady fixation to obtain a resting discharge (bias, sp/s) and an
eye-position sensitivity [kx,
(sp/s)/°] and periods of saccade-free smooth pursuit to obtain a
resting discharge (bias, sp/s), an eye-position sensitivity
[ksp, (sp/s)/°], and an
eye-velocity sensitivity [rsp,
(sp/s)/(°/s)] using a multiple regression analysis (Roy and
Cullen 1998
). Spike trains were assessed to determine whether
neurons paused or burst during saccades. In cases where neurons did
burst, the resting discharge (bias, sp/s), eye position [ksac, (sp/s)/°] and eye velocity
[rsac, (sp/s)/(°/s)] sensitivities were also estimated during saccades.
A least-squared regression analysis was then used to determine each
neuron's phase shift relative to head velocity, resting discharge
(bias, sp/s), and head velocity
[gpWBR (sp/s)/°/s] during pWBR and
pWBRc. Only unit data from periods of slow-phase vestibular nystagmus
during pWBR or steady fixation during pWBRc that occurred between quick
phases of vestibular nystagmus and/or saccades were included in the
analysis. A least-squared regression analysis was applied to neuronal
discharges during active head-on-body motion, active head and body
motion (driving paradigm), combined passive and active head motion,
passive head-on-body rotations, and passive body-under-head rotations.
The models utilized for each condition are described in
RESULTS. To quantify the ability of the linear regression
analysis to model neuronal discharges, the variance-accounted-for (VAF)
provided by each regression equation was determined. The VAF was
computed as {1 - [var(est
fr)/var(fr)]}, where est represents
the modeled firing rate (i.e., regression equation estimate) and fr
represents the actual firing rate. Note that only data for which the
firing rate was greater than zero were included in the optimization.
Statistical significance was determined using paired Student's
t-tests.
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RESULTS |
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The firing behaviors of two distinct classes of vestibular nuclei neurons are presented in the following text. First, we describe the responses of type I PVP neurons during a sequence of paradigms in which the gaze goal was systematically varied and the head movements were externally applied and/or self-generated. We then describe the responses of type II PVP neurons whose head and eye-velocity sensitivities in the head-restrained condition were opposite to those of type I PVP neurons, during each of the same conditions.
Type I PVP neurons
HEAD-RESTRAINED CHARACTERIZATION.
The type I PVP neuron illustrated in Fig.
1 is typical of our
sample (n = 24) in that its firing rate increased for
contralaterally directed eye positions during spontaneous eye movements
(Fig. 1A, see inset), and its firing rate phase
lagged contralaterally directed eye velocity and led contralaterally
directed eye position during smooth pursuit (Fig. 1B).
During pWBR (Fig. 1C) the neuron increased its firing rate
in response to ipsilateral head motion (i.e., a type I response). In
addition, each type I PVP neuron stopped firing or "paused" during
ipsilaterally directed saccades and vestibular nystagmus quick phases
(vertical arrows in Fig. 1, A and C). Thus the
type I PVP neurons in our sample were comparable to those that have
been described in previous reports (Cullen and McCrea
1993
; Fuchs and Kimm 1975
; Keller and
Daniels 1975
; Keller and Kamath 1975
; Roy
and Cullen 1998
; Scudder and Fuchs 1992
). We
also utilized a second pWBR paradigm in which the monkey cancelled its
VOR by fixating a head-centered visual target that moved with the
vestibular turntable (pWBRc; Fig. 1D). This VOR cancellation
paradigm has been used extensively to dissociate a neuron's vestibular
sensitivity from its eye-movement related modulation. As can be seen in
Fig. 1D, type I PVP neurons remained well modulated in
response to ipsilateral head velocity during this paradigm.
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VOLUNTARY HEAD-ON-BODY MOTION. Rapid gaze redirection. After the head-restrained characterization had been completed, the monkey's head was slowly released to allow a wide range of motion in all three axes (yaw, pitch, and roll). Unit activity was carefully monitored during the transition from the head-restrained to head-unrestrained condition to ensure that neurons remained isolated and undamaged.
The firing rate of each type I PVP neuron was then recorded during voluntary combined eye-head gaze shifts. For analysis, ipsilaterally directed gaze shifts (i.e., gaze shifts for which the head motion was in the neuron's "on direction") were sorted by amplitude into five separate data sets, each spanning 10° and ranging from 15 to 65°. In agreement with what we have previously shown (Roy and Cullen 1998
0.97 ± 0.47). We
have previously argued that the addition of an eye-velocity term to the
model would dramatically improve our ability to describe type I PVP neuron activity during gaze shifts (Roy and Cullen
1998
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head velocity) and Estimate 2 was used whenever gaze
velocity
0.
Type I PVP neuron activity was also characterized during
contralaterally directed gaze shifts (i.e., off direction of the neuron's head-velocity sensitivity). The majority of neurons (96%) did not pause during contralaterally directed head-restrained saccades
of all amplitudes (Fig. 3A).
The same neurons also did not pause or burst for small contralaterally
directed gaze shifts <35° (Fig. 3B, left). As
shown in Fig. 3B (left), the pWBR model superimposed well on the neuronal discharges for small gaze shifts. However, for larger-amplitude gaze shifts, the pWBR model described the
activity only until the neuronal discharges were driven to inhibition
as a result of the head velocity becoming sufficiently large (Fig.
3B, right). Accordingly, we found that whether a
neuron's firing rate was driven to zero during a gaze shift depended
on the balance between the bias and the head-velocity sensitivity of
the individual neuron. In general, head velocities were large enough to
drive the firing rate to zero for gaze shifts >35° in amplitude.
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Do type I PVP neurons differentially encode head velocity during self-generated vs. passively applied rotations of the head-in-space?
Both gaze shifts and gaze pursuit involve the voluntary movement
of the head on the body. To determine whether type I PVP neurons might
differentially encode head-velocity during self-generated versus
passively applied rotations of the head-in-space, we used a paradigm in
which head-restrained monkeys voluntarily drove or controlled the
direction and rotation velocity of the turntable, thus moving both
their heads and bodies together in space. The monkeys were trained to
align a turntable mounted laser target (Ttable) with a computer controlled
target (Tgoal; Fig.
5A, see schema), which either
stepped from one location to another or moved sinusoidally. The data
traces shown in Fig. 5A illustrate the discharge activity of
an example type I PVP neuron during the two behavioral tasks. When the
monkey redirected its gaze ipsilaterally to align the turntable with a
target that stepped (Fig. 5A; middle,
), the
pWBR model over-predicted the discharge of the neuron (pWBR model,
thick trace). Indeed, for the neurons tested (n = 8),
the estimated head-velocity sensitivity was significantly attenuated
relative to pWBR to a level comparable to that observed during gaze
shifts [Estimate 2 mean normalized
gest = 0.18 ± 0.21 (sp/s)/(°/s);
Fig. 5B,
]. Similarly, when the monkey pursued the
target (Fig. 5A; right), the pWBR model
overpredicted the discharge of the neuron (pWBR model, thick trace),
and the estimated head-velocity sensitivity was significantly reduced
relative to pWBR [Estimate 2 mean normalized
gest = 0.64 ± 0.04 (sp/s)/(°/s); Fig. 5B,
]. This attenuation was
comparable to that described for gaze pursuit and pWBRc above
(P > 0.7 and > 0.27, respectively).
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In contrast, in the intervals where the monkey had acquired the new
target, but the turntable was still moving (i.e., gaze was stable) the
pWBR model provided a good fit to the firing rate (Fig. 5A,
middle, pWBR model, thick trace; mean VAF = 0.64 ± 0.07) and accordingly the estimated head-velocity sensitivity was
not significantly different from that during pWBR [mean normalized gest = 0.92 ± 0.05 (sp/s)/(°/s); Fig. 5B, compare
and
]. This result
is analogous to that described in the preceding text for the
active head-on-body motion made when gaze is immobile
immediately following gaze shifts. Thus the head-velocity information
carried by type I PVP neurons was the same regardless of whether the
head was voluntarily moved on the body or whether the head and body were voluntarily moved together; head-velocity sensitivities were similarly reduced when the monkey redirected its gaze and were unaltered when the monkey stabilized its gaze. Taken together, these
findings support the hypothesis that type I PVP neuron responses to
head motion vary in a manner that depends exclusively on the monkey's
current gaze goal.
Type I PVP neurons
SIMULTANEOUS VOLUNTARY AND PASSIVE MOTION. In the behavioral tasks presented until this point, the head motion has been either passively imposed or self-generated, yet, under natural circumstances, passive perturbations of the head and/or body can occur at the same time as voluntary head motion. To further test the proposal that the head-velocity information carried by type I PVP neuron modulation depends only on current gaze goal, we characterized neuronal discharges during simultaneous passive and self-generated head motion. Head-unrestrained monkeys were encouraged to generate voluntary head-on-body movements (Fig. 6A, dashed line arrow in schema) while being passively whole-body rotated (Fig. 6A, solid arrow in schema). During this paradigm, the head-in-space motion is the sum of the passive turntable rotation and the active head-on-body motion.
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-in-space model, thick
trace; mean VAF = 0.73 ± 0.06). Consistent with the latter
model prediction, the head-velocity sensitivities to both passive and
active components of head-in-space motion obtained using Estimate
3 were comparable to the head-velocity sensitivity during pWBR
(Fig. 6B, compare gray shaded columns to solid column). In
summary, neuronal sensitivities to the passive and active components of
head motion were comparable during rapid gaze redirection
(P > 0.2), during slow gaze redirection
(P > 0.2), and during gaze stabilization
(P > 0.3). These results further support the
hypothesis that type I PVP neuron head-velocity responses do not
dependent on whether head motion was actively or passively generated but rather depend on the current behavioral goal of the monkey.
INFLUENCE OF PASSIVE NECK PROPRIOCEPTOR ACTIVATION. To determine whether afferent inputs from neck muscle proprioceptors influence the activity of type I PVP neurons, we used two different paradigms. First we passively rotated the monkey's body while its head was held earth-stationary (Fig. 7A, see schema). The torque produced by the monkey against the head restraint was concurrently measured and found to be small (less than ±0.5 Nm) compared with that produced when orienting to food target (more than ±3.5 Nm). Thus during these passive rotations, the neck motor efference signals generated by the monkeys were minimal, yet the musculature was stretched such that neck proprioceptors were activated. The neuron shown in Fig. 7A was typical in that its activity was not significantly affected by the passive rotation of the neck. Its firing rate was well predicted by the pWBR model (note, in this case: head velocity = 0; pWBR model, thick trace). This finding is best appreciated when the firing rate is corrected for the neuron's eye-position sensitivity (Fig. 7A; FRcorr). For all neurons tested (n = 12), the neck-related signals were negligible [mean neck-velocity sensitivity = 0.07 ± 0.05 (sp/s)/(°/s)].
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head velocity) of the monkeys is shown in the same figure
for comparison (0.9 ± 0.06; Fig. 7, B and
C). VOR gain was measured at 0.5 Hz and assumed to be
constant over the range of frequencies used in this study (see for
example: Bohmer and Henn 1983
]. However, neuron responses to
head velocity were significantly attenuated when the monkey rapidly
redirected its gaze during the passive head rotations [see
in Fig.
8A; mean normalized gest = 0.21 ± 0.18 (sp/s)/(°/s); Fig. 8B,
].
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SUMMARY OF NEURAL DISCHARGE DURING PASSIVE AND
VOLUNTARY HEAD MOTION.
Type I PVP neurons responses to both passive and self-generated head
motion were influenced by the gaze goal of the monkey. When the monkey
stabilized its gaze, the head-velocity sensitivity of the neurons was
comparable to that obtained during pWBR (Fig. 10;
). In contrast, when the monkey
redirected its axis of gaze either slowly (Fig. 10;
) or rapidly
(Fig. 10;
), the head-velocity sensitivity of the neurons was
significantly attenuated as compared with pWBR. The neuronal responses
were more attenuated during rapid gaze redirection than during slow
gaze redirection (Fig. 10; compare
and
). Whether the head was
passively or actively moved or whether the head moved relative to the
body or not did not affect the neural discharges once the gaze goal was
taken into account.
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Type II PVP neurons
In the present study, we also characterized type II PVP neurons. These neurons have opposite eye- and head-motion sensitivities to type I PVP neurons during the head-restrained paradigms shown in Fig. 1 and were included in the present report because they behaved very much like type I PVP neurons during each of the paradigms tested in our study. The only significant difference in firing behavior that we observed was that these neurons frequently discharged a burst during ipsilaterally directed saccades, vestibular quick phases, and gaze shifts. This difference is detailed in the following text.
The type II PVP neuron illustrated in Fig. 11 was typical of the neurons tested (n = 14) in that its firing rate increased for ipsilateral eye positions during spontaneous eye movements (Fig. 11A, see inset). The firing rate of type II PVP neurons was generally well correlated with eye position during ocular fixation (sample mean R2 = 0.64 ± 0.06). The example neuron had a kx of 1.31 (sp/s)/° [sample mean = 1.67 ± 0.37 (sp/s)/°] and a bias of 50 sp/s (sample mean = 55 ± 10 sp/s) during periods of fixation. During smooth pursuit, type II PVP neuron firing rate phase lagged ipsilateral eye velocity and led ipsilateral eye position (Fig. 11B). In general, neuron discharges were well described by the linear combination of eye velocity, eye position, and bias terms (sample mean VAF = 0.56 ± 0.09; Fig. 11B, smooth pursuit model, thick trace). The example neuron had a ksp of 0.61 (sp/s)/° [sample mean = 1.52 ± 0.6 (sp/s)/°], a rsp of 0.44 (sp/s)/(°/s) [sample mean = 0.54 ± 0.14 (sp/s)/(°/s)], and a biassp of 59 sp/s (sample mean = 64 ± 12 sp/s). The mean phase lag with respect to eye velocity for the sample of neurons during smooth pursuit was 64 ± 4.5°. During passive whole-body rotation in the dark (pWBR, Fig. 11C), the neuron increased its firing rate in response to contralateral head motion (i.e., a type II response). A model based on a combination of head velocity, eye position, and bias terms (Estimate 1) provided a good fit of type II PVP neuron activity during pWBR (sample mean VAF = 0.59 ± 0.06). The example neuron had a biaspWBR of 67 sp/s (sample mean = 80 ± 10), a kpWBR of 0.65 (sp/s)/° [sample mean = 1.25 ± 0.37 (sp/s)/°], and a gpWBR of 1.71 (sp/s)/(°/s) [sample mean = 0.89 ± 0.08 (sp/s)/(°/s); Fig. 11C, pWBR model, thick trace]. In addition, each type II PVP neuron stopped firing or "paused" during contralaterally directed saccades and vestibular nystagmus quick phases (note vertical arrows in Fig. 11, A and C). The head-velocity sensitivity of type II PVP neurons was obtained during pWBRc using Estimate 1 (mean sample VAF = 0.50 ± 0.1). The example neuron was representative in that its estimated head velocity was reduced by ~21% as compared with pWBR [normalized gest = 0.79 (sp/s)/(°/s); mean normalized gest = 0.71 ± 0.06 (sp/s)/(°/s); Fig. 11D, pWBRc estimate, thin trace]. This reduction was comparable to what we observed for type I PVP neurons. However, while type II PVP neurons paused during vestibular nystagmus quick phases and saccades in the "off direction" for eye motion (see contralateral saccade in Fig. 12A, left), they most often (n = 9/14) burst during saccades in the "on direction" (ipsilateral saccade shown in Fig. 12A, right). This latter behavior differed from that of type I PVP neurons. During ipsilaterally directed saccades, the eye-velocity sensitivity (rsac) of type II PVP neurons was estimated [fr = biasx + (kx * eye position) + (rsac * eye velocity)] and found to be 0.27 ± 0.05 (sp/s)/(°/s).
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Similar to their responses during head-restrained saccades, most
(10/13) type II PVP neurons paused for the duration of eye-head gaze
shifts in the contralateral direction (Fig. 12B). In
addition, most (8/13) neurons burst for the duration of gaze shifts in
the ipsilateral direction (Fig. 12C). Recall that the
activity of type I PVP neurons was attenuated, in an
amplitude-dependent manner, during ipsilaterally directed gaze shifts.
We estimated the eye- and head-velocity sensitivity of each type II PVP
neuron during ipsilaterally directed gaze shifts using Estimate
2. Even though they burst, the head-velocity sensitivities of type
II PVP neurons were significantly reduced for gaze shifts of all
amplitudes (Fig. 12D; compare
and
). While the
attenuation was not as great as that observed for type I PVP neurons
(Fig. 2B), the level of attenuation did significantly
increase with the increasing amplitude
(R2 = 0.83). In addition, the
estimated eye-velocity sensitivities were comparable to those estimated
during saccades on a neuron-by-neuron basis [sample mean = 0.27 ± 0.05 (sp/s)/(°/s); slope = 0.90, R2 = 0.96]. Type II PVP neurons
showed similar responses when the monkey rapidly redirected its gaze
during all of the behavioral tasks employed. Thus in light of the
results that we obtained from type I PVP neurons, we elected to limit
our analysis of rapid gaze redirections to saccades and gaze shifts (as
described in the preceding text).
Type II PVP neurons behaved similarly to type I PVP neurons whenever the monkey slowly redirected its gaze. The head-velocity sensitivity of the type II PVP neurons was reduced as compared with pWBR (Fig. 13; solid column) when the monkeys cancelled their VOR (pWBRc; Fig. 13; diagonally striped column) and during eye-head gaze pursuit (Fig. 13; vertically striped column). The attenuated response to head velocity was not dependent on whether the head motion was passively or actively generated but rather on the gaze goal of the monkey. This is illustrated by the response of the neurons during simultaneous passive whole-body rotation and voluntary head motion. When gaze was stable, the pWBR model provided a good prediction of the neural firing rate (sample mean VAF = 0.52 ± 0.07) and the head-velocity sensitivity was not attenuated as compared with pWBR (Fig. 13; gray shaded columns). When gaze was redirected the head-velocity sensitivity of the neurons was significantly attenuated (Fig. 13; horizontally striped columns). In addition, during the driving paradigm, where the monkey moved its head and body together in space, the neurons were less responsive when gaze was redirected (Fig. 13; open column) than when gaze was stabilized (Fig. 13; gray shaded column with horizontal stripes). The pWBR model provided a good prediction of the neural activity when gaze was stable during the driving paradigm (sample mean VAF = 0.64 ± 0.14). During ipsilaterally directed rapid gaze redirections (Fig. 13; gray shaded column with diagonal stripes), type II PVP neurons responses were more attenuated than during slow gaze redirection, similar to what was observed for type I PVP neurons (Fig. 10). The influence of afferent inputs from neck muscle proprioceptors on the activity of type II PVP neurons was tested using the same paradigms as described for type I PVP neurons [i.e., passive rotation of the head on the body (Fig. 13; gray shaded column with vertical stripes) and passive rotation of the body under an earth stationary head (data not shown)]. As with type I PVP neurons, the type II PVP neurons tested were not influenced by passive activation (dynamic or static) of the neck proprioceptors.
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DISCUSSION |
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Gaze stabilization vs. gaze redirection
The main finding of the present study is that the head-velocity-related response of the direct VOR pathways is modulated in a manner that is consistent with the behavioral goal of the animal. Neuronal activity of VOR interneurons (type I PVP neurons) was recorded during a diverse range of vestibular stimuli protocols including: passive whole-body rotation, passive head-on-body rotation, active eye-head gaze shifts, active eye-head gaze pursuit, self-generated whole-body motion (i.e., driving), and active head-on-body movements made while the monkey was passively rotated. Regardless of the stimulation condition, head-velocity-related modulation of type I PVP neurons was comparable whenever monkeys stabilized their gaze relative to space. In contrast, whenever the monkeys' behavioral goal was to redirect their gaze relative to space, type I PVP neuron responses to head motion were significantly reduced. We also found that type II PVP neurons, which are likely to contribute indirectly to the VOR, generally behaved in a similar manner. However, there were some important differences which we consider later in this discussion.
Absence of influence from neck proprioceptive inputs
In the present study, we found that neither static nor dynamic
activation of neck propioceptors alone influenced the activity of PVP
neurons (Fig. 14). This result is very
different from that of a recent study (Gdowski and McCrea
2000
) in which it was reported that the majority of type I PVP
neurons are sensitive to static head position relative to the trunk
(61%) and dynamic neck motion (76%). These investigators noted that
their findings might have important implications regarding the COR,
which functions to generate compensatory eye movements in response to
neck motion. They proposed that because PVP neurons carry neck-related
information, these same premotor VOR interneurons might also mediate
the COR. On the one hand, the difference between our results and those
of McCrea and colleagues is surprising given that neurons were recorded during the same paradigms: passive rotation of the monkey's body under
its earth-fixed head and/or passive rotation of its head on its body.
On the other hand, an important difference between these two studies is
that neurons were characterized in old world (rhesus) monkeys in the
present study and in new world (squirrel) monkeys in that of
Gdowski and McCrea (2000)
.
|
Prior studies have determined that COR gains are small to nonexistent
in most species including: rhesus monkeys (Bohmer and Henn
1983
; Dichgans et al. 1973
), humans
(Barlow and Freedman 1980
; Bronstein
1992
; Bronstein and Hood 1986
; Huygen et
al. 1991
; Jürgens and Mergner 1989
),
rabbits (Barmack et al. 1981
, 1989
, 1992
; Fuller
1980
; Gresty 1976
), and cats (Fuller
1980
). The results of the present study are consistent with
these prior reports; none of our rhesus monkeys had COR gains that
differed significantly from zero (Fig. 7, B and
C). However, it is interesting to note that squirrel monkeys
may be an exception to this general rule. In this species, COR gains in
the range of 0.4 have been recently reported (Godwski and McCrea
2000
). This marked difference between the COR gain of rhesus
and squirrel monkeys is consistent with the apparent difference that
neck proprioceptive inputs have on premotor vestibular nuclei neurons
for these two species. In addition, prior reports by our laboratory and
McCrea and colleagues have revealed an analogous difference regarding
the influence of neck proprioceptors on another class of vestibular
nuclei neurons, vestibular-only neurons. These neurons, which are
thought to contribute to the VCR, appear to carry neck afferent signals
in the squirrel monkey (McCrea et al. 1999
) but not in
the rhesus monkey (Roy and Cullen 2001
). In summary, the
results of this and previous studies suggest that use of neck
proprioceptive inputs by vestibular reflex pathways in rhesus and
squirrel monkeys differs greatly.
Absence of influence from neck efference copy
An unresolved question in the vestibular literature is whether or
not the gain of the VOR differs for active versus passive head motion.
Two previous studies have reported higher VOR gains during active
head-on-body motion as compared with pWBR when subjects fixated an
earth-fixed target (Jell et al. 1988
) and in the dark (Demer et al. 1993
). The gain enhancement observed by
Demer and colleagues (1993)
was attributed to an
efference copy of the motor command to the neck. However, there is much
accumulated evidence that suggests the VOR gains are comparable during
active and passive head motion. First, the gains of the VOR during
sinusoidal (0.25-1.0 Hz) passive whole-body rotation and active
head-on-body motion were similar (Hanson and Goebel
1998
). Second, numerous studies have reported that the gain of
the VOR was comparable during passive and active head-on-body motion
(Foster et al. 1997
; Hanson and Goebel
1998
; Pulaski et al. 1981
; Santina et al.
1999
, 2000
; Thurtell et al. 1999
). Third, in the
present report, we have recorded from the VOR interneurons and show
that the head-velocity-related modulation of type I PVP neurons was
comparable during pWBR and active head movements made when gaze was
stable (Figs. 2C, 5B, and 6B).
Finally, our neurophysiological results agree with our observation in
the present study that there was no significant difference in the gain
of the behavioral VOR during pWBR (Fig. 1C; VOR gain
0.94) and immediately following gaze shifts during the active head
motion that occurred once gaze was stable (Fig. 2C; VOR gain
0.98). Thus taken together, the results of behavioral and
single-unit recording experiments strongly suggest that an efference
copy of the neck motor command does not influence to status of the VOR
during active head-on-body motion (Fig. 14).
Our findings appear to be consistent with those of a recent report by
Gdowski and McCrea (1999)
. These investigators recorded the responses of PVP neurons in squirrel monkeys when slow head-on-body movements were made during passive whole-body rotation. They attributed these head-on-body movements to the vestibulocollic reflex and found
that neuronal modulation was better related to head-in-space motion
than to passive turntable motion. It is probable (although it is not
explicitly stated) that the analysis was limited to intervals in which
the axis of gaze was stable. Accordingly, these results could be
interpreted as further evidence that PVP neurons similarly encode
active and passive head motion when gaze is stable.
Influence of knowledge of self-generated motion
Traditionally the vestibular system is associated with generating
the reflexes that are crucial for our daily activities, such as
stabilizing gaze (Grossman et al. 1988
, 1989
) and
posture (for review, see Peterson and Richmond 1988
).
However, the role of the vestibular system is not limited to these
functions. The development of an accurate spatial representation,
proper implementation of navigation, and gaze control involves the
interaction between many brain structures that receive vestibular
information and in turn project back to the vestibular nuclei. It is
possible that these cortical (reviewed in Fukushima
1997
) and cerebellar (Voogd et al. 1996
)
projections could impinge on type I PVP neurons and result in the
differential encoding of head velocity. Here, we have examined whether
a monkey's knowledge of its self-generated motion modified the
head-velocity signals carried by type I PVP neurons. We found that for
active head movements made while gaze was stable, the discharge of type
I PVP neurons could be accurately predicted by their
head-velocity-related response during passive whole-body rotation. This
finding was consistent for active head-on-body movements, active
movements of the head and body together in space (i.e., the driving
paradigm), and combined active and passive head rotations. In all
cases, the attenuation of vestibular responses was limited to the
specific intervals in which monkeys actively redirected their gaze. We
therefore conclude that knowledge of self-motion, per se, does not
directly influence the vestibular sensitivity of type I PVP neurons
(Fig. 14). Note, we have previously shown that another class of neurons
in the vestibular nuclei
vestibular-only neurons, which are thought to
mediate the vestibulocollic reflex
are also not directly influenced by
the monkey's knowledge of self-generated motion (Roy and Cullen
2001
). Thus our results support the hypothesis that a monkey's
knowledge of its self-generated head motion relative to space does not
alter the processing of vestibular information at the level of the
vestibular nuclei.
Convergence of signals on type I PVP neurons
Although the head-velocity-related modulation of type I PVP
neurons was significantly attenuated whenever the monkey wanted to
redirect its gaze in space, the amount of suppression differed depending on the type of gaze movement. Type I PVP neurons were more
attenuated during rapid gaze redirections (Fig. 10,
), which included vestibular quick phases, saccades, eye-head gaze shifts, and
head/body-eye gaze shifts (i.e., driving paradigm step target), than
during slow gaze redirection (Fig. 10,
), which included VOR
cancellation, gaze pursuit, and head/body-eye pursuit (i.e., driving
paradigm pursuit target). We propose efference copies of
oculomotor/gaze motor commands are responsible for the behaviorally dependent modulation of type I PVP neurons
and as a result, for the
status of the VOR
during gaze redirection (Fig. 14). Accordingly, the
differing levels of suppression result from the different gaze premotor
circuitries that generate rapid versus slow gaze redirection.
MECHANISMS FOR VOR SUPPRESSION DURING RAPID GAZE REDIRECTION.
During the rapid redirection of gaze (i.e., saccades, vestibular quick
phases, and gaze shifts), the brain stem burst generator is active. We
have previously proposed that this premotor brain stem circuitry
mediates the attenuation of type I PVP neuron responses, which can be
observed during each of these behaviors (Fig.
15A) (Roy and Cullen
1998
). Burst neurons in the paramedian pontine reticular
formation (PPRF) generate a burst in activity to drive the eye during
saccades and gaze shifts (Cullen and Guitton 1997
). Burst neurons project to type II neurons in the vestibular nucleus (Sasaki and Shimazu 1981
), and in turn, type II neurons
send an inhibitory projection to type I PVP neurons (Nakao et
al. 1982
). Because the type II-type I vestibular projection is
inhibitory, this pathway would effectively invert the "burst"
behavior of burst neurons to create the "pause" in the type I PVP
response observed during rapid redirection of gaze.
|
MECHANISMS FOR VOR SUPPRESSION DURING CANCELLATION AND SLOW GAZE
REDIRECTION.
Because less is known about the connectivity of the brain stem premotor
circuits that mediate smooth pursuit and VOR cancellation than those
that mediate saccades, elucidating the mechanism responsible for the
attenuation in type I PVP neuron responses during slow gaze redirection
is less straightforward. During smooth pursuit eye movements in
head-restrained animals, the cerebellar flocculus and paraflocculus
send pursuit command signals to neurons in the vestibular nuclei
(Lisberger et al. 1994a
). Based on their responses during eye movements and head-rotation paradigms, it is generally agreed that these neurons are part of the same population of neurons that have been termed smooth-pursuit and eye-head neurons
(Cullen et al. 1993
and Scudder and Fuchs
1992
, respectively). Thus for the sake of simplicity, we will
refer to them as eye-head (E/H) neurons here. There is no evidence that
E/H neurons project to PVP neurons. It is possible that pursuit
information reaches the vestibular nuclei indirectly via the BT
neurons, which show robust modulation during smooth pursuit
(Cullen et al. 1993
; McConville et al.
1996
; McFarland and Fuchs 1992
). A schema in
which E/H neurons project to BT neurons and BT neurons, in turn, send
inhibitory pursuit signals to type I PVP neurons is shown in Fig.
15B.
Type II PVP neurons
The responses of type II PVP neurons during slow gaze-redirection tasks were not consistent with their playing a primary role in mediating the attenuation of type I PVP neurons if one assumes an inhibitory ipsilateral projection from type II PVP neurons to the type I PVP neurons (as we did in Fig. 15A). For instance during pWBRc, type II PVP neuron responses are attenuated as compared with during pWBR, which means that their modulation is opposite to what would be required to mediate the suppression of type I PVP neurons. This is not only a problem for pWBRc but also for all of the other slow gaze-redirection tasks because type II PVP neuron responses were attenuated (see Fig. 13). Thus while it is conceivable that type II PVP neurons project to type I PVP neurons, their activity does not appear to be integral for the short-term modulation of type I PVP neuron responses across different behavioral conditions. Given the complex interconnections between the vestibular nuclei, the prepositus hypoglossi, and the cerebellum, it is more likely that over the long term they play a role in balancing vestibular function across these structures.
Conclusion
In conclusion, we have shown that the activity of type I and II PVP neurons is modulated in a manner that depends strictly on the current gaze strategy of the monkey. Neuronal discharges were comparable during active and passive head motion whenever the monkey's gaze was stable. Similarly, discharges were attenuated during active and passive head motion when a monkey redirected its gaze. Thus the neuronal responses to head motion are altered in a manner that is consistent with maximizing the VOR gain when the goal is to stabilize gaze and reducing the VOR gain when the behavioral goal is to redirect gaze. We propose that the attenuation of the direct VOR pathways is mediated via inputs from the premotor circuitries that are known to generate saccades and smooth pursuit eye movements in head-restrained animals.
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ACKNOWLEDGMENTS |
|---|
We thank P. A. Sylvestre, J.T.L. Choi, J. Mok, and M. C. Taylor for critically reading the manuscript and E. Moreau, W. Kucharski, J. Knowles, and A. Smith for excellent technical assistance.
This study was supported by the Canadian Institutes of Health Research.
| |
FOOTNOTES |
|---|
Address for reprint requests: K. E. Cullen, Aerospace Medical Research Unit, 3655 Promenade Sir William Osler, Montreal, Quebec H3G 1Y6, Canada (E-mail: cullen{at}med.mcgill.ca).
Received 30 July 2001; accepted in final form 17 December 2001.
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