1Department of Neurobiology, Pharmacology, and Physiology, University of Chicago, Chicago, Illinois 60637; and 2Neuro-Sensory Research Center/Oregon Health Research Center, Oregon Health Science University, Portland, Oregon 97201
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ABSTRACT |
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McCrea, Robert A., Greg T. Gdowski, Richard Boyle, and Timothy Belton. Firing Behavior of Vestibular Neurons During Active and Passive Head Movements: Vestibulo-Spinal and Other Non-Eye-Movement Related Neurons. J. Neurophysiol. 82: 416-428, 1999. The firing behavior of 51 non-eye movement related central vestibular neurons that were sensitive to passive head rotation in the plane of the horizontal semicircular canal was studied in three squirrel monkeys whose heads were free to move in the horizontal plane. Unit sensitivity to active head movements during spontaneous gaze saccades was compared with sensitivity to passive head rotation. Most units (29/35 tested) were activated at monosynaptic latencies following electrical stimulation of the ipsilateral vestibular nerve. Nine were vestibulo-spinal units that were antidromically activated following electrical stimulation of the ventromedial funiculi of the spinal cord at C1. All of the units were less sensitive to active head movements than to passive whole body rotation. In the majority of cells (37/51, 73%), including all nine identified vestibulo-spinal units, the vestibular signals related to active head movements were canceled. The remaining units (n = 14, 27%) were sensitive to active head movements, but their responses were attenuated by 20-75%. Most units were nearly as sensitive to passive head-on-trunk rotation as they were to whole body rotation; this suggests that vestibular signals related to active head movements were cancelled primarily by subtraction of a head movement efference copy signal. The sensitivity of most units to passive whole body rotation was unchanged during gaze saccades. A fundamental feature of sensory processing is the ability to distinguish between self-generated and externally induced sensory events. Our observations suggest that the distinction is made at an early stage of processing in the vestibular system.
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INTRODUCTION |
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An accurate view of the external world depends on
the ability to distinguish between sensory experiences produced by
external forces and sensory events that are produced by self-generated movements. The distinction presumably is made by comparing sensory signals with an internal estimate of the sensory consequences of
self-generated movements (Grüsser 1986;
Mergner et al. 1997
; von Helmholtz 1867
;
von Holst and Mittelstaedt 1950
). The internal estimate
generally is considered to be constructed from efference copy signals
and proprioceptive reafferent sensory inputs (von Holst and
Mittelstaedt 1950
). The interaction between efference copy and
sensory reafferent signals clearly occurs at cognitive levels of
sensory processing (Anderson et al. 1997
; von
Helmholtz 1867
). However, the interaction also may occur at
early stages of sensory processing (Bell et al. 1997
;
Duffy and Lombrosco 1968
; Ghez and Pisa
1972
; von Holst and Mittelstaedt 1950
). The best known example of such early interaction occurs in muscle spindles, where the signals carried by gamma motoneurons related to active muscle
contractions modify signal transduction within the spindle itself and
allow it to respond primarily to external forces that stretch it
(Burke et al. 1980
; Vallbo 1981
).
In the vestibular system, the distinction between sensory events that
are related to active, voluntary head movements and passive head
movements is important for perception of spatial orientation and for
postural control (Blouin et al. 1998; Howard 1997
; Merfeld et al. 1993
; Mergner et al.
1997
; von Holst and Mittelstaedt 1950
). For
example, the sensory signals transduced in the crista ampullaris of the
semicircular canal are related to angular head rotation
(Goldberg and Fernandez 1971
), but these signals are
processed in different ways during active and passive head movements.
Active head rotation in the dark is usually not accompanied by a sense
of self-motion, but passive rotation of the head or body produces a
subjective sensation of self-motion (Howard et al. 1998
;
Mergner et al. 1983
). Passive rotation of the head in
space produces reflexive eye, neck, and limb movements (Wilson
and Melvill Jones 1979
), but reflexive movements are usually absent during active head movements (von Holst and Mittelstaedt 1950
). These behavioral and psychophysical observations suggest that semicircular canal vestibular signals are modified by efference copy and/or proprioceptive signals related to active head movements. One question is whether this interaction occurs at an early stage of
sensory processing
at secondary vestibular neurons in the vestibular nuclei that receive direct inputs from the vestibular nerve.
This paper focuses on the processing of vestibular signals by non-eye
movement related vestibular neurons, including antidromically identified vestibulo-spinal neurons, during active head rotations generated during gaze saccades. We present evidence that vestibular reafferent signals related to active self-generated head movements are
canceled or attenuated, whereas signals related to passive head
movements are largely unaffected by active head movements. A
preliminary report has been published elsewhere (Boyle et al. 1996).
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METHODS |
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Surgical preparation
Three adult squirrel monkeys were prepared for chronic
recordings of eye and head movements, single-unit activity, and
electrical stimulation of both labyrinths. Most methods are described
in detail elsewhere (Gdowski and McCrea 1999). A small
bolt was attached to the cranium with dental acrylic so that the head
could be restrained during experiments. Labyrinthine stimulating
electrodes were implanted bilaterally in the middle ears. A scleral
search coil was implanted on one eye so that eye movements could be
recorded with the magnetic search coil technique. Stimulating
electrodes made of Teflon-coated platinum wire (75 µm), exposed ~1
mm from their tips, were implanted through a small opening in the dura
into the ventromedial funiculus of the spinal cord on both sides of the
midline at C1 (Boyle 1993
; Boyle et al.
1996
) in two animals. The electrodes were attached to the dura
with a spring interface and cemented to the occipital bone. The
location of the spinal electrodes in both animals was verified histologically.
Experimental setup
The experimental apparatus is illustrated in Fig. 1A. The monkey was seated in a Plexiglas box on a vestibular turntable (a) that was surrounded by a cylindrical screen (not shown). The head was attached to a rod that rotated within a ball bearing assembly (f) that was fixed to the turntable. The rod's rotational axis was coincident with the turntable's rotational axis and was positioned at the level of the external auditory meatus within 5 mm of C1-C2 axis of rotation. The apparatus allowed the monkey to generate angular head movements (±40°) in the plane of the horizontal semicircular canal. A harness (c) was placed over the animal's shoulders to restrict body movements and to align its trunk toward the screen. Slight pitch and roll postural adjustments were accommodated with a universal joint (e) that was located in-line with the rod above the animal's head (7 cm). Passive whole body rotation with the head-fixed was accomplished by preventing the rod from rotating during turntable rotation (Fig. 1A, center inset). Active head movements were prevented by locking the rod in place with a block (i) and by disabling the universal joint with a rigid sleeve (h). Passive head on trunk rotation was produced by rotating the rod manually or with a motor (j) mounted on the ceiling (Fig. 1A, right inset). Head position was measured with a search coil (k) placed on the rod below the universal joint. Angular turntable velocity was recorded with an angular velocity sensor (Watson). Animals were trained to fixate and pursue visual targets that were laser projected onto the screen from the turntable with mirror galvanometers. Head, eye, turntable and target position signals were sampled at 200-500 Hz and saved on a computer for off-line analysis.
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Single-unit recording
A micromanipulator was used to stereotaxically insert an
epoxy-insulated tungsten microelectrode (4-7 M) attached to a
hydraulic microdrive into the cerebellum through a guide tube (22G).
The electrode and microdrive were then secured to the skull.
Microelectrode location in the vestibular nuclei was determined by
monitoring the synaptic field potentials evoked by shocking the
ipsilateral vestibular nerve (0.1 ms monophasic perilymphatic cathodal
pulses, 50-300 µA). The relative location of the microelectrode
within the vestibular nuclei was estimated based on the location of
other identified physiological landmarks in the brainstem such as the vestibular nerve, the abducens nucleus, and the nucleus of the solitary
tract. Most of the units included in this study were estimated to be
located in regions of the vestibular nuclei approximately 0.5-3 mm
caudal to the abducens nucleus and 3-5 mm from the midline (see
Gdowski and McCrea 1999
for details). Units were
considered to receive monosynaptic input from the vestibular nerve if
spike potentials were evoked at latencies
1.3 ms with currents that were at the threshold of evoking responses. Units were tested for
antidromic activation following electrical stimulation of the spinal
cord (0.1-ms monophasic pulses, 50-250 µA). They were considered to
be activated antidromically if spikes were evoked at constant latencies
near the threshold current and collided with synaptically evoked spikes
or spontaneously occurring spikes.
Action potentials (AP) of single units were time marked with a real time clock (0.1 ms resolution) after they were amplified conventionally and discriminated with a dual window discriminator (Bak). Unit recordings were discontinued if the signal-to-noise ratio was low (<2). Unit discharge rates were computed for each A/D sample (binwidth 2-5 ms) using a time-symmetric algorithm in which discharge rate was computed from the occurrence of spikes immediately before, after, and during the sample.
Experimental protocol
Whole body rotation (WBR) was used as a search stimulus as the
electrode was advanced toward the vestibular nuclei. The firing behavior of single units was studied during passive WBR with the head
restrained and with the head free to move. Unit responses during active
head movements typically were recorded for several minutes while the
monkey generated spontaneous gaze saccades in the absence of a target.
The head movements generated during gaze saccades had peak head
velocities 400°/s. The distribution of peak head velocity and
acceleration of gaze saccades recorded concomitantly with single-unit
recordings in the three animals is illustrated in Fig.
2.
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Unit responses during active gaze shifts were compared with responses during passive whole body rotation and passive forced head and neck rotation (Fig. 1B). Ideally, the unit response during active head movements produced during gaze saccades would have been compared with the unit's response during a step change in turntable position that had a similar acceleration and velocity. However, this was not possible because the turntable's maximum acceleration (~350°/s2) was significantly lower than the peak head acceleration of most gaze saccades. Alternatively, the active head movement responses were compared with responses recorded during sinusoidal WBR at 0.5 Hz (peak velocity 40°/s) and 2.3 Hz (20°/s). The higher frequency stimulus had the higher peak acceleration (289°/s2) and was used to estimate unit sensitivity to passive head movement. The responses of most units also were recorded during passive sinusoidal head on trunk rotation. In some units, passive head on trunk velocity trapezoids (50-100°/s peak velocity, 1,200-3,700°/s2 peak acceleration) were produced with the ceiling motor.
Data analysis
Unit sensitivities to head and eye position were assessed from 40 to 120 records of steady fixation when the head was free and when the head was restrained. Eye position sensitivity was assessed with a multiple regression analysis of the mean firing rate against vertical and horizontal eye position. Unit sensitivity to eye velocity was assessed from records of ocular saccades and from records of sinusoidal (typically 0.5 Hz, 40°/s peak velocity) smooth pursuit eye movements. The firing rate of the units included in this study was poorly correlated with eye position during periods of steady fixation and was not modulated during smooth pursuit eye movements. Sensitivity to head position was assayed in non-eye movement related neurons by linear regression of firing rate versus horizontal head position.
UNIT SENSITIVITY TO PASSIVE HEAD ROTATION IN SPACE DURING WBR.
Unit sensitivity to passive horizontal head rotation was assessed from
responses during 2.3 Hz whole body rotation. The records were edited to
include only epochs when the monkey was alert and to eliminate records
related to quick phases of nystagmus. The gain and phase of unit
responses were determined by regressing a sinewave function to an
average of 25 stimulus cycles. The rotational response was expressed
as a first-order differential equation based on head velocity
(gv) and head acceleration
(ga).
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(1) |
UNIT SENSITIVITY TO ACTIVE HEAD ROTATION DURING GAZE SACCADES. Spontaneous saccades were identified as gaze shifts with high peak accelerations (>1,000°/s2). A database of the gaze saccades recorded with each unit was compiled that included the starting eye and head positions, direction, final eye and head position, peak head and gaze velocity, time-to-peak head and gaze velocity, and duration of the gaze and head movements. Groups of saccades that had similar characteristics were aligned and averaged with respect to saccade onset, peak gaze velocity, peak head velocity, or the end of the saccade. In this study, unit responses were quantified primarily by averaging responses during saccades with similar peak head velocity.
The active head movement responses were usually assessed during gaze saccades that had peak head velocities between 50 and 150°/s. Unit discharge rate during active head movements was modeled with Eq. 1. Since units were less sensitive to active head movement than to passive head movement, a quantitative estimate of the attenuation (A) in sensitivity to head rotation during active head movements was made with the following equation:
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(2) |
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RESULTS |
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The majority (43/51) of the horizontal canal-related vestibular nucleus units included in this study had discharge rates that were not correlated with eye position or with eye velocity during fixation, saccades, or pursuit eye movements. Eight units also were included that were inhibited weakly during most ocular saccades but were not otherwise sensitive to eye movements. Approximately half of the units (26/51) were related to ipsilateral head velocity during WBR (type I units), and the remaining 25 units were related to contralateral head velocity (type II units).
Most units tested (29/35; 16/17 type I, and 13/18 type II) were
monosynaptically activated following electrical stimulation of the
ipsilateral vestibular nerve. Nine units, including four type I units
and five type II units, were antidromically activated following
electrical stimulation of C1. Three of the antidromically identified
vestibulo-spinal units were inhibited during saccades. Orthodromic and
antidromic evoked spikes of a vestibulo-spinal unit are illustrated in
Fig. 3. Stimulation of the ipsilateral vestibular nerve evoked short-latency spikes (0.7-1.3 ms), which suggested that the cell received monosynaptic inputs from the vestibular nerve. Spikes also were evoked at a constant latency (0.5 ms) following stimulation of the ventromedial funiculus of the spinal
cord at C1. These were considered to be evoked antidromically because
they were blocked by spontaneous or vestibular nerve evoked spikes that
occurred just before the C1 stimulus (Fig. 3, dashed trace). The
records illustrated in Figs. 4, 7, and 10A were from this
cell. The records illustrated in Figs. 5, 6, and 10B were obtained from other vestibulo-spinal units. Most units were estimated to be located in the midregion of the vestibular nuclei, just caudal to
the entrance of the vestibular nerve (for details, see Gdowski
and McCrea 1999).
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Unit responses to WBR
All units in this study were sensitive to angular head velocity (>0.2 sp/s/1/°/s re head velocity in space) during passive WBR in the plane of the horizontal semicircular canals. WBR responses usually were recorded at two frequencies (0.5 and 2.3 Hz). Type I units tended to be more sensitive to WBR than type II units. At 2.3 Hz, type I units had an average gain of 0.99 ± 0.15 sp/s/°/s re head velocity, whereas the average gain of type II units was 0.57 ± 0.06 sp/s/°/s. The rotational responses typically phase led head velocity. The mean phase lead was 16.9 ± 3.0° for type I units and 21.7 ± 4.3° for type II units.
Active head movement responses
Vestibular units were less sensitive to horizontal head movements
during gaze saccades than during WBR or during forced head on trunk
rotation. In most (37/51) units, sensitivity to active head movements
during gaze saccades was reduced by 80%. These units will be
referred to as canceled units. The remaining 14 units were sensitive to
active head movements during gaze saccades, but their vestibular
signals were attenuated by 20-75% during active head movements in one
or both directions. These units will be referred to as attenuated
units. Each of the two unit classes is described in detail below.
CANCELED UNITS. Most of the 37 units whose head movement signals were canceled during gaze saccades were activated at a monosynaptic latency after electrical stimulation of the ipsilateral vestibular nerve (19/24 tested). Sixteen of the units had type I responses during WBR and 21 had type II responses. The secondary canceled units included all nine of the antidromically identified vestibulo-spinal neurons. On average, the responses of canceled units to WBR at 2.3 Hz had a gain of 0.77 ± 0.08 sp/s°/s and phase led head velocity by 22 ± 4°.
The firing behavior of a vestibulo-spinal neuron during passive and active head movements is shown in Fig. 4. Figure 4A shows the unit's response during five WBR cycles while head movements were restrained. The averaged response recorded over 88 stimulus cycles is shown in Fig. 4B. The peak velocity of the sinusoidal rotation was 21°/s, and the peak modulation in unit firing rate was 20.6 sp/s. The unit's response phase led head velocity by 29.3°. The solid line superimposed on the unit histogram in Fig. 4B is a model of firing rate based on estimated sensitivity to head velocity (gv = 0.86 sp/s/°/s) and head acceleration (ga = 0.042 sp/s/°/s2).
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ATTENUATED UNITS. Fourteen units (11 type I and 3 type II) were sensitive to active head movements during gaze saccades, although the head movement response was attenuated. Most attenuated units were activated monosynaptically following electrical stimulation of the ipsilateral vestibular nerve (10/11 tested), and none of the three units tested was antidromically activated after electrical stimulation of the spinal cord. On average, the WBR responses of attenuated units at 2.3 Hz had a gain of 0.67 ± 0.10 sp/s/°/s and phase led head velocity by 18 ± 4°.
The type II unit, illustrated in Fig. 8, was more sensitive to active head movements than any other unit, but its response was attenuated during active head movements in one direction. The neuron was activated at a monosynaptic latency after electrical stimulation of the vestibular nerve. A model derived from its WBR response (Fig. 8A, solid line) is superimposed on its responses during active head movements produced during gaze saccades (Fig. 8, B and C). During contralateral, vestibular ON-direction gaze saccades (Fig. 8B), the unit's firing rate was close to the response predicted from its sensitivity to passive head movement. However, during OFF-direction saccades (Fig. 8C), the unit's response was smaller than predicted. The reduction in head movement sensitivity of all attenuated units ranged from 20 to 75%. Most units had attenuated responses during both ipsi- and contralateral saccades but half of the units had asymmetric attenuations. In those cells, like the unit illustrated in Fig. 8, the response attenuation was 15-40% greater during OFF-direction gaze saccades than during active head movements in the ON-direction. On average, the response attenuation of attenuated units was larger for head movements in the vestibular OFF-direction (A = 0.46 ± 0.05; n = 14) in comparison with the response attenuation for head movements in the ON direction (A = 0.29 ± 0.05). In most attenuated units, attenuated responses during saccades could be reasonably fit by assuming the reduction in response was produced by the addition or removal of an input whose dynamic characteristics were similar to WBR signals.
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Effects of saccade amplitude on unit discharge rates
In Fig. 10, the discharge rates of a canceled unit (A), a canceled unit that was inhibited during gaze saccades (B), and an attenuated unit (C) are plotted as a function of peak head velocity during gaze saccades of different amplitudes made in both directions.
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In the plots, each point is the unit discharge rate at the time of the peak head velocity during a gaze saccade; dashed line in each of the figures indicates spontaneous firing rate (labeled SR). The expected responses based on each unit's sensitivity to head velocity during WBR are plotted as solid line. The canceled vestibulo-spinal unit (Fig. 10A) was insensitive to saccades in either direction, regardless of their peak head velocity, and had peak firing rates that were distributed about its spontaneous rate. The discharge rate of the inhibited vestibulo-spinal unit (Fig. 10B) was usually less than the spontaneous rate regardless of the peak head velocity of the active head movement. The attenuated unit (Fig. 10C) had responses that changed proportionally with changes in head velocity in space, but these responses were smaller than would have been predicted from the unit's WBR response during large head movements in the units ON-direction and larger than predicted during many OFF-direction saccades.
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DISCUSSION |
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The main finding in this study is that the vestibular signals carried by secondary non-eye movement related neurons in the vestibular nuclei are modified during active head movements. The sensory signals related to active head movements were effectively canceled in most of these neurons, including all of the vestibulo-spinal neurons that were identified. Sensitivity to passive head rotation was preserved. Some units were sensitive to active head movements, but their responses were attenuated and directionally asymmetric. Thus, the head movements that accompany voluntary gaze shifts strongly affect sensory processing in the vestibular nuclei.
The change in unit sensitivity to vestibular stimulation was in part due to neck proprioceptive reafferent inputs that were demonstrable during passive head-on-trunk rotation. However, these proprioceptive inputs were usually too weak to account for the suppression of vestibular signals in canceled units. An additional input, presumably an efference copy of neck motor commands, is apparently also used to cancel vestibular signals related to self-generated head movements.
In the following discussion, we briefly review previous studies of vestibular unit responses during gaze saccades. We then will discuss the possible mechanisms responsible for modifying vestibular signals during active head movements and the role non-eye movement units may have in different central vestibular functions. We will focus particularly on the mechanisms involved in canceling vestibular signals on vestibulo-spinal neurons and the functional implications of this cancellation for the vestibulo-collic reflex.
Previous studies of vestibular unit responses during gaze saccades
Attenuation of the responses of non-eye movement
vestibular units during gaze saccades has been described in several
previous studies. Fuller (1978, 1988
, 1992
) found that
units in the vestibular nuclei exhibited a variety of responses during
gaze saccades and noted that most units received neck proprioceptive
inputs that could add destructively with vestibular signals during
active head saccades. He also observed that units remained sensitive to
passive perturbations of the head during gaze saccades. Khalsa and colleagues (1987)
described several non-eye movement
related vestibular units and a cerebellar unit that had head movement related signals during gaze saccades. Although they stressed the similarity of unit responses during active and passive head movements, they found that the slope of the regression of firing rate versus peak
head velocity was smaller during active than during passive head
movements. The regression of firing rate versus peak head velocity for
a "pure" vestibular unit they illustrated (Khalsa et al.
1987
, Fig. 4) was similar to the attenuated units of this study
(Fig. 10C). This group also presented evidence that some primate vestibular neurons receive neck proprioceptive inputs (Khalsa et al. 1988
). Phillips and colleagues
(1996)
described the firing behavior of four pure vestibular
neurons in the rhesus monkey. They found that the average head-velocity
sensitivity of those units was reduced during active gaze saccades
compared with their response during passive WBR, but that their
sensitivity to head acceleration was increased. The result suggested
that the neck movement input to those cells had different dynamic
characteristics than their vestibular inputs.
The firing behavior of eye movement related vestibular neurons during
active head movements also has been studied (Fuller et al.
1983; Khalsa et al. 1987
, 1988
; McCrea et
al. 1996
; Phillips et al. 1996
; Roy and
Cullen 1998
). Eye movement related neurons carry information
regarding vestibular signals and in addition also carry signals related
to ocular saccades, smooth pursuit eye velocity, eye position, neck
position, retinal image slip, and viewing distance. Consequently, the
assessment of their vestibular sensitivity during gaze saccades is much
more complex than the analysis of non-eye movement units. It is
sufficient to note that in the squirrel monkey eye movement related
secondary vestibular neurons receive neck proprioceptive inputs and
inputs related to active head movements that effectively cancel or
attenuate vestibular signals during gaze saccades (Gdowski and
McCrea 1997
; McCrea et al. 1996
).
How are the vestibular signals of non-eye movement units modified during gaze saccades?
There are several ways vestibular signals could have been attenuated or canceled during gaze saccades.
NECK REAFFERENCE.
Most vestibular neurons receive neck proprioceptive inputs whose
dynamics are such that they reduce the response to head rotation during
passive head on trunk movements (Anastasopoulos and Mergner 1982; Boyle and Pompeiano 1981
; Fuller
1988
; Wilson et al. 1990
). In this study,
passive head-on-trunk rotations at frequencies comparable with head
saccades usually evoked responses in canceled units, including units
whose signals were canceled during gaze saccades (Fig. 6). Therefore it
is unlikely that proprioceptive inputs from the neck alone were
responsible for the large reduction in sensitivity observed in most
units during gaze saccades.
PRESYNAPTIC AND POSTSYNAPTIC INHIBITION.
Presynaptic inhibition is another mechanism that may be responsible for
some of the reduction in vestibular sensitivity during gaze saccades.
Such interactions could occur as early as the vestibular sensory
epithelium or within the vestibular nuclei itself. Efferent vestibular
pathways from the CNS to the vestibular sensory epithelium are known to
modify the vestibular sensory signals transmitted by primary afferents
(Boyle and Highstein 1990; Brichta and Goldberg 1996
; Goldberg and Fernandez 1980
;
Highstein 1991
; Highstein and Baker
1985
). Efferent activation also directly hyperpolarizes horizontal canal hair cells and reduces their receptor potential modulation to canal stimulation (Boyle et al. 1998
).
Efferent vestibular neurons in the toadfish and guinea pig are
sensitive to behavioral arousal, and stimulation of neck and body
proprioceptors (Highstein 1991
; Marlinsky
1995
). Thus some of the neck movement sensitivity apparent in
the vestibular nuclei could be due to the effect of vestibular
efferents on vestibular afferent signals.
EFFERENCE COPY.
von Holst and Mittelstaedt (1950) suggested that the
computation of the difference between sensory afferent information and the expected sensory reafference produced by voluntary movement was a
fundamental feature of sensory processing. Sensory processing of
vestibular information in the context of postural reflexes was one of
several examples used by von Holst and Mittelstaedt to describe their
reafference principle, which is schematically illustrated in Fig.
11A. The descending central
command used to produce an active movement of an effector (EFF) was
viewed as being controlled by several hierarchical stages
(Z1...Zn). The output of
these stages generated an efferent command (E) that produced movement
of the effector and in addition produced sensory reafference signals
(A). To prevent reflexive movements from being generated as a
consequence of these sensory reafference signals, they were canceled by
subtraction of an efference copy (EC) of the expected sensory
reafferent signal produced by the voluntary movement. The difference
between the sensory signals related to active and passive movements (M)
is computed by subtraction of efference copy from the sensory
reafference. Von Holst and Mittelstaedt suggested that the difference
was often computed at the lowest, or earliest, stage of central
processing (Z1), and it represented an internal
estimate of sensory inputs produced by external forces or
perturbations. This estimate then could be used to adjust or correct
the central command, if necessary. We suggest that the firing behavior
of most canceled units during gaze saccades can be explained as the
difference between sensory reafferent inputs produced by active head
movements and an efference copy of neck motor commands (Fig.
11B).
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The role of non-eye movement units in different vestibular functions
Approximately half of the semicircular canal-related units we
encountered in the vestibular nuclei were non-eye movement units (Gdowski and McCrea 1999). There is little evidence that
these cells participate directly in producing the vestibulo-ocular
reflex, but they may be involved in several other important vestibular functions. They probably contribute to vestibulo-thalamic pathways because neurons in the vestibular cortex and associated regions of the
thalamus typically have discharge rates that are not related to eye
movements (Akbarian et al. 1993
1994
;
Büttner and Lang 1979
; Büttner et al.
1977
; Grüsser et al. 1990
; Magnin
and Fuchs 1977
). Canceled units would contribute to the
perceptual ability to distinguish passively induced movement of the
head or body in space from self-generated movements. Non-eye movement
related neurons also are thought to contribute to vestibular pathways related to velocity storage (Reisine and Raphan 1992
;
Yokota et al. 1992
) and to vestibulo-cerebellar pathways
(Waespe et al. 1981
, Zhang et al. 1993
).
Finally, many of the units that project to the spinal cord appear to be
non-eye movement units (Boyle 1993
).
The role of vestibulo-spinal units in producing the vestibulo-colic reflex
Vestibular reflexes tend to stabilize posture and oppose voluntary
movements (von Holst and Mittelstaedt 1950). These
reflexes need to be suppressed during active movements. The simple
solution would be to cancel the self-generated component of head
movement signals carried by vestibulo-spinal reflex pathways. The
results of this study suggest that vestibular signals related to
self-generated movements of the head on the trunk are canceled on many
vestibulo-spinal units.
The antidromically identified vestibulo-spinal units reported here
probably were related to the vestibulo-collic reflex (VCR). Horizontal
canal-related units that mediate the VCR have axons that descend to
cervical segments in the medial longitudinal fasciculus and the ventral
funiculus of the cervical spinal cord. The stimulating electrodes were
located in the ventral-medial funiculus and most of the identified
units were activated with low stimulus currents. In addition, the units
appeared to be located in the ventral lateral vestibular nucleus, which
is the region that contains medial vestibulo-spinal tract neurons in
the squirrel monkey (Boyle 1993; Minor et al. 1990
).
The VCR produces a compensatory head movement that tends to stabilize the position of the head in space during passive whole body rotation. A simple model of the role of the VCR in head movement motor control is illustrated diagrammatically in Fig. 11C. The figure illustrates the concept that VCR pathways construct an estimate of passive motion of the head in space that sums at segmental levels with active head movement commands to produce different combinations of voluntary and reflexive head movement. The estimate of passive head motion is constructed by subtracting an efference copy of saccade and reflex premotor commands from a semicircular canal estimate of the movement of the head in space. The diagram does not attempt to model all of the factors that contribute to compensatory VCR head movements. Many other factors, including neck stiffness, the inertial load of the head, and the position of the neck undoubtedly, play an important role in the VCR. Moreover, the medial vestibulo-spinal tract is not the only descending pathway that is involved in producing the VCR. Nevertheless it seems likely that the reflex was designed to compensate for passive external forces that perturb the stable posture of the head and deflect the trajectory of planned movements. Summation of vestibular and neck efference copy signals would allow the reflex to perform this function in a variety of behavioral circumstances.
Conclusion
The brain must distinguish between sensory events that are externally induced and those that are self-generated to develop an accurate perception of the external world and produce coordinated behavior. In the vestibular system, the distinction appears to be made by the first neurons in the brain that receive input from the vestibular nerve. Apparently, the recognition of self-generated and non-self-generated head movements is too important to be postponed until a later stage of sensory processing.
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ACKNOWLEDGMENTS |
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We thank J. Fuller and J. Goldberg for useful comments.
This work was supported by National Institutes of Health Grants R01-EY-08-041, DC-02072, and NS-27050.
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FOOTNOTES |
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Address for reprint requests: R. A. McCrea, Dept. of Neurobiology, Pharmacology, and Physiology, University of Chicago, 5806 S. Ellis Ave., Chicago, IL 60637.
The costs of publication of this article were defrayed in part by the payment of page charges. The article must therefore be hereby marked "advertisement" in accordance with 18 U.S.C. Section 1734 solely to indicate this fact.
Received 13 January 1999; accepted in final form 26 March 1999.
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REFERENCES |
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