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Rostral Fastigial Nucleus Activity in the Alert Monkey During ThreeDimensional Passive Head Movements
C. SIEBOLD, L. GLONTI, S. GLASAUER, AND U. BÜTTNER
Department of Neurology and Center for Sensorimotor Research, Ludwig Maximilians University,
D 81377 Munich, Germany
Siebold, C., L. Glonti, S. Glasauer, and U. Büttner. Rostral
fastigial nucleus activity in the alert monkey during three-dimensional passive head movements. J. Neurophysiol. 77: 1432–1446,
1997. The fastigial nucleus (FN) receives vestibular information
predominantly from Purkinje cells of the vermis. FN in the monkey
can be divided in a rostral part, related to spinal mechanisms, and
a caudal part with oculomotor functions. To understand the role
of FN during movements in space, single-unit activity in alert
monkeys was recorded during passive three-dimensional head
movements from rostral FN. Seated monkeys were rotated sinusoidally around a horizontal earth-fixed axis (vertical stimulation) at
different orientations 157 apart (including roll, pitch, vertical canal
plane and intermediate planes). In addition, sinusoidal rotations
around an earth-vertical axis (yaw stimulus) included different roll
and pitch positions ( {107, {207 ). The latter positions were also
used for static stimulation. One hundred fifty-eight neurons in two
monkeys were modulated during the sinusoidal vertical search
stimulation. The vast majority showed a uniform response pattern:
a maximum at a specific head orientation (response vector orientation) and a null response 907 apart. Detailed analysis was obtained
from 111 neurons. On the basis of their phase relation during
dynamic stimulation and their response to static tilt, these neurons
were classified as vertical semicircular canal related (n Å 79,
71.2%) or otolith related (n Å 25; 22.5%). Only seven neurons
did not follow the usual response pattern and were classified as
complex neurons. For the vertical canal-related neurons (n Å 79)
all eight major response vector orientations (ipsilateral or contralateral anterior canal, posterior canal, roll, and nose-down and noseup pitch) were found in FN on one side. Neurons with ipsilateral
orientations were more numerous and on average more sensitive
than those with contralateral orientations. Twenty-eight percent of
the vertical canal-related neurons also responded to horizontal canal stimulation. None of the vertical canal-related neurons responded to static tilt. Otolith-related neurons (n Å 25) had a phase
relation close to head position and were considerably less numerous
than canal-related neurons. Except for pitch, all other response
vector orientations were found. Seventy percent of these neurons
responding during dynamic stimulation also responded during
static tilt. The sensitivity during dynamic stimulation was always
higher than during static stimulation. Sixty-one percent of the otolith-related neurons responded also to horizontal canal stimulation.
These results show that in FN, robust vestibular signals are abundant. Canal-related responses are much more common than otolithrelated responses. Although for many canal neurons the responses
can be related to single canal planes, convergence between vertical
canals but also with horizontal canals is common.
INTRODUCTION
The cerebellum plays a major role in the processing of
vestibular signals. This does not only apply to the vestibu1432
locerebellum (flocculus, nodulus) but also to the vermis.
The vermis receives a major mossy fiber input from the
vestibular nuclei (Kotchabhakdi and Walberg 1978). The
Purkinje cells (P cells, the only output element of the cerebellar cortex) of the vermis project to the fastigial nucleus
(FN), the most medial deep cerebellar nucleus (Armstrong
and Schild 1978), and also directly to the vestibular nuclei
(Yamada and Noda 1987).
The anterior vermis (lobules I–V) is considered to be
part of the spinocerebellum. In contrast, lobuli VI and VII
of the posterior vermis receive a major pontine input (Yamada and Noda 1987) and are classified accordingly as pontocerebellum. These anatomic divisions are also reflected
in functional differences. Whereas the anterior vermis is
involved in spinal mechanisms (posture, neck, gait), lobuli
VI and VII of the posterior vermis play a role in oculomotor
functions (oculomotor vermis, Yamada and Noda 1987).
The P cells of the vermis project onto the ipsilateral FN
in a topographic fashion, i.e., the anterior vermis to the rostral FN and the posterior vermis to the caudal FN (Armstrong
and Schild 1978). Accordingly, a functional division can
also be demonstrated for FN by single-unit recordings under
natural conditions. Whereas eye movement (saccade,
smooth pursuit)-related neurons are encountered in the caudal FN (Büttner et al. 1991; Fuchs et al. 1993), neurons
in rostral FN exhibit no activity related to individual eye
movements, but respond to vestibular stimulation (Büttner
et al. 1991; Gardner and Fuchs 1975).
Most studies of the vestibular signals in FN have concentrated on stimulation in the horizontal plane around the Zaxis (yaw stimulation). Under these conditions the majority
of neurons in rostral FN exhibit a type II response (Büttner
et al. 1991; Gardner and Fuchs 1975) according to the nomenclature of Duensing and Schaefer (1958). These neurons
have no eye movement sensitivity and are classified as ‘‘vestibular-only’’ neurons. Neurons in caudal FN with vestibular
sensitivities generally also respond during smooth pursuit
eye movements, many of them encoding ‘‘gaze velocity’’
with little or no response during the vestibuloocular reflex
and an increased response during visual suppression of the
VOR (Büttner et al. 1991).
Under natural conditions, head movements are performed
in three-dimensional space and vestibular signals are generated accordingly. Very little is known about the central processing of three-dimensional vestibular signals beyond the
vestibular nuclei. Gardner and Fuchs (1975) reported that a
high percentage (75%) of vestibular-only neurons in rostral
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FIG . 1. Schematic drawing of the applied stimuli. Drawing of the monkey’s head includes ( A) approximate orientation
of the vertical canals and (B) and (C) approximate orientation of the horizontal canals. A: head orientations during vertical
dynamic stimulation. RALP, right anterior/left posterior; LARP, left anterior/right posterior. B and C: head orientations for
the static positions, which were also used in combination with yaw stimulation around the Z-axis. RED, right ear down;
LED, left ear down; NU, nose up; ND, nose down. During yaw stimulation with ND the horizontal canal is close to the
optimal stimulation plane.
FN were modulated during horizontal and pitch stimulation,
indicating some canal convergence. More systematic studies
have been performed in the vestibular nuclei. In the alert cat
it was found that most neurons received input from one canal
pair. Neurons with input from two canal pairs were more
common than those with input from all three canal pairs
(Baker et al. 1984a). About one third of the neurons had
more complex response properties and differed in their spatial orientation and dynamic properties (spatial-temporal
convergence) from canal responsive neurons, indicating canal-otolith interaction (Baker et al. 1984a,b).
The detailed studies from vestibular nerve afferents have
classified vertical canal plane (VCP) responsive neurons
(Goldberg and Fernandez 1984). According to this, the left
anterior and right posterior (LARP) canals lie in almost the
same plane of orientation, as do the right anterior and left
posterior (RALP) canals. Optimal activation occurs when
the nasooccipital axis is in the LARP or RALP plane ( b Å
0457 and /457, respectively) during stimulation around an
earth-horizontal axis (Fig. 1A). For the horizontal canal
(HC) pair, the optimal orientation during yaw stimulation
around the Z-axis in the monkey is during nose-down tilt of
g Å 157 (Fig. 1C) (Böhmer et al. 1985). With increasing
deviations from the optimal orientation the response declines
monotonically with a sine function to zero (null response)
when the canal plane is orthogonal to the optimal orientation.
The phase of the neuronal response is constant, and is close
to stimulus velocity except for a 1807 phase shift at the null
response. This applies for stimulus frequencies between 0.1
and 2 Hz. All other neuronal response characteristics (constant responses and varying phases at different orientations)
indicate spatiotemporal convergence with an (additional)
otolith input, as has been described for the vestibular nuclei
(Baker et al. 1984b).
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To fully understand the role of the cerebellum in the control of three-dimensional head-dependent movements and
other movements it is necessary to know what vestibular
information is present. Because detailed information on the
response pattern of rostral FN neurons during yaw stimulation is already available in the literature (Büttner et al. 1991;
Gardner and Fuchs 1975), we focused our investigation on
neuronal activity to natural vestibular stimulation in pitch,
roll, and intermediate planes, applying a pure vertical searching stimulus (pitch, roll, or VCP stimulation). In addition,
most neurons that responded to vertical dynamic stimulation
were tested subsequently for horizontal modulation. It will
be shown that many FN neurons carry a clear vestibular
signal, which can be related to individual canals. Many neurons also show a convergence either of different vertical
canals (VCs) or of HCs and VCs. Other neurons had an
otolith input. Only vestibular-only neurons will be considered. Preliminary data have been reported elsewhere (Büttner et al. 1996).
METHODS
Two monkeys (Macaca mulatta) were used for this study. Before surgery the monkeys were accustomed to sitting in a primate
chair and were trained to follow a small visual target (0.57 ) with the
eyes. Under general anesthesia and aseptic conditions, the monkeys
were chronically prepared for single-unit recordings (for details
see Boyle et al. 1985). In short, a recording chamber was implanted
(stereotaxic coordinates: mediolateral 0 mm, posterior 6 mm) to
allow a vertical approach in the stereotaxic plane of FN on both
sides. Horizontal, vertical, and torsional eye position was recorded
by a dual search coil system (Bartl et al. 1996) and neuronal
activity was recorded with varnished tungsten microelectrodes (impedance 2.5–4 MV ). During the experiment the head was immobilized by a head holder and the monkey sat with the head erect
(stereotaxic horizontal) in a primate chair.
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C. SIEBOLD, L. GLONTI, S. GLASAUER, AND U. BÜTTNER
Definitions of coordinates and directions
The directions of the head-fixed coordinate system are defined
according to the right hand rule, with positive values for leftward
movements around the Z-axis (yaw), downward movements
around the Y-axis (pitch), and right-ear-down movements around
the X-axis (roll). The attributes pitch/roll/yaw are used to indicate
head-fixed coordinates throughout the paper. Throughout the
manuscript we distinguish between VCP-related neurons, with the
best response during LARP and RALP stimulation, and VC-related
neurons, which includes also pitch and roll neurons.
The stimuli and the position of the monkey are described relative
to an earth-fixed coordinate system to indicate whether or not the
monkey was rotated around an axis parallel to gravity (earth-vertical axis rotation, no stimulation of the otoliths).
Vestibular stimulation
The primate chair was mounted on a rotating device with three
motor-driven axes of rotation. The innermost frame allowed rotations around the monkey’s Z-axis [angle b, used to rotate the
monkey to predefined positions (range {907, step size Db Å 157 )]
(Fig. 1). The medium frame rotated the primate chair around an
earth-horizontal axis (angle d, dynamic and static vertical stimulation). The outermost frame rotated the whole device around an
earth-vertical axis (angle d, dynamic horizontal stimulation). Three
different dynamic stimulation paradigms were applied (Fig. 1).
1) VC stimulation with earth-horizontal axis rotation in different
b positions. Sinusoidal rotations around the earth-horizontal axis
(angle d, referred to as ‘‘vertical stimulation’’ throughout the paper) caused pitch or roll stimulation of the monkey, depending on
the orientation of the inner frame (angle b, pitch: b Å 07, roll:
b Å {907 ) (Fig. 1). Thus pitch stimulation occurred around the
Y-axis and roll stimulation around the X-axis in the monkey’s head
coordinates. With orientations of the primate chair of b Å {457,
stimulation was close to the LARP or RALP VCP orientation,
respectively. As a routine, orientations were investigated at Db Å
157 intervals, and the stimulus amplitude was g Å {157 at 0.6 Hz
(maximum velocity {607 /s). This yielded 12 orientations (13
including b Å /907 and b Å 0907, Fig. 1A).
2) Earth-vertical axis rotation in different roll positions ( b Å
{907 ). Similarly, sinusoidal rotations around the earth-vertical axis
were applied with an amplitude d Å {157 at 0.6 Hz while the
monkey remained in different roll positions by adjusting the medium frame to different fixed roll angles ranging from g Å 0207
to g Å 207 ( Dg Å 107 ) (Fig. 1B).
3) Earth-vertical axis rotation in different pitch positions ( b Å
07 ). Sinusoidal rotations around the earth-vertical axis were applied
with an amplitude d Å {157 at 0.6 Hz while the monkey remained
in different pitch positions by adjusting the medium frame to different fixed pitch angles ranging from g Å 0207 to g Å 207 ( Dg Å
107 ) (Fig. 1C).
Amplitudes of sinusoidal stimulation could be varied between 0
and {207. Static tilts up to g Å {207 were applied in different
orientations of the inner frame (angle b ).
Data analysis
All signals (3-dimensional head and eye position, neuronal activity) were monitored and stored on an FM tape recorder (Teac XR
310) for further off-line computer analysis. Signals were digitized
with real time occurrence of neuronal activity (spikes) and a sampling rate of 200 Hz for the other channels. For a given sinusoidal
stimulus condition, neuronal activity was averaged for 7–12 cycles.
Averaged neuronal activity was fitted by a least-square best-sine
function. In cases in which the neuronal activity was silenced during sinusoidal stimulation (‘‘cutoff ’’), a weighting factor W (W Å
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1 for the episode with neuronal activity and W Å 0 for the cutoff)
was applied. Thus, assuming that the modulation of the neuronal
activity had the same frequency as the sinusoidal vestibular
stimulation, the least-square best-sine function was defined
by the neuronal activity above threshold. Sensitivity
(imprs 01 /(degrs 01 ), i.e., the amplitude of the resulting leastsquare best-sine function divided by the velocity of the vestibular
stimulation) and phase were determined in relation to head velocity, with positive phase values indicating that neuronal activity was
leading head velocity. Neurons were grouped in one of four major
orientation groups [pitch ( b Å 07 ), roll ( b Å {907 ), RALP, and
LARP ( b Å {457 )] that lay closest ( Db Å {22.57 ) to their direction of maximum modulation. Because maximal responses can be
related to each of the two stimulus directions (up or down), eight
response types were distinguished. Response always refers to excitation in a given stimulus direction. During static tilt stimulation,
neuronal activity was sampled over 40–60 s and a neuron was
considered as modulated if the firing frequencies in two positions
were statistically different (t-test, P õ 0.001).
At the end of all experiments, the animal was placed under
deep barbiturate anesthesia and perfused transcardially with 10%
Formalin. Coronal sections, taken every 50 mm in the stereotaxic
plane, were stained with cresyl violet. Electrode tracks were reconstructed with the aid of small electrolytic lesions that had been
placed by passing 30- to 100-mA current for 10–20 s after particularly fruitful recording sessions.
RESULTS
General characteristics
The results are based on the quantitative analysis of 158
neurons responding to dynamic VC stimulation, and according to histological reconstructions located in FN. From
these 158 neurons, 120 were also tested during yaw stimulation and 61 during static tilt. For 53 neurons, all three conditions (dynamic vertical and horizontal stimulation as well
as static tilt) were applied.
Neurons responding to dynamic vertical stimulation composed Ç15–20% of the neurons tested. Some of these nonresponsive neurons localized in the caudal FN were clearly
modulated with saccades (Büttner et al. 1991; Fuchs et al.
1993) and will not be considered here. Neurons with both
vestibular and smooth pursuit sensitivities will also not be
considered. All vestibular-only neurons (n Å 158) were
spontaneously active (range 21–104 imp/s; average 58.5
imp/s) with an irregular discharge rate. Coefficient of variation of the interspike interval for all neurons ranged between
0.2 and 1.4, with an average of 0.73 (see Fig. 7), which is
considerably higher than the values found for vestibular
nerve afferents. No attempt was made to relate occasional
bursts or silent periods in some of the neurons to a certain
behavioral pattern. None of the vestibular-only neurons had
activity related to saccades or eye position. Vestibular responses were the same in light and darkness. Responses were
also not affected by the level of alertness as judged by the eye
movement recordings. The disappearance of the vestibular
modulation for several cycles (waxing and waning), which
has been described for vestibular responses of PCs in the
oculomotor vermis (Suzuki and Keller 1988a,b), was seen
in three (2%) neurons. Because it was not a common phenomenon it will not be considered further.
During sinusoidal vestibular stimulation many neurons
were silenced in one direction (cutoff) as shown in Fig. 2.
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FIG . 2. Activity of a ‘‘vestibular-only’’ neuron in the right fastigial nucleus (FN) during sinusoidal vertical stimulation
(0.6 Hz, {607 /s) around a horizontal earth-fixed axis with the head oriented in the directions yielding maximal ( b Å 0307 )
and minimal ( b Å 607 ) response modulation. Shown are individual impulses, instantaneous frequency, and stimulus velocity.
Orientations for minimal (null) and maximal responses are 907 apart. During maximal responses neuronal activity is in phase
with stimulus velocity and decreases to 0 during part of the cycle (‘‘cutoff ’’). Because this neuron had its best modulation
during upward head movements with the head oriented at 0307 (ipsilateral to the recording side), it was classified as an
ipsilateral posterior canal (iPC) neuron.
With our stimuli this was found in 51% of the neurons, which
is in agreement with earlier studies showing that cutoff is
a common phenomenon (Büttner et al. 1991; Gardner and
Fuchs 1975). All neurons showing an activity increase during stimulation in one direction showed a decrease in the
opposite direction (types I and II). None of the neurons
showed an activity increase (type III) or decrease (type IV)
in both directions.
Of 158 neurons, 47 were only tested in fewer than four
different orientations during dynamic vertical stimulation.
These data were considered insufficient to permit conclusions about the response vector orientation, and particularly
about complex response patterns (see below). They were
therefore excluded from further analysis and not included in
Tables 1 and 2. However, the data supported the general
finding that the activity of most neurons (32 of 47) was in
phase ( {457 ) with head velocity and that for only 15 of 47
neurons was the activity in phase ( {457 ) with head position.
Of 28 neurons tested, 12 exhibited an additional response
to HC (yaw) stimulation. The responses of seven of these
neurons were type I and the remaining five were type II
responses (Duensing and Schaefer 1958).
The remaining 111 neurons were attributed to one of the
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following groups according to their dynamic response during
VC stimulation and their phase relation: VCP and VC convergence neurons (n Å 79), otolith-related neurons (n Å
25), and complex neurons (n Å 7).
Because we determined response vector orientations at
one frequency, we cannot exclude the possibility that some
of the neurons classified as VC related reflect an irregular
otolith input. In contrast to regular otolith neurons, for which
the phase stays close to head position, the phase for irregular
neurons can vary considerably ( ú1807 ) for frequencies
ú0.01 Hz (Schor et al. 1985). We assumed a VC response
when the phase was within {457 of head velocity and neurons did not respond to static tilt.
VC and VC convergence neurons
Seventy-nine neurons were attributed to this group. Of these, 59 were tested at all 12
orientations (13, including roll b Å /907 and 0907 ) during
vertical dynamic stimulation. The remaining 20 neurons
were investigated at 4–11 orientations, which covered a
range of ¢1207 for each neuron. Of the 79 neurons, 53 were
classified as VCP-related neurons with an optimal response
GENERAL CHARACTERISTICS.
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TABLE
C. SIEBOLD, L. GLONTI, S. GLASAUER, AND U. BÜTTNER
1.
Sensitivity and phase relation of vertical canal-related neurons
Sensitivity, (imprs01 )/(degrs01 )
iR
cR
uP
dP
iAC
cAC
iPC
cPC
Ipsi
Contra
Total
Phase (Relative to Head Velocity)
N
Average
Range
Average
Range
10
6
3
7
21
3
21
8
52
17
79
0.82
0.5
0.66
0.89
0.63
0.54
1.25
0.71
0.88
0.6
0.8
0.22–1.60
0.34–0.80
0.36–0.88
0.35–1.60
0.33–1.25
0.43–0.70
0.42–2.52
0.36–0.94
0.22–2.52
0.34–0.94
0.22–2.52
3.5
04.6
14.75
4.5
3.1
011.5
4.4
06.5
3.6
06.5
2.07
/25 to 018
/29 to 021
/22 to /7.5
/20 to 05
/22 to 020
05 to 018
/20 to 026
/0.6 to 019
/29 to 026
/29 to 021
/29 to 026
0.59
0.39
0.49
0.23–1.24
0.30–0.61
0.23–1.24
6.1
26.8
16.4
/44 to 045
/50 to /1
/50 to 045
Horizontal canal stimulation
Type 1
Type 2
Total
10
9
19
Ipsi and Contra: combined values for neurons with a response vector orientation ipsilateral [ipsilateral roll (iR), ipsilateral anterior canal (iAc),
ipsilateral posterior canal (iPC)], and contralateral [contralateral roll (cR), contralateral anterior canal (cAC), contralateral posterior canal (cPC)] to
the recording side. The values for some of the vertical canal-related neurons also responding to horizontal canal stimulation are shown at bottom. uP,
pitch up; dP, pitch down.
during ipsilateral anterior canal (iAC), ipsilateral posterior
canal (iPC), contralateral anterior canal (cAC), or contralateral posterior canal (cPC) stimulation (Table 1). The other
26 neurons reflected convergence of two VCs with optimal
responses during either roll or pitch movements. Of the 79
neurons investigated during dynamic vertical stimulation, 69
were also tested during HC stimulation around the earthvertical axis.
All neurons had a maximal response for one orientation
during vertical dynamic stimulation and a minimal (null)
response with spontaneous activity only at an orientation 907
apart (Figs. 2 and 3). Between maximum and minimum the
responses decreased monotonically and were closely fit by
a sine function (Fig. 3).
Phases of the neuronal response were for all orientations
on average close to stimulus (head) velocity, except for a
phase shift of 1807 around the minimal (null) response.
TABLE
2.
Phases ranged for different neurons between /297 (lead)
and 0267 (lag). Phases for neurons with different optimal
orientations were similar (Table 1).
None of the neurons tested in this group (n Å
41) responded to static tilt in the roll, pitch, or optimal
angle b orientation. This supports the assumption that these
neurons receive only a canal and not an otolith-related input.
STATIC TILT.
In each FN on both sides
all eight response types [iAC, cAC, iPC, cPC, ipsilateral
roll (iR), contralateral roll (cR), pitch down (dP), and pitch
up (uP)] were found (Table 1). Thus neurons had their
optimal response in the canal planes (Fig. 3A), but also
during iR, cR, uP, and dP movements (Fig. 3B). In the
optimal orientation the sensitivity at 0.6 Hz varied for different neurons between 0.22 and 2.52 (imprs 01 )/(degrs 01 ).
There was no statistically significant difference between the
RESPONSE VECTOR ORIENTATION.
Sensitivity and phase relation of otolith-related neurons
Sensitivity, (imprs 01 )/(degrs01 )
iR
cR
i45 ND
c45 ND
i457 NU
c457 NU
Total
Phase (Relative to Head Velocity)
N
Average
Range
Average
5
5
7
4
1
4
25
0.62
0.52
0.69
0.81
0.7
0.57
0.62
0.51–0.85
0.27–0.72
0.34–0.97
0.7–0.96
0.7
0.30–0.93
0.27–0.97
076.2
093.5
077
0100.6
081
083.2
084.9
0.67
0.63
0.66
0.54–0.78
0.63
0.54–0.78
29.8
42
31.5
Range
060
062
069
063
081
074
060
to
to
to
to
0133
0111
0128
0110
to 0106
to 0133
Horizontal canal stimulation
Type 1
Type 2
Total
10
1
11
/54 to 026
42
/54 to 026
Values were measured during dynamic vertical stimulation (top) and during dynamic horizontal stimulation (bottom) ipsilateral (i), contralateral (c),
nose down (ND), nose up (NU). For abbreviations, see Table 1.
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FIG . 3. Sensitivity (top) and phase (bottom) of an iPC neuron (A) and a pitch down (dP) neuron ( B) during different
head orientations at sinusoidal vertical stimulation (0.6 Hz, {607 /s). Sensitivity decreases monotonically from a maximal
to a minimal value at an orientation 907 apart. Dashed line: fit by a sine function (note that negative values of the sine
function were multiplied by 01). The calculated maxima are b Å 0467 for A and b Å 037 for B. Neuronal activity increases
during up (A) and down (B) head movements. Phase is close to head velocity, with a slight phase lag in A, except for a
phase shift of 1807 around the null response (457 in A and {907 in B).
sensitivity for different response types except for iPC neurons, which yielded the most sensitive neurons. There was
no difference of sensitivities between roll-, pitch-, and canalrelated neurons. However, neurons with ipsilateral orientations (iAC, iPC, iR) were on average (sensitivity 0.88
(imprs 01 )/(degrs01 ) more sensitive than contralateral orientations (cAC, cPC, cR) (average sensitivity 0.6
(imprs 01 )/(degrs01 ) (Fig. 4A). These differences were
statistically significant (P õ 0.001, t-test for independent
samples). This was also reflected in individual neurons. The
largest sensitivity for a neuron with a contralateral optimal
orientation was 0.94. However, there were 18 neurons with
sensitivities between 0.9 and 2.52 (imprs 01 )/(degrs01 ) and
ipsilateral orientations. Furthermore, 52 neurons (75%) had
an ipsilateral canal (iAC, iPC, iR)-related orientation compared with 17 (25%) neurons related to contralateral orientation (cAC, cPC, cR) (Fig. 4A).
There was a definite number of pitch neurons (n Å 10),
which increased their activity with nose-down (dP neurons)
or nose-up (uP neurons) movements (Fig. 3B). Accordingly
they had null responses during roll movements.
HC STIMULATION. The majority of neurons tested did not
respond during yaw stimulation ( g Å 07 ) (45 of 69,
65%) on the basis of a sensitivity criterion of ú0.2
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(imprs 01 )/(degrs01 ). However, 24 neurons were modulated, 14 neurons with a type I and 10 neurons with a type
II response. Of the 24 yaw-modulated neurons, 5 were roll
neurons, 1 was a pitch neuron, and the remaining 18 were
VCP-related neurons. As shown by the following numbers,
there was no specific preference for any combination between horizontal and vertical response types: type II / iAC
(n Å 4), type II / cAC (n Å 1), type II / iPC (n Å 3),
type II / cR (n Å 2); type I / iAC (n Å 3), type I / iPC
(n Å 6), type I / cPC (n Å 1), type I / iR (n Å 2), type
I / cR (n Å 1), type I / dP (n Å 1).
Yaw stimulation was routinely applied with the monkey’s
head in the erect position, which is Ç157 off the optimal orientation for the HCs (Fig. 1C) and leads to a VC stimulation
(Böhmer et al. 1985). The effect of the angle between the VC
orientation and the stimulus plane (defined by g ) during yaw
stimulation applies for VCP-related and roll neurons, but not
for pitch neurons. It follows simple trigonometric rules (see
APPENDIX ). The maximal (100%) VCP response is therefore
reduced to Ç20% at g Å 07 ( b Å 07 ) and to 0% at g Å /157.
For roll neurons this value would be 27% at g Å 07. This
implies a sensitivity of ¢1.0 (imprs 01 )/(degrs01 ) for VCPrelated neurons and 0.8 (imprs 01 )/(degrs01 ) for roll-related
neurons during earth-horizontal axis rotation to result in a mod-
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FIG . 4. Response vector orientations for (A) 79 vertical canal-related neurons and (B) 25 otolith-related neurons in FN.
Length of vector indicates sensitivity (imprs 01 )/(degrs01 ). A: although neurons with orientations in all directions are
present, there is a clear preference, both in terms of numbers and sensitivities, for neurons with iAC and iPC orientations.
B: otolith-related neurons are less common than vertical canal-related neurons. In comparison, there is also a lack of highsensitivity neurons and a noticeable absence of pitch neurons. ND, nose down; NU, nose up.
ulation of ú0.2 (imprs 01 )/(degrs01 ) (sensitivity criterion)
during yaw stimulation ( g Å 07 ). It also has to be considered
that an interaction of a VC and an HC input could be additive
or subtractive for yaw stimulation in the erect position. A cAC,
cPC, and type I response would add and the opposing combination (iAC, iPC, and type I) would subtract (see APPENDIX ).
High sensitivity values [e.g., ú1.0 (imprs 01 )/(degrs01 )
(VCP) and ú0.8 (imprs 01 )/(degrs01 ) (roll)] were found for
seven of the VCP neurons and one of the five roll neurons
tested during yaw stimulation. The remaining 16 (of 24) neurons tested had values below this calculated threshold. From
this it can be concluded that the yaw response for these 16
neurons in the erect position is at least partly determined by
an HC input. In agreement with this, the modulation of these
HC-related neurons should increase during nose-down ( g Å
/207 ) earth-vertical axis stimulation. An example of this is
shown in Fig. 5.
For the seven VCP-related neurons with sensitivities ú1.0
and responses during yaw stimulation at g Å 07 [iAC /
type II; iPC / type I (n Å 5); iPC / type II], the relative
contribution of the VCs and HCs was calculated (see APPENDI X ). For five neurons [iPC / type II; iPC / type I (n Å
4)] the modulation was indeed mainly determined by the
VC input, but for the remaining two neurons the yaw response was due predominantly to the HC stimulation. For
the five neurons that only received a VC input, the sensitivity
should decrease during g Å /157 earth-vertical axis stimulation, which was indeed seen in one neuron tested.
We also tested whether high-sensitivity VCP neurons
showed a predicted yaw response. This applied to 3 of 10
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neurons. Theoretically this could result from subtractive interaction of VC and HC inputs as seen in some of the examples described above.
Similarly we determined for the high-sensitivity roll neuron the relative contribution of the roll response to the yaw
response. Also for this neuron the yaw response was predominantly determined by the HC input with the VC inputs
interacting in a subtractive fashion. Other high-sensitivity
roll neurons [ ú0.8 (imprs 01 )/(degrs01 ); n Å 2] were not
tested during yaw stimulation.
In summary, we conclude that 19 (of 24) neurons responding to yaw stimulation in the erect position had an
additional HC input, but that for the remaining 5 neurons
the yaw response reflected a VC input. Of these 19 HCrelated neurons, 13 showed convergence between the HC
and one VCP pair. Of the remaining neurons, five were roll
neurons and one was a pitch neuron.
During yaw stimulation, HC-related neurons had
on average a phase advance relative to head velocity of
/167 and a sensitivity ranging from 0.23 to 1.24
( imprs 01 ) / ( degrs01 ) ( Table 1 ) .
Finally, it was also possible that an HC-mediated response
leads to modulation during roll stimulation. This was seen
in one roll neuron with a yaw sensitivity ú0.8 (imprs 01 )/
(degrs01 ), actually the same neuron in which the VC (roll)
sensitivity also interacted with the yaw response under our
stimulus conditions. In this example, the numerical analysis
(see APPENDI X ) showed an unexpectedly high contribution
of the HC [contributions to sensitivity (imprs 01 )/
(degrs01 ): ipsilateral HC (iHC), 1.7; iPC, 0.8; iAC, 0.5].
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FIG . 5. Averaged responses of a canal-related neuron in the right FN that receives convergent input from a vertical canal
(A and B; iAC) and a horizontal canal (C and D; type I). Left: stimulus velocity for vertical canal stimulation. Right:
stimulus velocity for horizontal stimulation. Two stimulus cycles are repeated for clarity. During vertical stimulation the
neuron has its maximal response (A) at b Å 477 and null response (B) close to b Å 0457. During yaw stimulation the
response is larger in D ( g Å /207 ) than in C ( g Å 07 ), i.e., when the horizontal canal is close to optimal stimulation.
During vertical (A) and horizontal (D) stimulation, neuronal activity leads stimulus velocity.
From this it can be concluded that the roll response was
determined by an additive 33% HC input to the VC input.
In contrast, the yaw response due to the HC input was reduced by 16% by the VC input, which proves that stimulation around the earth-horizontal axis alone is not sufficient
to discriminate between VC-VC convergence (roll neurons)
or neurons receiving their main input from the HC. All roll
neurons investigated received a VC input.
Otolith-related neurons
On the basis of their phase relation ( {457 around head position), 25 neurons were classified as receiving mainly an otolith input. In many aspects
these neurons responded similarly to canal-related neurons.
During vertical dynamic stimulation they also exhibited for
different head orientations ( Db ) a response maximum and
a minimum (null response) 907 apart (Fig. 6). Sensitivity
decreased monotonically between maximum and minimum
GENERAL CHARACTERISTICS.
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and could be fitted best by a sine function. As for the VCrelated neurons, the phase was constant for different orientations except for a phase shift of 1807 around the null response. The major difference from VC-related neurons and
also the reason to classify these neurons as otolith related
was that the phase of the neuronal response was close to
head position. For the 25 neurons the average phase at 0.6
Hz and the optimal orientation was 0857 (range 0607 to
01337 ), i.e., leading head position by 57. There was no
systematic difference of phase relation for neurons with different orientations (Table 2).
Although fewer otoliththan canal-related neurons were recorded, most orientations
except pitch neurons were encountered (Table 2, Fig. 4B).
Otherwise there was no obvious preference for response vector
orientations. The response amplitudes were similar for different
orientations (Table 2, Fig. 4B). Also the average sensitivity
[0.62 (imprs 01 )/(degrs01 )] during dynamic stimulation was
RESPONSE VECTOR ORIENTATION.
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C. SIEBOLD, L. GLONTI, S. GLASAUER, AND U. BÜTTNER
FIG . 6. Otolith-related neuron recorded in the left FN during dynamic vertical (0.6 Hz, A–C) and static roll (D) and
pitch (E) stimulation. During dynamic stimulation, neuronal activity (A and B) is in phase with head position (vertical
dashed lines). Orientation is close to maximal in A and close to the null response in C. Static response increases during
LED and ND. The calculated response vector orientation was b Å 0557 for the dynamic condition and b Å 0487 for the
static condition.
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FIG . 7. Otolith-related neuron recorded in the left FN during static roll (A) and pitch (B) stimulation. Static response
increases from RED to LED and from ND to NU. Despite the irregularity of the neuronal responses, there are clear differences
of average responses between different static positions.
comparable with that of the canal-related neurons [0.8
(imprs 01 )/(degrs01 )]. However, in comparison there was a
clear lack of high-sensitivity neurons (Fig. 4).
STATIC TILT. Of 25 neurons, 10 were additionally tested
during static tilt. Seven of these neurons were also modulated
during static tilt (Figs. 6, D and E, and 7) and three were
not. For the modulated neurons the static and dynamic response vector orientation was similar, with differences
not exceeding 157. The position-related sensitivity
(imprs 01 /deg) was for all neurons higher during dynamic
[average 0.6 (imprs 01 )/(degrs01 ), corresponding to 2.33
imprs 01 /deg, range 1.08–3.08 imprs 01 /deg] than during
static (average 1.03 imprs 01 /deg, range 0.47–1.92
imprs 01/degrs 01 stimulation. Three neurons with dynamic
sensitivities ranging from 1.44 to 3.84 imprs 01 /deg were
not modulated at all during static stimulation ( {207 ) in the
roll and pitch planes.
HC STIMULATION. Of 18 neurons investigated, 11 had in
addition to the otolith-related response a modulation during
yaw stimulation, which was for 10 neurons a type I response
and for 1 a type II response. The remaining seven neurons
were not modulated during yaw stimulation. Sensitivity
during yaw stimulation ranged between 0.54 and 0.78
(imprs 01 )/(degrs01 ) and the phase advance relative to head
velocity averaged /31.57. These values were similar to those
values of the VC-related neurons (Table 1).
/ 9k0e$$mr20 J523-6
The same considerations as for the VC-related neurons
with regard to erect head position during yaw stimulation
were also made for the otolith-related neurons. The percentage of yaw-responding otolith-related neurons (61%) was
actually higher than that of VC-related neurons (35%). As
for the VC-related neurons, there was also no preference for
any combination of the yaw response (in nearly all instances
type I) and the response vector orientation. None of the
otolith neurons tested for yaw response had a sensitivity
ú1.0 (imprs 01 )/(degrs01 ) (or 0.8 for the roll-related neurons). Thus on the basis of the arguments given above for the
VC-related neuron the yaw response for all otolith-related
neurons could at least be partially related to an HC input.
There was also no high-sensitivity otolith-related neuron
among those neurons that did not respond during yaw stimulation.
Complex neurons
GENERAL CHARACTERISTICS. Seven neurons were classified
as complex neurons. Of these, six did not follow the pattern
described above for canal- and otolith-related neurons, i.e.,
their response vectors at different orientations could not be
fitted by a sine function with a 1807 phase shift around the
null response. For four neurons there was no null response
and the phase varied continuously with different orientations,
although phase changes were steeper around the minimal
response (Baker et al. 1984a). One neuron had a constant
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C. SIEBOLD, L. GLONTI, S. GLASAUER, AND U. BÜTTNER
sensitivity and phase relationship at all orientations except
a null response around b Å 0607 with a 1807 phase shift,
and for another neuron a null response was present over a
range of Db Å 457. Finally, one neuron with a head velocityrelated sensitivity as seen for the canal-related neurons and
a response to static tilt was included in this group, although
such response combinations could reflect an otolith input
(Schor et al. 1985).
STATIC TILT AND HC STIMULATION. Of six complex neurons
tested, five responded to static tilt. This reflects an otolithrelated input and is in good agreement with present concepts
about ‘‘complex’’ vestibular responses. These require convergence from neurons with different orientations (response
vectors) and frequency responses. For the latter at least one
otolith-related input is required (Baker et al. 1984b). One
type I response was encountered in five complex neurons
tested during yaw stimulation.
Anatomic location
According to the reconstructions there was no systematic
distribution of neurons with different response vector orientations. This was true for the rostral-caudal, mediolateral,
and ventral-dorsal extent of FN. Vestibular-only neurons
responding to vertical dynamic stimulation appeared to be
located over the whole FN, being less frequent in the caudal
third. On single electrode tracks the most dorsal and most
ventral vestibular neuron could be separated by 2.4 mm.
This covers most of the ventrodorsal diameter of FN, which
is up to 2.5 mm in the monkey. There was some tendency
for iAC neurons to be more rostral than iPC neurons, but
certainly neurons with either orientation could be recorded
on one electrode penetration. The lack of a systematic distribution of response vector orientations is also supported by
the analysis of single electrode tracks. It showed that 94% of
tracks with more than one vestibular-only neuron contained
neurons with more than one orientation. On individual
tracks, up to four different orientations, including ipsi- and
contralateral orientations, could be encountered (Fig. 8).
However, there was also some indication of clustering for
certain orientations revealed by the analysis of the remaining
6% of the tracks. On these tracks all vestibular neurons had
the same orientation for up to nine neurons on one track. In
24% of the tracks, three to four neighboring neurons had
the same or adjacent response vector orientations.
The otolith-related neurons were found intermingled with
VC-related neurons. Also, the otolith-related neurons did
not show a specific spatial distribution of response vector
orientations.
DISCUSSION
Studies of the vestibular nerve provide detailed knowledge
as to which information from the canal and otolith organs
reaches central nervous structures (Goldberg and Fernandez
1984).
It has been shown in several studies that 1) the activity
of many vestibular nuclei neurons can be related to individual canal pairs, 2) the responses for a large number of neurons indicate canal-canal or canal-otolith convergence with
the same spatial orientation, and 3) only a minority of neu-
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rons shows a complex response pattern reflecting convergence of neurons (with ¢1 otolith input) with different spatial and temporal properties (Baker et al. 1984a,b; Endo et
al. 1995; Iwamoto et al. 1996; Kasper et al. 1988). This is
also the pattern found in FN during dynamic vertical stimulation.
Because we investigated neurons only at one frequency
(0.6 Hz), it is conceivable that some of our neurons classified as canal neurons are actually reflecting an input from
dynamic otolith afferents. Such neurons have been encountered in the vestibular nuclei after plugging of all six semicircular canals (Schor et al. 1985). Dynamic otolith neurons
do not encode head position at most frequencies and can
alter their phase relation by up to 1807 at different frequencies (Schor et al. 1985). Thus they could potentially encode
head velocity at just 0.6 Hz (the frequency in this study).
However, we feel that this is unlikely for the vast majority of
neurons. Preliminary (unpublished) results in this laboratory
also indicate that the VC-related FN neurons remain in phase
with head velocity at different frequencies, with little change
in sensitivity (related to head velocity), similarly to what
has been described for HC-related neurons in FN (Büttner
et al. 1991).
Nearly 30% of the neurons responding to vertical dynamic
stimulation reflect an otolith input, on the basis of a phase
relationship close to head position during dynamic stimulation and responses to static tilt. This has not been reported
before in the monkey. In a previous study (Gardner and
Fuchs 1975) mainly aimed at horizontal vestibular responses, only a small number of neurons was tested during
vertical stimulation, which easily explains how these otolithrelated neurons might have been missed. Our findings are
in agreement with an earlier study in the decerebrate cat
(Ghelarducci 1973), in which neurons responding to static
tilt had been encountered.
Noticeable pitch orientations for otolith-related neurons,
either up or down, were missing. This lack of pitch orientations has also been reported for vestibular nuclei neurons
(Schor et al. 1984). The response vector orientations during
dynamic and static stimulation were always similar and supported the assumption that the responses reflected an otolithrelated input. The dynamic sensitivity was always higher
than the static sensitivity, as in the vestibular nuclei (Schor
et al. 1985) and vestibular nerve afferents (Fernandez and
Goldberg 1976). A few otolith-related neurons did not respond during static stimulation but responded only during
dynamic stimulation. Considering that in vestibular nerve
afferents the sensitivity during static and dynamic stimulation can differ by a factor of 10 (Fernandez and Goldberg
1976), it is conceivable that the small angles of static tilt
used in this study and the irregular discharge rate of FN
neurons prevented the detection of a possible static response.
The static responses of our otolith-related neurons, with a
monotonic increase or decrease of activity during different
static head positions, reflected basically an utriculus input
(Goldberg and Fernandez 1984). However, our limited number
of neurons certainly does not exclude the presence of neurons
with sacculus-related responses with a decrease or increase of
activity in both directions deviating from the erect head position. It also has to be considered that the range of angles
investigated ( {207 ) was small, and that the high coefficient of
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1443
FIG . 8. Semischematic drawing of a transverse section through FN combined with a reconstruction of 2 electrode tracks
with vestibularly related neurons. The track on the right yielded vestibular-related neurons (n Å 8) that all had the same
response vector orientation (cR, contralateral roll). For the track on the left, among 11 vestibular-related neurons 4 major
orientations (dP, cR, iAC, iPC) were encountered. Tracks with multiple orientations were more common than those with
only 1 orientation. IN, interpositus nucleus; IV, fourth ventricle.
variation of the interspike interval of FN neurons makes it
difficult to establish smaller activity changes.
A high percentage of otolith-related neurons also responded to yaw stimulation. This reflects an otolith-HC interaction, a feature also commonly found in vestibular nuclei
neurons (Bush et al. 1993).
Surprisingly, there was only a small number of complex
neurons reflecting spatiotemporal convergence. This is surprising for a number of reasons. First, complex responses are assumed to reflect an otolith-VC (or otolith-otolith) interaction
in which the various inputs differ in their dynamic response
properties and their response vector orientations (Baker et al.
1984a). Considering that many of our otolith-related neurons
also reflect an HC input, one also might expect considerable
otolith-VC interaction. It is possible that neurons have to be
tested over a wider frequency range to obtain more indication
of complex responses. Second, responses in FN might be expected to differ more from the primary vestibular input than
the vestibular nuclei because of the more numerous stages of
processing: this is certainly not supported by the present data.
Third, it has been suggested that complex responses are less
frequent in the decerebrate state (Baker et al. 1985): this is
supported neither by our data nor by recent data from the
cat in which the same paradigms were used in the alert and
decerebrate preparation (Iwamoto et al. 1996).
Comparison with vestibular nuclei neurons
For reasons given above, a comparison with vestibular
nuclei neurons should be restricted to vestibular-only nonoculomotor neurons. Most of related studies have been performed in the vestibular nuclei of the cat (Baker et al.
/ 9k0e$$mr20 J523-6
1984a,b; Endo et al. 1995; Iwamoto et al. 1996; Kasper et
al. 1988). The results show that a high percentage of neurons
receives either a VC-related or an otolith-related input. Complex neurons are rare, and most neurons respond to excitation
from one ipsilateral canal. HC-VC convergence is more
common than ipsilateral VC-VC convergence (roll neurons). Contralateral inputs are rare. Canal-related pitch neurons, indicating convergence from ipsilateral and contralateral VCs, are generally not encountered in the vestibular
nuclei. There is also evidence for convergence from all three
canal pairs on individual vestibular nuclei neurons (Baker
et al. 1984b).
A predominant input from ipsilateral vertical semicircular
canals to the vestibular nuclei is also supported by recordings
from the alert monkey (Reisine and Raphan 1992). Besides
this, there is only sparse information about canal interaction
in the vestibular nuclei of the alert monkey (Phillips et al.
1992). According to this preliminary study, type II (horizontal) vestibular nuclei neurons generally also respond during pitch stimulation, whereas type I neurons do not.
On the basis of this comparison it can be concluded that,
similar to the vestibular nuclei, neurons in FN show a clear
preference for ipsilateral canal orientations. It appears that
response vector orientations are more widely distributed in
FN. Particularly, pitch neurons, which have not been encountered in the vestibular nuclei, are present. Whether this convergence of contra- and ipsilateral canal inputs is actually
achieved at the cerebellar level has yet to be determined.
Comparison with other cerebellar structures
Vestibular responses have been mainly studied in the vestibulocerebellum (flocculus, nodulus, uvula). It should be
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C. SIEBOLD, L. GLONTI, S. GLASAUER, AND U. BÜTTNER
emphasized that the nodulus receives a major direct vestibular nerve input. A recent study (Barmack et al. 1993) demonstrated that 70% of the vestibular nerve afferents in the rabbit
project at least as collaterals to the vestibulocerebellum. The
main output from the vestibulocerebellum is to the vestibular
nuclei, thus comparable with the projection from the vermis
to FN.
P cells in the flocculus can carry a precise vestibular signal, with many neurons reflecting convergence from multiple
canals (Fukushima et al. 1993; Powell et al. 1996). Otolithrelated responses were not found. This is in contrast to the
nodulus-uvula complex, where 40% of the neurons are modulated during static stimulation (otolith input) (rabbit, Barmack and Skojaku 1995). The remaining neurons are activated during VC but not during HC stimulation. The response vector orientations for all these neurons indicate
activation of the ipsilateral VCs, mostly of the ipsilateral
posterior canal, without evidence for roll or pitch neurons.
One major input to FN derives from P cells in the vermis,
mainly from the anterior vermis for the vestibular-only neurons under discussion. So far there are no studies investigating P cells in the anterior vermis under natural vestibular
stimulation conditions. Earlier studies (Precht et al. 1977)
reported polysynaptic vestibular inputs to lobules I–V in the
cat. A vestibular input to the anterior vermis is also supported
by anatomic studies (Kotchabhakdi and Walberg 1978).
spinal mechanisms (Büttner-Ennever 1992). There is also
a direct fastigiospinal projection, terminating at the ventral
horn in the upper cervical region (Asanuma et al. 1983).
Thus efferents from FN can reach spinal motor structures
without relaying within the vestibular nuclei.
Functional considerations
A homunculus-like figure has been attributed to the deep
cerebellar nuclei (Thach et al. 1992). With regard to FN,
the head would be located in caudal FN and the lower extremities in rostral FN. Vestibular-related neurons in FN
could interface with all spinal mechanisms related to posture,
gait, and neck movements. From lesion studies it is known
that a unilateral FN lesion causes a tendency to fall to the
ipsilateral side (Kurzan et al. 1993; Thach et al. 1992). So
far nothing is known about how the vestibular neurons in
FN affect different muscle groups. It is known that many
neck muscles have response vectors toward the pitch axis
(Baker et al. 1985; Banovetz et al. 1995), an input not
directly provided by vestibular nuclei neurons. It would be
of interest to investigate further whether the pitch neurons
in FN could provide this input through its fastigiospinal
pathway (Asanuma et al. 1983). The present results on FN,
with its large variety of response vectors and response combinations, suggest that these muscle requirements could be
met very specifically by the fastigial efferents.
Afferent connections
FN receives an ipsilateral input from the vermis. Lobules
I–V project to rostral FN and lobules VI–IX project to
caudal FN (Armstrong and Schild 1978; Noda et al. 1990).
Also, the nodulus (lobule X) has been reported to project
to the ventral region of FN besides its major projection to
the vestibular nuclei (Wylie et al. 1994). Occasional collaterals to FN from primary vestibular afferents have been
reported (Sato et al. 1989). However, they are sparse enough
that a major functional role appears unlikely. Mossy fiber
projections from the brain stem are generally bilateral: they
derive from all vestibular nuclei (except the lateral vestibular
nucleus) (Noda et al. 1990), and include other head movement-related structures (perihypoglossal nuclei, dorsolateral
and dorsomedial pontine nuclei, and nucleus reticularis tegmenti pontis) (Gonzalo-Ruiz and Leichnetz 1990; Noda et
al. 1990).
APPENDIX
To decide whether a neuronal response could be attributed to
the linear convergence of canal afferents, a least-square fit of the
expected response to the found dynamic response patterns was
performed. In this way the three weighting factors of each canal
direction could be determined.
A requirement for this analysis is that the phase of the neuronal
response be close to angular velocity over the whole stimulus
range, so that the neuron can be classified as being a ‘‘canal only’’
neuron.
To simplify the analysis, the semicircular canals were assumed
to be perpendicular to each other, with the VCs rotated by a Å
457 with respect to the sagittal plane and the canals tilted backward
by w Å 0157.
Thus the transformation from head to canal coordinates can be
described by the following matrix THC
THC Å
Efferent connections
Most efferent pathways from FN cross within the cerebellum, traverse within the contralateral FN, and leave the cerebellum via the uncinate fasciculus. Crossed fibers terminate
in nucleus reticularis tegmenti pontis, dorsomedial and dorsolateral pontine nuclei, and perihypoglossal nuclei (Asanuma et al. 1983; Batton et al. 1977; Noda et al. 1990). The
projections from the caudal part of FN (fastigial oculomotor
region) are bilateral and mainly to lateral vestibular nucleus
and inferior vestibular nucleus. More rostral areas of FN
also project to the contralateral medial vestibular nucleus
and superior vestibular nucleus (Noda et al. 1990). In general, FN projects mainly to those parts of the vestibular
nuclei that are known to be largely involved with vestibulo-
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F
cos arcos w sin a
0sin arcos w cos a
sin w
0
0cos arsin w
sin arsin w
cos w
G
(1)
With the rotation angles of the stimulation device defined in METHODS, the transformation matrix from stimulus to head coordinates
TSH can be written as
TSH Å
F
cos brcos g sin b 0cos brsin g
0sin brcos g cos b sin brsin g
sin g
0
cos g
G
(2)
Thus any stimulus vector s, defined as the direction of an angular
velocity vector applied at the position ( b,g ), can be expressed in
canal coordinates by the equation
r Å THCr TSHr s
(3)
With the definitions above, the canal coordinate vector r refers to
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positive excitatory responses of the cAC, iAC, and iHC to a neuron
in the left hemisphere.
For the three paradigms used, Eq. 3 has to be written with the
following parameters.
1) Earth-horizontal axis rotation in different yaw orientations
(EHY)
g Å 0;
b varying;
sEHY Å [0
1
b Å 90;
sEVR Å [0
0
1] T
3) Earth-vertical axis rotation in different pitch orientations
(EVP)
g varying;
b Å 0;
sEVP Å [0
0
1] T
By defining a gain vector p Å [ ccA ciA ciH ] T with ci being
the contributions of the cAC, iAC, and iHC expressed in
( imprs 01 ) / ( degrs01 ) , the answer for a linear canal convergence neuron in response to one of the paradigms above can be
expressed as
r( b,g ) Å p 7r Å p 7 (THCr TSHr s)
(4)
where 7 denotes the scalar product. The maximal response of the
neuron is then calculated by rmax Å É pÉ.
It can be shown that r( b,g ) is a sinusoidal function of the form
arsin b / brcos b or arsin g / brcos g for all three paradigms.
To evaluate the contribution p of the three canals to the neuronal
response r( b,g ) of a single neuron, the theoretical response functions can be fitted to the measured data g( b,g ) of the three paradigms (EHY, EVR, EVP) by a least-square fit
∑ [p 7rEHY ( bi ) 0 gEHY ( bi )] 2 / ∑ [p 7rEVR ( g j ) 0 gEHR ( g j )] 2
i
j
/
∑ [p 7rEVP ( gk ) 0 gEVP ( gk )] 2 Å min (5)
k
with i, j, and k being the indexes of single stimulations in the
different experimental conditions.
Equation 5 can then be solved analyticly for the contribution
vector p, which gives the gain factors for the projection of the
canal afferents onto the examined neuron.
Because positive values for ccA , ciA , and ciH indicate excitatory
contributions from the cAC, iAC, and iHC, negative values denote
excitatory contributions from the corresponding canals, i.e., iPC,
cPC, and contralateral HC. Thus a positive value for ciA denotes
contribution from the iAC, and a negative value for ciA denotes
contribution from the contralateral posterior canal.
As an example, consider a purely VC neuron receiving input
from the cAC with a sensitivity of 1.0 (imprs 01 )/(degrs01 ) in
the optimal orientation: its contribution vector p (imprs 01 )/
(degrs01 ) is then [1.0 0.0 0.0] T . Inserting p in Eq. 4 predicts
a response to earth-vertical (pure yaw) stimulation of r(0.07,
0.07 ) Å 1.0 ∗ cos a∗ sin w Å 00.18 (imprs 01 )/(degrs01 ). Here,
the negative value of the sensitivity simply denotes a phase shift
of 1807.
The signs of the contributions also show whether the neuron
receives input from only one side ([ 0, /, / ] or [ /, 0, 0 ])
or from two different sides (all other combinations), with the
distribution being a consequence of the coordinate system used.
Pure roll neurons, for example, are receiving input from only
one side with equal weights for both VCs, whereas pitch neurons
are combinations of both anterior or both posterior VCs, again
having equal weights.
We gratefully acknowledge the technical assistance of S. Langer and the
secretarial work of B. Pfreundner, M. Seiche, and I. Wendl.
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This work was Supported by the Deutsche Forschungsgemeinschaft.
Address for reprint requests: U. Büttner, Neurologische Klinik, Marchioninistraße 15, D-81377 Munich, Germany.
Received 3 July 1996; accepted in final form 18 October 1996.
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