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The Journal of Neuroscience, March 15, 2001, 21(6):2131-2142
Selective Processing of Vestibular Reafference during
Self-Generated Head Motion
Jefferson E.
Roy and
Kathleen E.
Cullen
Aerospace Medical Research Unit, McGill University, Montreal,
Quebec, Canada H3G 1Y6
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ABSTRACT |
The vestibular sensory apparatus and associated vestibular nuclei
are generally thought to encode head-in-space motion. Angular head-in-space velocity is detected by vestibular hair cells that are
located within the semicircular canals of the inner ear. In turn, the
afferent fibers of the vestibular nerve project to neurons in the
vestibular nuclei, which, in head-restrained animals, similarly encode
head-in-space velocity during passive whole-body rotation. However,
during the active head-on-body movements made to generate orienting
gaze shifts, neurons in the vestibular nuclei do not reliably encode
head-in-space motion. The mechanism that underlies this differential
processing of vestibular information is not known. To address this
issue, we studied vestibular nuclei neural responses during passive
head rotations and during a variety of tasks in which alert rhesus
monkeys voluntarily moved their heads relative to space. Neurons
similarly encoded head-in-space velocity during passive rotations of
the head relative to the body and during passive rotations of the head
and body together in space. During all movements that were generated by
activation of the neck musculature (voluntary head-on-body movements),
neurons were poorly modulated. In contrast, during a task in which each
monkey actively "drove" its head and body together in space by
rotating a steering wheel with its arm, neurons reliably encoded
head-in-space motion. Our results suggest that, during active
head-on-body motion, an efferent copy of the neck motor command, rather
than the monkey's knowledge of its self-generated head-in-space motion
or neck proprioceptive information, gates the differential processing
of vestibular information at the level of the vestibular nuclei.
Key words:
vestibular nucleus; self-motion; reafference; efference
copy; gaze shift; gaze pursuit; vestibular reflexes; head-unrestrained
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INTRODUCTION |
On the basis of behavioral
experiments, von Holst and Mittelstaedt (1950) proposed that the
sensory signals that arise from an animal's own movement, which they
termed reafference, could be distinguished from sensory signals
generated by external sources. They postulated that a copy of the motor
command (efference copy) is combined with the afferent sensory signal
to selectively remove the reafferent component caused by the motor
behavior. Indeed, it is now well established that, in certain model
systems, for example the electrosensory system of the electric fish
(Bell, 1981) and mechanosensory system of the crayfish (Krasne and
Bryan, 1973; Edwards et al., 1999), sensory signals are suppressed at the level of afferent fibers and/or the central neurons to which they
project, via an efference copy signal. Accordingly, sensory information
is filtered such that signals arising from external sources are emphasized.
Whether reafferent signals from the vestibular semicircular canals are
selectively processed during self-generated motion is an issue of
continuing controversy. Because it is technically difficult to maintain
isolation of a single vestibular receptor cell or primary afferent
during active motion, this question has been addressed only at the
level of second-order neurons in the vestibular nucleus. Recent
experiments in squirrel monkey (Boyle et al., 1996; McCrea et al.,
1996, 1999) have shown that a specific subclass of second-order neurons
[vestibular-only (VO) neurons] are significantly less sensitive to
the head motion generated during active eye-head gaze shifts than
during passive whole-body rotations. In contrast, in rhesus monkey,
single-unit recordings showed that VO neurons similarly encode head
velocity during passive whole-body rotation and combined eye-head
pursuit (Khalsa et al., 1987). Unfortunately, the interpretation of
these previous studies is limited, because neuronal responses were
tested during different voluntary behaviors, i.e., gaze shifts (Boyle
et al., 1996; McCrea et al., 1999) or gaze pursuit (Khalsa et al.,
1987).
Although the above findings in squirrel monkey are consistent with the
hypothesis that an efference copy of the neck motor command selectively
suppresses vestibular signals that arise from active head motion, it is
also possible that other mechanisms mediate the observed attenuation of
VO neuron responses. First, VO neurons could be selectively inhibited
by the premotor circuitry that generates gaze shifts. This would
account for the apparent discrepancy between previous studies, because
the brainstem burst generator is active throughout gaze shifts but is
silent during smooth pursuit (Keller, 1974; Cullen and Guitton, 1997a).
Therefore, we recorded from the same VO neurons during gaze shifts and
gaze pursuit to determine whether vestibular reafferent signals were similarly suppressed. In addition, neuronal responses were
characterized immediately after gaze shifts in which the burst
generator is silent and the axis of gaze is stable, yet the head is
still moving in space (Cullen et al., 1993b; Cullen and Guitton,
1997b). Alternatively, it is possible that the monkey's knowledge of
its self-generated head motion attenuates the sensitivity of VO neurons
to head velocity during gaze shifts. To test this hypothesis, we
designed a novel behavioral task in which a head-restrained monkey
voluntarily "drove" its head and body together in space by manually
rotating a steering wheel. Finally, we investigated whether inputs from the neck muscle proprioceptors might contribute, at least in part, to
the attenuation of VO neuron responses during gaze shifts. To date,
there has been no clear agreement on how strongly this input influences
the activity of VO neurons in alert animals (cat: Fuller 1988;
squirrel monkey: McCrea et al., 1999; Gdowski and McCrea, 1999; rhesus:
Khalsa et al., 1987, 1988). To address this question, neurons were
characterized during passive rotation of the head relative to the body
while the monkey was generating minimal neck motor commands.
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MATERIALS AND METHODS |
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 described previously by Sylvestre and Cullen (1999). Briefly, surgical levels of anesthesia were achieved using isoflurane gas (2-3% initially) and maintained for the duration of the surgery (0.8-1.5%). A dental acrylic implant was fastened to each animal's skull using stainless steel screws. A stainless steel post, which was
used to restrain the animal's head, and a stainless steel recording
chamber, which was positioned to provide access to the medial
vestibular nucleus (posterior and lateral angles of 30°), were
attached to the implant. In the same procedure, an 18-19 mm in
diameter eye coil (three loops of Teflon-coated stainless steel wire)
was implanted in the right eye behind the conjunctiva. After the
surgery, buprenorphine (0.01 mg/kg, i.m.) was used for postoperative
analgesia. Animals were given 2 weeks to recover from the surgery
before any experiments were performed.
Data acquisition. During the experiments, the monkey
was comfortably seated in a primate chair, which was fixed to the
suprastructure of a vestibular turntable. The monkey's head was
initially restrained during each experiment, and the room was dimly
lit. Extracellular single-unit activity was recorded using
enamel-insulated tungsten microelectrodes (7-10 M impedance;
Frederick Haer Co., Bowdoinham, ME) as has been described
previously (Sylvestre and Cullen, 1999). The locations of the medial
and lateral vestibular nuclei were determined relative to the abducens
nucleus, which was identified based on its stereotypical discharge
patterns during eye movements (Cullen et al., 1993a; Sylvestre and
Cullen, 1999). Gaze and head position were measured using the magnetic
search coil technique (Fuchs and Robinson, 1966). Turntable velocity
was measured using an angular velocity sensor (Watson Inc.). Unit
activity, horizontal and vertical gaze and head positions, target
position, and table velocity were recorded on digital audio tape
for later playback. The isolation of each unit was carefully
reevaluated off-line. During playback, action potentials were
discriminated using a windowing circuit (BAK Electronics Inc.,
Germantown, MD) that was manually set to generate a pulse
coincident with the rising phase of each action potential. Gaze
position, head position, target position, and head velocity signals
were low-pass filtered at 250 Hz (eight-pole Bessel filter) and sampled
at 1000 Hz.
Behavioral paradigms. All monkeys were trained to follow a
target light for a juice reward. The activity of vestibular neurons was
initially recorded with the monkey in the head-restrained condition
during voluntary eye movements and passive whole-body rotations. A
target light (HeNe laser) was projected, via a system of two
galvanometer-controlled mirrors, onto a cylindrical screen located 60 cm away from the monkey's head. Neuronal responses were recorded
during eye movements made to track a target that was (1) stepped
between horizontal positions over a range of ±30° and (2) moved
sinusoidally (0.5 Hz, 80°/sec peak velocity) in the horizontal plane.
Neuronal sensitivities to head velocity were tested by passively
rotating monkeys about an earth vertical axis (0.5 Hz, 80°/sec peak
velocity) in the dark [ passive whole-body rotation (pWBR)]
and while they cancelled their vestibulo-ocular reflex 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; Hays et al.,
1982).
After a neuron was fully characterized in the head-restrained
condition, the monkey's head was slowly and carefully released. Once
released, the monkey was free 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 horizontal head movements made during combined
eye-head gaze shifts (15-65° in amplitude) and combined eye-head
gaze pursuit of a sinusoidal target (0.5 Hz, 80°/sec peak velocity).
Neuronal responses to combined passive and active head motion were
tested by passively rotating (0.5 Hz, 80°/sec peak velocity) monkeys
in the head-unrestrained condition, such that they could simultaneously
generate voluntary head-on-body movements. We analyzed those intervals
in which head motion velocity differed from turntable velocity by
>10°/sec. The active component of head motion was calculated by
subtracting the turntable velocity from the head-in-space velocity. The
passive component of head motion was the velocity of the passive
turntable rotation. This analysis assumes that the vestibulo-collic
reflex (VCR) response is minimal in rhesus monkeys, which is consistent
with our preliminary data (our unpublished observations). Finally, to
investigate the influence of neck proprioceptive inputs on neural
discharges, two different paradigms were used: (1) the monkey's head
was held stationary relative to the earth while its body was passively rotated below (0.5 Hz, 80°/sec peak velocity), and (2) the
experimenter manually rotated the monkey's head to induce rapid motion
of the head relative to a stationary body. In the first of these two paradigms, the torque produced against the head restraint was measured
using a reaction torque transducer (Sensotec, Columbus, OH).
Neuronal responses to voluntary head-in-space motion generated by
behaviors that did not involve activation of the neck musculature were
characterized using one of two head-restrained paradigms. In the first,
monkeys fixated a light-emitting diode (LED) target that was
attached to the turntable. When the LED began to flash, the monkey
depressed a switch initiating a constant velocity-direction rotation
of the turntable (40°/sec). In the second, monkeys were trained to
operate a steering wheel that controlled the rotation of the turntable
on which they were seated to track a laser or a food target. During
this latter "driving paradigm," the position of the steering wheel
was fed into the turntable servo, which in turn controlled the position
of the turntable. Thus, monkeys controlled the initiation of the
movement and also the rotational velocity of the turntable, via the
speed at which they rotated the steering wheel.
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 msec for saccades
and gaze shifts and 10 msec for the remainder of the paradigms) (Cullen
et al., 1996). Saccade and gaze shift onsets and offsets were defined
using a ±20°/sec gaze velocity criterion. Subsequent analysis was
performed using custom algorithms (Matlab; MathWorks Inc., Natick, MA).
Statistical significance was determined using a paired Student's
t test.
In this study, we only present data from neurons that were not
sensitive to eye position during ocular fixation and eye position or
velocity during smooth pursuit. To verify that a neuron was unresponsive to eye position and/or velocity, we analyzed periods of
steady fixation and saccade-free smooth pursuit using a multiple regression analysis (Roy and Cullen, 1998). A least-squared regression analysis was then used to determine the phase shift of each unit relative to head velocity, resting discharge (bias, spikes per second),
and head velocity sensitivity [gpWBR
(spikes per second)/(degrees per second)]. This analysis was
done during pWBR and pWBRc to obtain two estimates of head velocity
sensitivity of a neuron. Only unit data from periods of slow-phase
vestibular nystagmus (pWBR) or steady fixation (pWBRc) that occurred
between quick phases of vestibular nystagmus and/or saccades were
included in the analysis.
Confirmation of neuron isolation. To confirm that isolation
of the same neuron was maintained before and after the
head-restrained-head-unrestrained transition, resting discharge rates
were compared. Values were not significantly different before and after
head release on a neuron-by-neuron basis (population mean, 61 ± 33 vs 64 ± 33 spikes/sec, respectively;
R2 = 0.9; p > 0.8). In addition, the pWBRc paradigm was repeated for the majority
(77%) of neurons after head release, and the neuronal modulation was
found to be comparable with that observed during the initial
head-restrained characterization [mean head velocity sensitivity,
0.53 ± 0.24 vs 0.50 ± 0.25 (spikes/sec)/(°/sec), respectively; R2 = 0.86;
p > 0.6].
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RESULTS |
Vestibular-only neurons: head-restrained condition
A distinct population of vestibular nuclei neurons, VO
neurons, are known to receive direct monosynaptic projections from vestibular nerve afferents (Scudder and Fuchs, 1992; Cullen and McCrea,
1993; McCrea et al., 1999). To date, VO neurons have been well
characterized in head-restrained monkeys (Fuchs and Kimm, 1975; Keller
and Kamath, 1975; Tomlinson and Robinson, 1984; Scudder and Fuchs,
1992; Cullen and McCrea, 1993); their firing frequency is modulated by
head-in-space motion during whole-body rotation but not by eye-in-head
motion. An example of VO neuron discharge is illustrated in Figure
1. During pWBR about an earth vertical axis, the neuron was strongly modulated in response to ipsilaterally directed head velocity [head velocity sensitivity, 0.62 (spikes/sec)/(°/sec)] (Fig. 1A). Because the pWBR
paradigm elicited a compensatory eye motion response [i.e., the
vestibulo-ocular reflex (VOR)], each neuron was also characterized
during passive whole-body rotation while the monkey suppressed its VOR
by fixating a visual target that moved with its head (pWBRc) (Fig.
1B). This neuron was representative of the cells in
our sample (n = 40) in that its head velocity sensitivity during pWBRc was the same as during pWBR [sample mean head
velocity sensitivity, 0.52 ± 0.24 (±SD) and 0.53 ± 0.24 (spikes/sec)/(°/sec), respectively]. Moreover, all neurons were
unresponsive to eye position during steady fixation (Fig.
1C), eye motion during saccades (Fig. 1C,
arrows), and smooth pursuit (Fig. 1D).
Depending on whether their activity increased during ipsilaterally
(n = 23) or contralaterally (n = 17)
directed passive whole-body rotation, neurons were further classified
as type I or type II, respectively. For the purpose of this paper, type
I and II neurons were considered collectively, because they encoded
similar signals during each behavioral task.
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Figure 1.
Activity of an example VO neuron (unit
79_5) during the head-restrained condition.
A, B, Passive whole-body rotation was
used to characterize the response of the neuron to head movements
during VOR in the dark (A) and head movements
while the monkey cancelled its VOR by fixating a target that moved with
the table (B). A model based on head-restrained
head movement sensitivities during VOR in the dark (pWBR
prediction, thick trace) is superimposed on the
firing rate traces. C, D, The neuron was
unresponsive to eye movements during saccades (arrows in
C) and smooth pursuit (D). Note
that neurons were also unresponsive to vestibular quick phases
(arrows in A). Traces
directed upward are in the ipsilateral direction.
E, Eye position; H, head position;
 , eye-in-head velocity;  ,
head velocity;  , gaze velocity
( + );
FR, firing rate.
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Vestibular-only neurons: voluntary head-on-body motion
The sensitivity of each VO neuron to voluntary head motion was
also characterized during combined eye-head gaze shifts. The monkey's
head was released from its restraint, allowing rotation through the
natural range of motion in all three axes. During the critical
transition between the head-restrained and head-unrestrained conditions, the waveform of the action potential of each neuron was carefully monitored to ensure that the cell remained undamaged and
well isolated (see Materials and Methods). Our example neuron was
typical of all neurons tested in that it was poorly modulated by
voluntary head motion during small (25-35°) and large (55-65°) horizontal gaze shifts (Fig.
2A, filled
arrows, left and right panels,
respectively). For each cell, we determined whether a model (Fig.
1A, thick trace) based on the head
velocity sensitivity of the neuron during passive whole-body rotation
could predict the firing rate of the neuron during combined
eye-head gaze shifts. The model is given by the following
equation:
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where fr is the firing rate, and
gpWBR is the head velocity sensitivity
of the neuron during passive whole-body rotation. This model
consistently overestimated the discharge of the neuron during active
head-in-space motion (Fig. 2A, pWBR
prediction, thick traces). To quantify this
observation, we determined the best estimate of head velocity
sensitivity of each neuron
(gest) during gaze shifts
(range, 15-65°) using the following equation:
VO neurons were less modulated for the voluntary head-on-body
movements made during gaze shifts than during passive whole-body rotation (Fig. 2A, compare pWBR prediction
with estimate). The mean head velocity sensitivity of our
sample of neurons was significantly reduced compared with that observed
during pWBR [0.17 ± 0.16 vs 0.53 ± 0.24 (spikes/sec)/(°/sec); p < 0.005], in agreement with previous studies in rhesus monkey (Roy and Cullen, 1999) and squirrel monkey (Boyle et al., 1996; McCrea et al., 1996, 1999).
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Figure 2.
Activity of an example VO neuron (unit
79_5) during and after voluntary combined eye-head gaze
shifts. A, Superimposed on the firing rate are fits for
the pWBR prediction and the estimate of the head velocity sensitivity.
The pWBR prediction overestimated the discharge of this neuron during
small (middle panel) and large (right
panel) amplitude gaze shifts. Dotted vertical
lines indicate the onset and offset of gaze shifts using a
±20°/sec criterion. Two time intervals are denoted: the duration of
the gaze shift (large filled arrows) and 10-80 msec
immediately after the gaze shift (large open arrows).
B, During gaze shifts, the head velocity sensitivity of
our sample of VO neurons was similarly attenuated for all gaze
shift amplitudes from 15 to 65° (gray columns),
and responses were significantly (p < 0.005) smaller than those resulting from pWBR (black
column). C, Comparable attenuation was observed
in the postgaze shift interval (gray columns).
Error bars show SEM. Abbreviations as in Figure 1.
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Here and for all subsequent tasks (see below) during which VO neurons
were tested, head velocity sensitivity of each cell was normalized
relative to passive whole-body rotation (pWBR) to facilitate comparison
(normalized sensitivity, gest for a
given task/gpWBR). For example, during
gaze shifts, the normalized head velocity sensitivity of VO neurons was
0.17 ± 0.16/0.53 ± 0.24 = 0.32 ± 0.35 (spikes/sec)/(°/sec), corresponding to an attenuation of 68%.
Figure 2B illustrates that the attenuation of neural
sensitivities to head velocity that we observed during gaze shifts was independent of gaze shift amplitude. For each neuron, gaze shifts were
sorted into separate data sets, each spanning 10° and containing at
least 10 and generally 15 or more examples. The head velocity sensitivities were estimated separately for each amplitude range. For
our entire sample of VO neurons, the attenuation of head velocity sensitivity was not significantly different for large gaze shifts than
for small ones [e.g., normalized
gest, 0.36 ± 0.33 (spikes/sec)/(°/sec) for 55-65° vs 0.28 ± 0.36 (spikes/sec)/(°/sec) for 15-25°); p > 0.2] and
was always significant relative to pWBR (p < 0.005).
To determine whether the same neurons demonstrated similar attenuation
during all voluntary motion of the head on the neck, neural responses
were characterized during (1) voluntary head movements made when gaze
was immobile and (2) voluntary head movements made during combined
eye-head gaze pursuit. To address whether VO neuron responses to head
motion were attenuated during the period that immediately followed a
gaze shift in which the head was still moving but gaze was immobile
(Fig. 2A, open arrows), a quantitative
analysis was performed. The pWBR prediction provided a poor estimate of
VO neuron activity during this interval (thick traces). We
obtained an estimate of head velocity sensitivity (gest) over the interval of
10-80 msec that immediately followed each gaze shift and found that
the mean calculated attenuation in neural modulation was comparable
with that observed during gaze shifts [normalized
gest, 0.35 ± 0.3 (spikes/sec)/(°/sec); p > 0.6]. Figure
2C illustrates the attenuation in head velocity sensitivities that we observed immediately after gaze shifts for our
population of VO neurons. As was the case during gaze shifts, the level
of attenuation did not vary systematically with gaze shift amplitude
(p > 0.5). Furthermore, for our entire sample of VO neurons, attenuation was comparable during the postgaze shift
interval and the gaze shift itself for all amplitudes
(p > 0.9) (Fig. 2, compare B,
C).
We characterized VO neuron responses to head motion during combined
eye-head gaze pursuit and obtained an analogous result (Fig.
3A). All neurons tested
(n = 31) were less sensitive to head-in-space (or
head-on-body) motion during gaze pursuit [normalized gest, 0.32 ± 0.44 (spikes/sec)/(°/sec)] than during passive whole-body rotation
(p < 0.005). This is illustrated for our
example neuron in which the pWBR prediction (Fig. 3A, thick
trace) consistently overestimated the modulation of the neuron
during gaze pursuit. The mean peak head movement velocities generated
in this task were significantly less than those generated during gaze
shifts larger than 35° (Fig. 3B) and were much less
stereotyped. Nevertheless, the estimated head velocity sensitivities
during gaze pursuit were comparable with those observed during gaze
shifts on a neuron-by-neuron basis
(H0, slope of 1; p > 0.9) (Fig. 4).
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Figure 3.
Responses of a typical VO neuron (unit
79_5) to voluntary head-on-body motion during combined
eye-head gaze pursuit. A, The response of the unit to
self-generated head motion was reduced compared with that predicted by
the sensitivity of the neuron to passive whole-body rotation (compare
pWBR prediction and estimate).
B, Comparison of head velocities generated during gaze
shifts and gaze pursuit. The mean peak head velocities generated during
gaze shifts (>35° in amplitude; gray columns) were
significantly larger than those generated during gaze pursuit
(black column).  , Target velocity.
All other abbreviations as in Figure 1.
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Figure 4.
VO neuron responses during gaze shifts and gaze
pursuit. Despite the differences in peak head velocities and type of
eye motion generated during the two tasks, the normalized head velocity
sensitivities were not significantly different. Comparable trends were
found for type I ( ) and type II ( ) VO neurons. Dashed
line represents unity.
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Figure 5 summarizes the head velocity
information carried by VO neurons during passive whole-body rotation
paradigms versus self-generated head motion resulting from activation
of the neck musculature. We found that the head velocity signal carried
by our population of neurons was similarly attenuated for all behaviors in which head-in-space motion resulted from active motion of the head-on-body (gray columns). Furthermore, the
observed attenuation was not dependent on whether the behavioral goal
was to redirect gaze (gaze shifts and gaze pursuit) or stabilize gaze
in space (i.e., in the interval after gaze shifts). VO neuron responses were similarly decreased during and immediately after gaze shifts [normalized gest averaged across all
amplitudes, 0.32 ± 0.33 vs 0.35 ± 0.3 (spikes/sec)/(°/sec)] and gaze pursuit [normalized gest, 0.32 ± 0.44 (spikes/sec)/(°/sec)]. In contrast, when gaze was redirected during
passive whole-body rotation to cancel the VOR, VO neurons showed little
or no attenuation in their head velocity sensitivity [black
column; normalized gpWBRc,
0.97 ± 0.12 (spikes/sec)/(°/sec)]. Thus, the discharge of VO
neurons depended on whether head-in-space motion resulted from an
active head-on-body movement and not the monkey's gaze strategy (i.e., to stabilize or redirect gaze). The implications of this differential processing of head velocity information will be considered in Discussion.
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Figure 5.
During self-generated head-on-body motion, the
suppression of the head velocity sensitivity was not dependent on
whether the monkey was stabilizing or redirecting its gaze. During the
pWBRc paradigm (black column) in which the monkey was
redirecting its gaze, the neuronal responses were not significantly
different from those observed during pWBR, yet when gaze was redirected
during gaze shifts and gaze pursuit (gray
columns), neuronal responses were significantly attenuated. VO
neurons response were selectively attenuated during active motion of
the head-on-body: gaze shifts, gaze pursuit, and the period immediately
after the gaze shifts (rightmost column) in which gaze
was immobile but the head continued to move. Error bars show SEM.
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Vestibular-only neurons: simultaneous voluntary and passive
head motion
We next addressed whether VO neurons selectively encode vestibular
inputs that arise from external sources (i.e., passively applied
motions) when the vestibular system is simultaneously stimulated by
passive and self-generated head motion. Neurons were recorded while the
monkey generated voluntary head movements on its body (Fig.
6A, dashed
arrow in schema) while undergoing passive
whole-body rotation (Fig. 6A, filled arrow
in schema). During this paradigm, the head-in-space movement
(S) is the sum of the passive whole-body
rotation ( S) and the voluntarily generated
head-on-body motion (B). Remarkably, our
example neuron responded robustly to only the component of
head-in-space motion produced by passive rotation of the body (Fig.
6A, S
prediction, thin dark trace and  in bottom
left panel). This finding is in agreement with studies in
squirrel monkey (Boyle et al., 1996; McCrea et al., 1999). In contrast,
the neuronal response to the component of head-in-space motion
generated by the monkey's own voluntary head-on-body movements was
relatively weak or negligible (Fig. 6A,
S prediction, thick
dark trace and  in bottom left panel). For
the sample of neurons (n = 24), responses to the
voluntary component of head-on-body motion were significantly reduced
when gaze was redirected [normalized
gvol, 0.33 ± 0.33 (spikes/sec)/(°/sec)] (Fig. 6B, black
column) or stabilized [normalized
gvol, 0.33 ± 0.36 (spikes/sec)/(°/sec)] (Fig. 6B, gray
column), whereas responses to the passive component of the motion
were not attenuated, regardless of monkey's gaze strategy [normalized
gpass, 0.98 ± 0.12 and 0.95 ± 0.23 (spikes/sec)/(°/sec) gaze redirected and stabilized,
respectively] (Fig. 6B, white columns).
Thus, the vestibular afferent input to VO neurons was not cancelled in
its entirety (i.e., gated out) during self-generated head motion;
vestibular afferent signals related to the voluntary head-on-body
motion were effectively suppressed, but neurons continued to respond to
unexpected perturbations of the head.
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Figure 6.
VO neuron responses to combined voluntary and
passive head-in-space motion. A, Head-unrestrained
monkeys generated voluntary head-on-body movements (dashed
arrow in schema) while being passively rotated
by the vestibular turntable (thick arrow in
schema). Head-in-space movement
(S) is the sum of the body-in-space motion
(S) generated by passive rotation and
voluntary head-on-body movements (B). The
modulation of the example neuron (unit 79_5) was well
correlated with the passive body-in-space motion
(S prediction,
thin dark trace) but was poorly related to the voluntary
head-on-body component of head-in-space motion
(S prediction,
thick dark trace). Bottom left panel,
Modulation in response to passive body-in-space motion () and to
voluntary head-on-body motion during combined stimulation ().
B, The response to the voluntary component of
head-in-space motion was significantly attenuated when the monkey was
either redirecting (black column) or stabilizing
(gray column) its gaze. In contrast, the neurons
showed no attenuation in response to the passive rotation component
(white columns). Error bars show SEM. All other
definitions as in Figure 1.
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Vestibular-pause neurons
To emphasize the implications of the above findings, we recorded
from an additional 10 neurons termed vestibular-pause (V-pause) neurons, which have been well characterized in head-restrained animals
(Fuchs and Kimm, 1975; Keller and Kamath, 1975; Scudder and Fuchs,
1992; McCrea et al., 1999). V-pause neurons differ from VO neurons only
in that they stop firing (pause) for saccades and vestibular quick
phases (Fig. 7 arrows,
A and B, respectively). Like VO neurons, V-pause
neurons are not sensitive to eye position (Fig. 7A) or eye
velocity during smooth pursuit (data not shown) and are strongly
modulated by head-in-space motion during pWBR (Fig. 7B).
Moreover, their responses during pWBR and cancellation of the VOR
(pWBRc) are comparable [head velocity sensitivities, 0.90 ± 0.60 and 0.87 ± 0.47 (spikes/sec)/(°/sec)]. V-pause neurons further
resembled VO neurons in that their vestibular responses to active
head-on-body movements immediately after gaze shifts (Fig.
7C, open arrows) and during gaze pursuit were
similarly attenuated [normalized gest, 0.47 ± 0.23 vs 0.56 ± 0.19 (spikes/sec)/(°/sec), respectively;
p > 0.1]. Figure 7C shows that the
normalized head velocity sensitivities estimated for these two tasks
were well correlated for the population of neurons (right
panel) (H0, slope of 1;
p > 0.2). However, during gaze shifts, V-pause neurons
paused (Fig. 7C, filled arrows) as they did
during head-restrained saccades. Accordingly, the normalized head
velocity sensitivity of all V-pause cells was nearly zero [normalized
gest, 0.12 ± 0.14 (spikes/sec)/(°/sec)] and was poorly correlated with vestibular sensitivities measured during
other self-generated movements of the head-on-body. Head velocity
sensitivities of V-pause neurons were estimated using a model that
included an eye velocity term, as well as a bias term and a head
velocity term. In addition, the neural responses of V-pause neurons
during simultaneous stimulation with passive and voluntary head motion
were similar to those of VO neurons when the monkey's goal was to
either stabilize its gaze or redirect its gaze using slow eye
movements. Otherwise, during rapid eye movements, the neurons paused in
activity. Thus, V-pause neurons differ from vestibular-only neurons in
that they appear to receive an additional source of inhibition from the
saccadic premotor circuitry during gaze shifts, as well as during
saccades and vestibular quick phases. The responses of V-pause neurons
were comparable with VO neurons, except during rapid eye movements, for
the remainder of the tasks in this study.
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Figure 7.
Activity of an example V-pause neuron (unit
b44_1) during head-restrained and head-unrestrained tasks.
A, V-pause neurons paused (stop firing) during saccades
(arrows) and were not sensitive to eye position.
B, During pWBR, V-pause neurons were strongly modulated
and paused for vestibular quick phases in both directions
(arrows). C, V-pause neurons paused
during gaze shifts (filled arrows) and responded
with an attenuated sensitivity to head motion immediately after gaze
shifts (open arrows, pWBR prediction).
Bottom left panel, The normalized head velocity
sensitivities during the postgaze shift period and during gaze pursuit
were comparable for our sample of V-pause neurons (slope of 0.70).
Definitions as in Figure 1.
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Self-generated motion of the head and body in space
To determine whether the monkey's knowledge of its self-generated
head motion attenuates the sensitivity of VO neurons to head velocity,
we characterized neural activity during two voluntary tasks in which
the head and body moved together relative to space. In the first task
(Fig. 8A,
schema), monkeys were trained to depress a switch at the
appearance of a light cue. By pushing the switch, the monkey initiated
a vestibular turntable rotation of a constant velocity, direction, and
duration, after which it received a juice reward. The example neuron
was typical of the three neurons tested in that it was strongly
activated by the resultant head motion; its activity could be reliably
predicted by its head velocity sensitivity during passive whole-body
rotation (Fig. 8A, pWBR prediction,
thick trace). During this task, the monkey anticipated the
head movement, because it initiated the motion of the turntable. However, it is arguable whether the resultant head movement was truly
voluntary, because the monkey had no control over the actual trajectory
of table motion.
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Figure 8.
VO neuron responses to voluntary combined
head-body motion. A, Head-restrained monkeys pressed a
switch, which in turn initiated rotation of the turntable
(dashed arrow in schema). The activity of
an example neuron (unit 103_1) was well predicted by its
sensitivity to head velocity during pWBR (pWBR
prediction, thick trace). A velocity of 0°/sec
is indicated by the horizontal dotted line.
B, Head-restrained monkeys manually controlled a
steering wheel to rotate the vestibular turntable relative to
space. Their goal was to align a turntable-fixed laser target
(Ttable) with a computer-controlled
target (Tgoal). Example neuron (unit
141_1) was typical in that its response was well predicted
by its sensitivity to head velocity during pWBR
(pWBR prediction, thick trace).
B denotes head-on-body motion
(0°/sec in A, B). All other
abbreviations as in Figure 1.
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To address this issue, we designed a second task in which the monkey
directly controlled the velocity and direction of the vestibular
turntable. Monkeys drove their own body motion by rotating a
steering wheel connected to the motor controller of the vestibular turntable (Fig. 8B, schema). Each animal
was well trained in this task and would generate accurate head-in-space
motion to align its head-body position with either a laser target
[laser task (Fig. 8B)] or a food reward (banana
task; data not shown). Thus, the trajectory of the head motion was the
direct result of a goal-directed action taken by the monkey. All
neurons tested (n = 15) were strongly modulated by the
resultant voluntary head-in-space motion [normalized gest, 1.04 ± 0.18 and 1.05 ± 0.16 (spikes/sec)/(°/sec), laser and banana task, respectively].
Moreover, the activity of each neuron was predicted well by a model
based on the modulation of the neuron during passive whole-body
rotation (Fig. 8B, pWBR prediction, thick trace). Together, these results indicate that
vestibular-related modulation was not attenuated by the knowledge of
self-generated motion of the head relative to space and that the
specific motor command (i.e., activation of the neck musculature) used
to produce the behavior must be considered.
Effect of neck afferent activation
It is known that in decerebrate animals neck muscle spindle
afferents influence the activity of vestibular nuclei neurons (Boyle
and Pompeiano, 1981; Anastasopoulos and Mergner, 1982; Wilson, 1991) via a disynaptic pathway (Sato et al., 1997). It is
conceivable that in alert monkeys neck afferent inputs contribute to
the suppression of VO neuron responses during and after gaze shifts
(Fig. 2A) and during gaze pursuit (Fig.
3A). To address this possibility, we tested neurons during
two experiments in which the head was rotated relative to the body. It
is likely that the passive neck rotation resulted in even greater
activation of neck proprioceptors than did active head-on-body
rotations, because gamma motoneurons are more active during passive
than active movements (Prochazka et al., 1987), and, in turn, the
sensitivity of muscle spindles to passive neck rotation is likely to be
greater (Hulliger et al., 1977).
In the first experiment, the monkey's head was held stationary
relative to space and its body was rotated beneath it (Fig. 9A, filled arrow in
schema). The example VO neuron was representative of our
sample in that it vigorously responded to passive whole-body rotation
(Fig, 1A) but was unresponsive to passive rotation of the body under the neck (Fig. 9A, bottom left
panel, compare with ). The activity of the neuron was well
described by its spontaneous discharge rate (Fig. 9A,
B prediction, thick
trace) and poorly predicted by a model that would be consistent
with neck afferent inputs suppressing vestibular responses during
voluntary head-on-body motion (Fig. 9A,
S prediction, thin
trace). Neck rotation sensitivities were negligible [normalized
sample mean, 0.12 ± 0.18 (spikes/sec)/(°/sec)] (Fig.
9B, white column) for all neurons tested
(n = 15) and thus did not significantly contribute to
the attenuation that was observed during self-generated head motion
(Fig. 9B, gray columns). 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 monkeys oriented to food targets (torque of more than
±3.5 Nm). Thus, the neck motor commands, and by extension neck motor
efference copy signals, generated by the monkeys were minimal during
these passive rotations.
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Figure 9.
Response of VO neurons to passive neck rotation.
A, The response of example neuron (unit
br31_2) was typical in that it was not modulated when the
monkey's body was passively rotated beneath its stationary head; the
mean and variance of the discharge of the neuron was comparable during
this paradigm and head-restrained eye movement paradigms (mean
interspike interval, 18 ± 13 vs 17 ± 13 msec,
respectively). The neural discharge was well described by the
B prediction, which was based on head motion (zero
in the paradigm), and was overestimated by the S
prediction, which was generated using the hypothetical neck sensitivity
required to account for the attenuated vestibular response of the
neuron during active head-on-body motion. Bottom
left panel, Comparison of neural modulation in response
to pWBR () and to passive neck rotation (). B, The
normalized neck velocity sensitivity (white column) is
insufficient to account for the attenuation observed during gaze
shifts, after gaze shifts, and during gaze pursuit (gray
columns). Error bars show SEM. Abbreviations as in Figure
1.
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The influence of neck afferent inputs was further investigated using a
paradigm during which the experimenter rapidly rotated the animal's
head on its neck (Fig.
10A, hand
in schema). The passively elicited head-on-body movements
had head-in-space trajectories and velocities comparable with those
generated during large voluntary gaze shifts (mean peak head velocity,
167 ± 63 vs 153 ± 55 °/sec for 55-65° gaze shifts).
Torque was not measured during this paradigm, but the analysis was
restricted to intervals in which monkeys exhibited little resistance to
rotation. The neuronal firing rate of the example neuron was well
predicted by the head velocity sensitivities during passive
head-on-body rotation (Fig. 10A, pWBR prediction, thick trace), indicating that the passive
activation of the neck muscle spindles did not alter the sensitivity of
VO neurons to head-in-space motion [Fig. 10A,
bottom left panel, compare the responses to passive neck
motion () with responses to passive head motion ()].
Furthermore, for the neurons tested (n = 23), the
neural head velocity sensitivities during passive head-on-body rotations were similar to those measured during passive whole-body rotations, regardless of whether the monkey was redirecting or stabilizing its gaze (Fig. 10B, compare black
columns with gray columns).
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Figure 10.
Response of VO neurons to passive rotation of the
head-on-body. A, The experimenter (hand
in schema) passively rotated the monkey's head relative
to its earth stationary body. The discharge of example neuron (unit
br31_2) was reliably predicted by the sensitivity of the
neuron to pWBR (thick trace). Bottom
left panel, Relationships between neural modulation
() and residual modulation (; total discharge  B-related modulation) and head-in-space motion
(where S = B).
B, For our sample of VO neurons, responses during
passive head-on-body rotation were comparable with those resulting
passive whole-body rotation [pWBR (used for normalization) and pWBRc
(leftmost black column)], regardless of whether the
monkey was redirecting (black columns) or stabilizing
(gray column) its gaze. Error bars show SEM.
Abbreviations as in Figure 1.
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Likewise, passive activation of neck proprioceptors did not influence
the discharges of V-pause neurons. When the monkey's head was held
stationary and its body was rotated beneath it, neuronal sensitivities
to neck velocity were negligible [sample of n = 4;
mean, 0.06 ± 0.02 (spikes/sec)/(°/sec)]. Moreover, during passive rotation of the head-on-body, the head velocity-related modulation of V-pause neurons was comparable with that observed during
passive whole-body rotation (n = 7; p > 0.4).
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DISCUSSION |
Previous studies in squirrel monkey have demonstrated that VO
neurons differentially encode head motion during passive rotation and
the active head movements that are generated during gaze shifts (Boyle
et al., 1996; McCrea et al., 1996, 1999). In contrast, a previous
investigation of VO neurons in rhesus monkey (Khalsa et al., 1987) had
reported that neurons similarly encode head velocity signals during
passive whole-body rotation and gaze pursuit, suggesting a species
difference. Here we found that neuronal responses in rhesus monkey were
attenuated by, on average, ~70% during gaze shifts, a finding that
is consistent with the previous studies in squirrel monkey.
Furthermore, we showed that VO neurons demonstrate comparable
attenuation during self-generated head-on-body movements made when the
premotor saccadic burst generator is not active: immediately after gaze
shifts and during gaze pursuit (Fig.
11A, compare
black columns). The discrepancy between our study and that
of Khalsa et al. (1987) may be the result of two factors: a sampling
bias in their data set and/or a difference in the analysis approach.
First, it is possible that these investigators inadvertently excluded
the VO neurons that showed the greatest attenuation by assuming that
they had lost neuronal isolation during the transition from the
head-restrained to head-unrestrained condition. Indeed, we were
initially concerned that this might have been the case in the present
study and were therefore careful to confirm neuronal isolation (see
Materials and Methods). Second, these authors used a regression
analysis to relate mean firing frequencies to mean head velocities,
whereas we used a more sensitive dynamic analysis method to quantify VO
neuron discharges. Thus, if their data set included only those VO
neurons that showed the least attenuation, it is possible that their
analysis was not sufficient to provide evidence that neuronal head
velocity sensitivities were altered.
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Figure 11.
Vestibular reafferent information is
differentially processed at the level of the vestibular nuclei.
A, The responses of VO neurons were significantly
suppressed during voluntary head-on-body movements (black
columns) compared with pWBR (gray
columns). Similarly, when monkeys made voluntary head-on-body
movements during passive rotation, neuronal responses to the voluntary
component (open column) remained attenuated, whereas the
responses to the passive component (horizontally striped column) remained encoded. In
contrast, neurons continued to encode head-in-space motion when the
head was passively rotated on the body (diagonally striped
column) and when the monkey generated voluntary head-in-space
motion by driving the motion of the vestibular turntable
(vertically striped column). Error bars show SEM.
B, Proposed mechanism for the selective processing of
vestibular information by VO neurons during voluntary head-on-body
motion. An efferent copy of the neck motor command (voluntary
B) is subtracted from the vestibular
afferent-related signal (S) at the level of
either the semicircular canals (A), presynaptic
to the VO neurons (B), and/or at the VO neuron
itself (C). Neither neck proprioceptive
information nor knowledge of self-generated head-in-space motion
contributes to the differential processing of self-generated
head-on-body motion. (Note that the hypothetical pathways that have
been eliminated are indicated by X.) C,
Alternatively, an efference copy of the neck motor command could
function to selectively gate in inhibitory neck proprioceptive
inputs.
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In the present study, we also describe the behavior of a second class
of vestibular nuclei neurons, V-pause neurons, that differed from VO
neurons in that their sensitivity to head velocity information is
reduced to a much greater extent during gaze shifts than during other
active motion of the head-on-body. We propose that the preferential
suppression of V-pause neuron responses during gaze shifts is mediated
via two mechanisms: one similar to that of VO neurons and the other a
suppression of activity by the saccadic burst generator (Cullen and
Guitton, 1997b). This latter mechanism could be mediated, in part, by
projections of premotor burst neurons to type II vestibular neurons
(Sasaki and Shimazu, 1981), which in turn send inhibitory projections
to neurons within the vestibular nucleus (Shimazu and Precht, 1966).
However, this pathway is unlikely to contribute to the attenuation of
VO neuron head velocity responses given that they are similarly reduced for all active head-on-body movements.
Negligible role of neck afferent inputs
Our finding that the activation of neck proprioceptors did not
significantly influence the firing patterns of VO neurons was unexpected in light of previous studies (McCrea et al., 1996, 1999;
Gdowski and McCrea, 1999). These studies reported that in squirrel
monkey most, if not all, secondary vestibular neurons (including VO
neurons) are sensitive to passive rotation of the neck. In contrast, we
used a comparable experimental approach and concluded that passive
activation of neck proprioceptors had little effect on VO responses in
rhesus monkey. We found that (1) passive rotation of the monkey's head
on its body elicited responses comparable with those elicited by
passive whole-body rotation (Fig. 11A,
diagonally striped column), and (2) VO neurons were not
sensitive to passive rotation of the monkeys body under its stationary
head. We propose that the discrepancy between our results and those of
McCrea and colleagues might result from either of two factors. First,
squirrel monkeys have a relatively small oculomotor range
(approximately ±20°) (Cullen et al., 1991) compared with humans and
rhesus monkeys (approximately ±50°) and thus rely more heavily on
head motion to redirect gaze. Therefore, it is conceivable that neck
proprioception information is processed differently in the two species.
Second, because these investigators did not measure neck torque during
the paradigms they used to passively activate neck proprioceptors, the
possibility that the monkeys generated some resistance (i.e., a
non-negligible efference copy signal) cannot be ruled out.
Neck efference copy and the principle of reafference
Our results are consistent with von Holst and Mittelstaedt's
(1950) original idea of reafference, in which an efference copy signal
is combined with the vestibular afferent signal to selectively remove
the reafferent component caused by the monkey's behavior. We propose
that attenuation is mediated by a direct efference copy of the neck
motor command input to the VO neurons (Fig. 11B) or
alternatively by efference copy signal that functions to selectively "gate in" inhibitory neck proprioceptive inputs (Fig.
11C). However, the site of this behaviorally dependent
gating of vestibular information is, as yet, unknown. Modulation of
sensory information could occur at the level of the semicircular canals
themselves (Fig. 11B, site A) via the
vestibular efferent system. It is possible that this efferent feedback
is used to tune the sensitivity of the vestibular nerve (or a subset of
afferents) to voluntary head-on-body movements (Goldberg and Fernandez,
1980). Although this idea is supported by the finding that the toadfish
efferent system selectively modulates the activity of afferent fibers
during self-motion (i.e., swimming behavior; Highstein, 1992), it has
not been tested in primates. Conversely, modulation may occur in the
vestibular nucleus itself, either presynaptically (Fig.
11B, site B) or at the level of
second-order vestibular neurons (Fig. 11B, site
C). Additional experiments are needed to determine the location of
the behaviorally dependent modulation. Additional experiments will also
be required to determine whether vestibular reafference is suppressed
during other naturally occurring behaviors. Although neurons responded
robustly during the cognitively demanding driving task (Fig.
11A, vertically striped column), it is
possible that, during locomotion and/or combined eye-head-body gaze
shifts, the motor efference signals generated by the activation of the
head, torso, and limb musculature might collectively influence the
response of vestibular nuclei neurons to self-generated head motion in
space. Pending the results from these experiments, we suggest that a
more suitable name for VO neurons would be vestibular reafference gated
(VRG) neurons.
Behaviorally dependent modulation in the vestibular nucleus
The attenuation of head velocity signals encoded by VO neurons was
similar during all active head-on-body movements, regardless of whether
the animal was stabilizing its gaze or redirecting its gaze to a new
point in space. For example, the head movement sensitivity of VO
neurons is attenuated not only during combined eye-head gaze shifts
(Fig. 2A, filled arrows) and pursuit (Fig. 3A) but also immediately after gaze shifts, when gaze is
stable in space but the head is still moving (Fig.
2A, open arrows). In contrast, the head
velocity-related activity of another class of vestibular nuclei
neurons, VOR interneurons (i.e., position-vestibular-pause neurons that also receive direct inputs from the vestibular nerve but
project to the extraocular motor nuclei) is attenuated only while
gaze is being redirected in space (Roy and Cullen, 1998), regardless of
whether the head motion is actively or passively generated. The
difference in behaviorally dependent modulation of these two cell types
is consistent with the their role in mediating the vestibulo-collic
reflex (see below) and VOR, respectively.
Functional implications
Emerging evidence suggests that the VCR, a reflex that functions
to stabilize the head in space via activation of the neck musculature
during head motion, is mediated, at least in part, by VO neurons that
project directly to the ventromedial funiculus of segments C1-C2 of
the spinal cord (Wilson et al., 1990; Boyle et al., 1996; Gdowski and
McCrea, 1999). Because the stabilization response produced by the VCR
would be counterproductive during voluntary behaviors in which an
animal's goal is to move its head on its body, it would be logical to
selectively attenuate VO neuron responses to voluntary head-on-body
movements. Accordingly, the VCR would be effectively suppressed for
self-generated head motion but would remain responsive to unexpected
perturbations of the head. Indeed, we found that, when a monkey
actively rotates its head on its body while undergoing passive
whole-body rotation, VO neurons continued to encode the passive
component (S) of the head-in-space
movement (Fig. 11A, horizontally striped
column). This result is in agreement with previous studies (Boyle
et al., 1996; McCrea et al., 1999). Furthermore, we discovered for
combined active and passive head motion that neuronal responses to the component of head-in-space velocity produced by active head-on-body motion were weak and comparable with those observed during active head-on-body motion in the absence of simultaneous passive rotation (Fig. 11A, compare open columns with black
columns).
The information encoded by VO neurons could also be combined with other
vestibular pathways to produce an estimate of our current orientation
in space during self-generated motion. VO neurons are well situated
within extensive cerebellar and cortical recursive networks. The
nodulus-uvula of the cerebellum receives inputs from vestibular
afferents (Korte and Mugnaini, 1979) and is thought to be reciprocally
connected to VO neurons (Wylie et al., 1994; Voogd et al., 1996; Wearne
et al., 1998). The transformation of head-centered motion information
into an inertial (gravity-centered) coordinate frame requires the
nodulus-uvula (Angelaki and Hess, 1995; Wearne et al., 1998). In
addition, many cortical areas involved in spatial representation,
navigation, and gaze control receive vestibular information and in turn
project back to the vestibular nuclei (for review, see Fukushima,
1997). For example, posterior parietal neurons have been shown to
encode body-referenced and world-referenced information in two separate
streams (Snyder et al., 1998) and project via direct and polysynaptic
pathways to the vestibular nuclei (Faugier-Grimaud and Ventre, 1989).
Indeed, it has been suggested recently that VO neurons transform
vestibular head-in-space information into body-in-space coordinates
(Gdowski and McCrea, 1999). However, although this proposal is
consistent with the observation that VO neurons reliably encode passive
head-in-space motion during simultaneous passive whole-body rotation
and active head-on-body motion, it cannot account for our finding that
neurons continue to encode head-in-space velocity during passive
rotation of the head on a stationary body. Thus, VO neurons do not
simply transform head-in-space signals into body-in-space coordinates but rather encode vestibular information from which self-generated head-on-body motion has been selectively eliminated. We suggest that
this behaviorally dependent processing of vestibular information contributes to both the control and maintenance of posture and the
computation of an internal estimate of spatial orientation.
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FOOTNOTES |
Received Oct. 16, 2000; revised Dec. 22, 2000; accepted Dec. 22, 2000.
This study was supported by the Medical Research Council of Canada. We
thank Drs. D. Guitton, D. Watt, and G. Mandl for many helpful
discussions, P. A. Sylvestre, M. Huterer, and A. Dubrovsky for
critically reading this manuscript, and M. Drossos, W. Kucharski, J. Knowles, and A. Smith for excellent technical assistance.
Correspondence should be addressed to Kathleen E. Cullen, Aerospace
Medical Research Unit, 3655 Drummond Street, Montreal, Quebec, Canada
H3G 1Y6. E-mail: cullen{at}med.mcgill.ca.
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ABSTRACT
INTRODUCTION
