Department of Neurology, University of Munich, D-81377 Munich, Germany
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ABSTRACT |
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Siebold, C.,
J. F. Kleine,
L. Glonti,
T. Tchelidze, and
U. Büttner.
Fastigial Nucleus Activity During Different Frequencies and
Orientations of Vertical Vestibular Stimulation in the Monkey.
J. Neurophysiol. 82: 34-41, 1999.
Neurons in the rostral part of the fastigial nucleus (FN) respond to
vestibular stimulation but are not related to eye movements. To
understand the precise role of these vestibular-only neurons in the
central processing of vestibular signals, unit activity in the FN of
alert monkeys (Macaca mulatta) was recorded. To induce vestibular stimulation, the monkey was rotated sinusoidally around an
earth-fixed horizontal axis at stimulus frequencies between 0.06 (±15°) and 1.4 Hz (±7.5°). During stimulation head orientation was changed continuously, allowing for roll, pitch, and intermediate planes of orientation. At a frequency of 0.6 Hz, 59% of the neurons had an optimal response orientation (ORO) and a null response (i.e., no
modulation) 90° apart. The phase of neuronal response was constant
except for a steep shift of 180° around the null response. This group
I response is compatible with a semicircular canal input, canal
convergence, or a single otolith input. Several other features
indicated more complex responses, including spatiotemporal convergence
(STC). 1) For 35% of the responses at 0.6 Hz, phase changes were gradual with different orientations. Fifteen percent of
these had a null response (group II), and 20% showed only a minimal
response but no null response (group III). The remaining responses
(6%), classified as group IV, were characterized by a constant
sensitivity at different orientations in most instances. 2) For the vast majority of neurons, the stimulus
frequency determined the response group, i.e., an individual neuron
could show a group I response at one frequency and a group II (III or
IV) response at another frequency. 3) ORO changed with
frequency by >45° for 44% of the neurons. 4)
Although phase changes at different frequencies were close to head
velocity (±45°) or head position (±45°) for most neurons, they
exceeded 90° for 29% of the neurons between 0.1 and 1.0 Hz. In most
cases, this was a phase advance. The change in sensitivity with change
in frequency showed a similar pattern for all neurons; the average
sensitivity increased from 1.24 imp · s1 · deg
1 at 0.1 Hz to 2.97 imp · s
1
· deg
1 at 1.0 Hz. These data demonstrate that only an
analysis based on measurements at different frequencies and
orientations reveals a number of complex features. They moreover
suggest that for the vast majority of neurons several sources of canal
and otolith information interact at this central stage of vestibular
information processing.
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INTRODUCTION |
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The fastigial nucleus (FN), the most medial deep
cerebellar nucleus, plays an important role in the processing of
vestibular information. Anatomically it receives a strong direct input
via mossy fiber collaterals from the vestibular nuclei (Noda et
al. 1990). The axons of these mossy fibers project to the
vermis, mainly to the anterior part (lobulus I-V) (Kotchabhakdi
and Walberg 1978
; Voogd et al. 1996
). In turn
the Purkinje cells (PCs) of the anterior vermis send efferents to the
FN (Armstrong and Schild 1978
). Finally, the efferents
of the FN project back to the vestibular nuclei (Noda et al.
1990
).
Functionally the FN has been divided into a rostral and a caudal part
(Büttner et al. 1991; Noda et al.
1990
). The caudal part has also been labeled fastigial
oculomotor region (FOR) (Noda et al. 1990
) because many
of its neurons are modulated during either saccadic (Fuchs et
al. 1993
; Helmchen et al. 1994
) or smooth pursuit eye movements, including the interaction of smooth pursuit and
vestibular stimuli (Büttner et al. 1991
). In
contrast, the rostral FN contains neurons that are modulated during
vestibular stimulation; they show no eye-movement- or
eye-position-related sensitivity (Büttner et al.
1991
; Gardner and Fuchs 1975
; Siebold et
al. 1997
). They therefore have been called
"vestibular-only" neurons and are believed to participate in the
control of spinal mechanisms (neck, gait, posture).
The precise functional role of these vestibular-only neurons is not
known. Previous studies have shown that vestibular-only neurons in FN
respond to vestibular stimulation in both the horizontal and vertical
planes (Gardner and Fuchs 1975; Siebold et al.
1997
). As regards vertical stimulation, neurons reach their
optimal modulation when orientated along the rotation axis (also called
response vector orientation, RVO) (Goldberg and Fernandez
1984
) not only for vertical canal planes, i.e., in the right
anterior-left posterior (RALP) or left anterior-right posterior (LARP)
plane, but also during roll and pitch stimulation, which indicates
canal convergence (Siebold et al. 1997
). Based on their
response to static tilt and their phase relation during sinusoidal
stimulation, >20% of the neurons that responded to vertical
vestibular stimulation were classified as receiving an otolith input
(Siebold et al. 1997
). However, these responses were
only determined at one frequency (0.6 Hz). The percentage of neurons
receiving an otolith input might actually be higher because
otolith-related neurons in the vestibular nuclei may have
frequency-related phase changes of >180° (Schor et al.
1984
). Thus a phase related to the stimulus velocity of the
neuronal activity does not exclude an otolith-related input.
Three different groups of neurons have been distinguished in the
vestibular nuclei of the decerebrate cat based on their phase and gain
characteristics: vertical canal, otolith, and otolith plus
canal-related neurons (Kasper et al. 1988). The
convergence of canal and otolith inputs also has been found to lead to
more complex response patterns (spatiotemporal convergence, STC), which occur when inputs have a different phase behavior and different response orientations (Angelaki et al. 1992
;
Baker et al. 1984b
).
To evaluate the possible functional role of vestibular-only neurons in
FN, particularly in comparison with vestibular nuclei neurons
(Kasper et al. 1988) and vestibular nerve afferents
(Goldberg and Fernandez 1984
), it is important to know
their response characteristics at different stimulus frequencies and
orientations. These responses were examined in the alert monkey during
vertical stimulation around an earth-fixed horizontal axis. Some
preliminary results have been published elsewhere (Büttner
et al. 1999
).
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METHODS |
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Three monkeys (Macaca mulatta, 4-5 kg) were prepared
for chronic single-unit recordings. Under general anesthesia and
aseptic conditions, a chamber for single-unit recordings was implanted (coordinates: mediolateral 0 mm, posterior 6 mm) to allow a vertical approach in the stereotaxic plane of FN on both sides. Bolts were attached to the skull to maintain a stable head position during the
experiments (for details, see Boyle et al. 1985). Before
surgery monkeys were familiarized with the experimental environment and trained to sit in a primate chair. Single-unit activity was recorded with varnished tungsten microelectrodes (impedance 2.5-4 M
) and horizontal, vertical, and torsional eye position with a dual
search-coil system (for techniques and calibration, see Bartl et
al. 1996
). During the experiment, the head was immobilized by a
head holder so that the monkey sat with its head erect (stereotaxic
horizontal) in a primate chair. In this head position, the horizontal
semicircular canals are tilted 15° upward from the optimal
orientation for yaw stimulation.
Definitions and coordinates
Directions are expressed in a head-fixed, right-handed Cartesian system 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).
Vestibular stimulation
For vertical vestibular stimulation, the monkey was
rotated sinusoidally around an earth-fixed horizontal axis at
amplitudes up to ±20°. The following stimulus protocol was applied.
First, the optimal neuronal response (optimal response orientation,
ORO) was determined at 0.6 Hz (±15°). An independent motor rotated the monkey on the turntable at a low speed (0.36-2.2°/s) to
different orientations over a range of 180° including roll ( = ±90°), pitch (
= 0°), RALP (
= +45°) and LARP (
=
45°) stimulation (Fig. 1). After this
rotation, neurons were investigated at different frequencies between
0.06 (±15°) and 1.4 Hz (±7.5°), usually including 0.1, 0.2, 0.4, 0.8, 1.0, and 1.2 Hz. At each frequency, the ORO also was determined by
continuously changing the head orientation at low speed. For some
neurons, different frequencies were investigated only at the ORO
obtained at 0.6 Hz. With this stimulus protocol, the applied velocities
ranged from 5.6 to 66°/s. The maximal acceleration was
580°/s2 and occurred at 1.4 Hz.
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Data analysis
All data (single-unit activity, eye position, vestibular
stimuli) were stored on an FM magnetic tape recorder (TEAC XR310) for
further analysis. Signals were digitized with real-time occurrence for
neuronal activity and at a sampling rate of 200 Hz for the other
channels. When head orientation remained constant, 5-15 cycles were
averaged at different stimulus frequencies. During continuously
changing head orientation, one to seven cycles (0.06-1.4 Hz)
corresponding to a 12-15° sector were averaged. This yielded 12-15
phase and sensitivity values for the 180° range of orientations that
were assigned to the centers of the respective sectors. Averaged neuronal activity was fitted by a least-square best-sine function. Silencing of neurons ("cutoff") during part of the stimulation was taken into account by introducing a weighting factor W
(W = 1 for the episode with neuronal activity and
W = 0 for the cutoff). 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
(imp · s1 · deg
1) and phase were determined in relation to
head position. A response was assumed when neuronal modulation exceeded
0.5 imp · s
1 · deg
1 (sensitivity criterion). Positive phase
values indicate that neuronal activity leads head position. The phase
behavior of an individual neuron in relation to the vertical
stimulation was attributed to head velocity or head position for phase
values ±45° around head velocity respectively position. Only neurons with phase changes exceeding 90° were attributed to a third class.
At selected recording sites small electrolytic lesions (30-100 µA of
DC anodal current for 20-30 s) or tracer substances [i.e., Di I
(Snodderly and Gur 1995), nontoxic choleratoxin subunit
B] were placed to aid the reconstruction of electrode tracks. At the
end of all experiments, the monkeys were deeply anesthetized with
barbiturate and perfused transcardially with 10% formalin. The brain
was removed and blocked in the stereotaxic plane. Coronal sections,
taken every 50 µm, were processed for the tract-tracing substances
and counterstained with cresyl violet.
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RESULTS |
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General characteristics
The data presented in this paper are based on a quantitative
analysis of 89 neurons in three monkeys. All neurons responded to
sinusoidal vertical vestibular stimulation around an earth-fixed horizontal axis and were located in the rostral FN of both sides by
means of histological reconstructions. Activity in FN was generally easy to identify. In the applied approach, the electrode passed initially through layers of Purkinje cells, which could be recognized by the presence of complex spikes. Immediately dorsal to FN, the electrode passed through white matter. No neurons were isolated here,
indicating that the electrodes used were unsuitable for fiber
recordings. The presence of activity related to saccadic and smooth
pursuit eye movements in caudal, but not in rostral FN, allowed a
functional separation of both structures. Neurons were investigated at
a minimum of two frequencies. The general characteristics of the
neurons presented here were comparable with those in our previous study
(Siebold et al. 1997). All neurons responded only to
vestibular stimulation; they were not modulated during saccadic or
smooth pursuit eye movements. Neurons responded in only one stimulus
direction. Neurons responding in both stimulus directions (type III
responses) (Duensing and Schaefer 1958
) were not
observed. The neurons were spontaneously active (average 62 imp/s,
range 18-108 imp/s) with an irregular firing rate. The coefficient of
variation of the interspike intervals was determined for 10 arbitrarily
chosen neurons. It ranged from 0.34 to 1.50 (0.65 ± 0.39;
mean ± SD). The level of alertness as judged by the eye movements
did not affect the response of the neurons. Waxing and waning (periods
of no response during vestibular stimulation), which were described for
vestibular responses in the oculomotor vermis (Suzuki and Keller
1988
), were generally not observed.
As described in our previous paper (Siebold et al.
1997), all neurons (n = 89) investigated were
modulated at 0.6 Hz (±15°) vertical vestibular stimulation around an
earth-fixed horizontal axis. For all neurons, the orientation of the
head was varied continuously over a range of 180° from roll (
=
90°) through pitch (
= 0°) to roll (
= +90°). These
changes of orientation during the vertical stimulation systematically
altered the modulation of the neuronal response (Fig. 1).
The changes of modulation were fitted by a cosine function for 84 (of
89) neurons. All these neurons had either a null response or a minimal
modulation at a given orientation and an optimal modulation (ORO) at an
orientation 90° apart. According to their response characteristics,
neurons were assigned to one of the following three response groups.
Neurons with a group I response had a null response, and their phase
was constant at all orientations except for a steep phase reversal of
180° around the null response (Fig. 2,
A-D). Thus a clear response vector orientation (RVO) could
be determined for these neurons (Baker et al. 1984a).
Fifty-nine percent of the neurons in our study belonged to group I at
0.6 Hz.
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Neurons with group II responses also had an optimal response and a null
response (not illustrated). However, their phase changes around the
null response were more gradual and extended over a range of 70°.
Often phase changes were continuous over the whole range of
orientations. Group II responses were encountered in 15% of the
neurons at 0.6 Hz.
Neurons with group III responses did not show a null response, i.e., they were modulated at all orientations. However, they had an optimal response (ORO) and a minimal response, which occurred 90° away from the ORO (Fig. 2F). The minimal response sensitivity was on the average 31% (range 13-56%) of the optimal response. Total phase changes were 180° for 180° changes in orientation. The phase changes of 50% of the group III responses were steeper around the minimal response, whereas they were continuous and lacked a steeper phase change for the other 50% (Fig. 2F). Group III responses were seen in 20% of the neurons at 0.6 Hz.
ORO is used here as a general term for optimal responses of groups
I-III. Because the term RVO is established in the literature to
signify group I responses only (Baker et al. 1984a), it
is not used here.
For the few neurons remaining (5 of 89), these rules did not apply, and they accordingly were classified as group IV. The sensitivity was constant for three neurons that lacked an ORO and a minimal response; their phase changed continuously with orientation. The response could not be further classified for the other two neurons.
ORO at different frequencies
The responses of 41 neurons were investigated at different
frequencies (0.06-1.4 Hz) and orientations. At a given frequency, orientation was altered continuously from =
90° to
= +90°. This continuous change of orientation was carried out in 235 instances. Twenty-three (of 41) neurons were examined at six to nine
frequencies, including low (
0.2 Hz) and high frequencies (
1.0 Hz).
Neurons responded at all frequencies with the exception of seven
neurons (of 30 investigated), which were not modulated at 0.06 and/or 0.1 Hz.
Group I responses were encountered at all frequencies. They amounted to
60% of the total responses (140 of 235 investigations). Group II
responses were also found at all frequencies and were observed in 22%
of all investigations (51 of 235). Group III responses were only rarely
encountered at low frequencies ( 5% of the low-frequency investigations). Thirteen percent of the responses for all frequencies and neurons were group III responses.
Five percent of the responses (13 of 235) were classified as group IV. They were encountered in 12 of 41 neurons. Thus group IV responses rarely occurred at different frequencies for a given neuron. For the vast majority of neurons, the responses could be attributed to groups I, II, or III, which were found at all frequencies. Six (of 41) neurons consistently exhibited only group I responses and 3 (of 41) only group II and/or group III responses at all frequencies. The remaining neurons exhibited a combination of responses depending on the stimulus frequency. Because a clear optimum and minimum could be determined for all responses except the small number of group IV responses, the ORO was taken as the indicator for neuronal behavior at different frequencies.
For the majority of neurons (23 of 41), frequency had little effect on ORO, i.e., the ORO varied by <45° (Table 1, Figs. 3A and 4A). The remaining neurons had larger ORO changes, often exceeding 90° (Table 1, Figs. 3B and 4B). For instance, the neuron in Fig. 4B had an ORO with RALP at 0.2 Hz and an ORO with LARP stimulation at 1.2 Hz.
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Effect of stimulus frequency on phase and sensitivity at the response orientation (ORO)
For most of the 23 neurons with stable OROs, the phase was close to head velocity (Table 1, Fig. 4A). For these neurons, phase advanced on the average from 75° at 0.1 Hz to 106° at 1 Hz. Neurons with head position-related phase changes were generally rare. Phase changes exceeding 90° were more common for neurons with ORO changes >45° (Table 1, Fig. 4B). If all neurons (n = 41) were considered, there was a weak tendency for neurons with larger ORO changes to also have larger phase changes (correlation coefficient r = 0.48, P = 0.0014). Phase changes exceeding 90° between 0.1 and 1.0 Hz meant that a head position and a head velocity-related phase could easily occur for individual neurons depending on the stimulus frequency. Group I responses also tended to be more common among neurons with stable OROs than among those with ORO changes >45° (Table 1).
The sensitivity of the ORO was remarkably uniform for the different
subgroups (Table 1). It increased, on average, for all neurons
(n = 41) from 1.24 imp · s1 · deg
1 at 0.1 Hz to 2.97 imp · s
1 · deg
1 at 1.0 Hz. There were only four neurons
with an 8- to 9-fold increase of sensitivity, which is still less than
the 10-fold increase expected for a relationship encoding velocity. A
10-fold increase in sensitivity to position (imp · s
1 · deg
1)
manifests itself as a stable sensitivity to velocity (imp · s
1/deg · s
1).
Responses at different frequencies and the ORO at 0.6 Hz
For 89 neurons the ORO was initially determined at 0.6 Hz. Then
the neurons were examined at this orientation at different frequencies
(0.06-1.4 Hz). This protocol included the 41 neurons described above.
Of the 89 neurons, 70 were tested at three or more frequencies,
including 0.2 and
1 Hz and used for further analysis. Sixty-four
neurons were tested at
5 frequencies. Neurons were divided into three
groups according to their dominant phase behavior: neurons with a head
velocity-related response over the whole frequency range, neurons with
a head position-related response, and neurons with phase changes
>90°.
Head velocity-related neurons
The largest group of neurons (32 of 70, 46%) encoded head
velocity over the whole frequency range (Figs.
5A and
6). On the average they showed a slight
phase advance with increasing frequency. Whereas neurons generally
lagged behind head velocity by 20-30° at frequencies <0.4 Hz, there
was a phase advance of 10-20° at frequencies >0.4 Hz (Fig. 6).
Sensitivity was low at 0.1 Hz (average 1.11 imp · s1 · deg
1) and
increased to 3.45 imp · s
1 · deg
1 (average) at 1.0 Hz (Fig. 6).
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Head position-related neurons
The smallest group of neurons (11 of 70, 16%) had a phase close to
head position over the whole frequency range (Fig. 6). Phase lagged
slightly on the average with increasing frequency; it exhibited a small
lead at 0.06 Hz and a lag of 20-30° at frequencies >0.1 Hz (Fig.
6). Sensitivity on average did not differ from that of the
velocity-related neurons (Fig. 6), with a value of 0.87 imp · s1 · deg
1 at 0.1 Hz and 3.75 imp · s
1 · deg
1 at 1.0 Hz.
Neurons with larger phase changes
Twenty-seven neurons (of 70, 39%) had phase changes of more than
90° between 0.1 and 1.0 Hz (Figs. 5B and 6). This was in most instances (n = 21) an increasing phase lead, which
exceeded 150° for 11 (of 21) neurons and on the average was
>120° (Fig. 6). The sensitivity increased with frequency from 1.29 imp · s1 · deg
1 at 0.1 Hz to 2.82 imp · s
1 · deg
1 at 1.0 Hz.
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DISCUSSION |
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General considerations
This analysis of orientation and frequency of a large sample of vestibular neurons in the FN of an alert animal has shown that spatiotemporal convergence (STC) is quite common among vestibular-only neurons. Despite the irregular firing rate of FN neurons, it was possible to clearly attribute the responses to one of four different groups. Although group I responses were clearly the most common type of response at all frequencies, neurons with group I responses at all frequencies accounted for only 15% of the total neurons. All other neurons exhibited a combination of group I, II, III, or IV responses, depending on the stimulus frequency, which indicates STC.
A single otolith or canal/canal input predicts that the ORO will be stable at different frequencies. Although this was found in nearly 60% of the neurons, the remaining neurons had ORO changes that increased with stimulus frequency. In many instances they exceeded 90°, again indicating STC.
When tested at a single frequency, the responses of most neurons could be attributed to a canal or otolith input. However, when investigated at various frequencies, the factors discussed above [group II-IV responses; different groups (I-IV) at different frequencies for a given neuron; and changes of ORO with stimulus frequency] show quite clearly, that there are probably only a few, if any, neurons that reflect only an otolith or a canal input.
In view of the large variation of phases and OROs with regard to stimulus frequency, it is remarkable that sensitivity was rather uniform in relation to stimulus frequency. The sensitivity of nearly all neurons increased with stimulus frequency by 2.5-fold on the average. Thus the sensitivity for neurons in phase with head velocity was similar for those in phase with head position.
The different classifications used do not necessarily reflect different classes of neurons. This was an arbitrary construct to facilitate description. In general, there was a continuum between two extremes. One extreme is represented by neurons with a stable ORO and constant phase (usually related to head velocity). These neurons were more numerous than the other extreme, neurons with large ORO and phase changes.
Comparison with vestibular nuclei neurons and neurons in cerebellar structures
In their investigation of nuclei neurons in the alert cat
Baker et al. (1984a,b
) showed that about one-third of
the neurons had response characteristics indicating STC. Thus the signs
of STC found for vestibular neurons in FN already are present in the
vestibular nuclei. This has also been shown recently for the monkey
(Yakushin et al. 1999
).
STC seems to be less common in the decerebrate cat (<10% of the
neurons examined) (Kasper et al. 1988; Wilson et
al. 1996
). Another study found similar results with little
evidence of STC in the decerebrate and the alert cat (Iwamoto et
al. 1996
). However, only one stimulus frequency (0.5 Hz) was
applied in the study. As our present results demonstrate, this is
insufficient to exclude STC.
Neurons were examined in the decerebrate cat at different frequencies
and attributed to a canal, otolith, and canal plus otolith group based
on their phase and sensitivity behavior (Kasper et al.
1988; Wilson et al. 1996
). Our data do not
permit such a distinction for vestibular-only neurons in the FN.
Neurons with a phase related to head velocity (presumably receiving a
canal input) should have a sensitivity quite distinct from those
neurons with a phase related to position (assumed to receive an otolith
input); however, this was generally not found for FN neurons. As
mentioned in the preceding text, the sensitivity increase was
independent of the phase behavior.
STC of Purkinje cells in the anterior vermis recently has been
investigated in the decerebrate cat (Pompeiano et al.
1997). As in our study of the FN, neurons in the anterior
vermis had a broad distribution of response vector orientations in
response to vertical vestibular stimulation. Although only one stimulus frequency was applied, >70% of the neurons had signs of STC (broadly tuned bidirectional and unidirectional neurons). Purkinje cells in the
cerebellar cortex and the deep cerebellar nuclei are known to have an
irregular firing rate, which also is seen for the vestibular neurons
described here. Also with regard to vestibular functions it is not well
understood which information is reflected in the irregularity of the
activity pattern.
Functional considerations
Spatiotemporal convergence can be achieved by combining two inputs with a different phase and different spatial orientation. Generally this is assumed for canal-otolith convergence, but it certainly also can occur for otolith-otolith interaction.
At a given frequency, the behavior of many of our neurons can be
modeled by assuming linear summation of signals from two cosine tuned
neurons (Kleine, unpublished results). However, it often seems
impossible to simply assume a canal-otolith interaction. With such an
approach neuronal responses would be dominated in the low frequency
range by an otolith-related and in the high-frequency range by a
canal-related input. Evidence for this has been found in the vestibular
nuclei (Baker et al. 1984b). Group I responses and a
phase related to head position should dominate at low frequencies, whereas signals should be related to head velocity at high frequencies. Group II-IV responses should occur mainly in the midfrequency range.
We generally did not find such a clear separation.
We also hardly encountered any neurons for which the phase and
sensitivity relationships allowed the classification of a simple canal-
or otolith-related neuron. In a previous study, we showed (Siebold et al. 1997) that some FN neurons respond to
static tilt and thus prove otolith-related input. For most of these
neurons, dynamic sensitivity was higher than static sensitivity. Thus
given our limited stimulus range, an absence of static sensitivity does not rule out an otolith input (Siebold et al. 1997
).
The interaction of two signals allows for the shift of the ORO over a certain range of orientations. However, we encountered a number of neurons in which the ORO changes clearly exceeded 90°. These neurons also tended to have phase changes of >90°. Further investigations are needed to determine whether these large changes still can be achieved by a linear combination of only two inputs if realistic assumptions are made as to the frequency dependence of the converging signals.
All evidence supports the view that neurons in the rostral FN are
involved in vestibulospinal mechanisms. Unilateral lesions produce a
tendency to fall to the ipsilateral side (Kurzan et al.
1993; Pélisson et al. 1998
). FN neurons
project to the vestibular nuclei (Homma et al. 1995
;
Noda et al. 1990
) and in addition back to the cerebellar
cortex (Batini et al. 1989
). It could be demonstrated that muscimol microinjections into the anterior vermis alter the gain
and spatiotemporal properties of vestibulospinal reflexes (Manzoni et al. 1997
). It is quite possible that FN
neurons interfere with vestibulospinal reflexes in the skeletomotor
system in a similar way. In this context, it is of interest that the
anterior cerebellar vermis sends efferents both directly and indirectly via the FN to the vestibular nuclei (Corvaja and Pompeiano
1979
; Voogd 1989
; Voogd et al.
1991
). It will be a challenge for further investigations to
determine how these direct and indirect pathways from the anterior
vermis to the vestibular nuclei differ functionally.
With regard to the transformation of sensory inputs to motor
performance in three-dimensional space, it becomes increasingly clear
that these relations appear to be far more complex in the skeletomotor
system (Georgopoulos et al. 1988) than in the oculomotor system (Graf et al. 1993
). Our results moreover suggest
that the temporal sequence of events also might be an important factor for determining the neuronal response patterns. They also clearly demonstrate that such a complex response as STC often can be revealed only by a detailed investigation using different frequencies and orientations, whereas the use of a single stimulus frequency would suggest a simple canal- or otolith-related input for a large majority of neurons. The responses of many neurons cannot be attributed to a
certain response orientation (ORO) because it varies with stimulus
frequency. Similarly, phases can change over a narrow frequency range
by >90°. This indicates central processing and prevents an
attribution to a canal or otolith input based on the phase behavior.
The complex response characteristics of vestibular-only neurons in the FN suggest that the sensory information in the cerebellum is transformed and adjusted in such a way that it can no longer be related directly to the sensory input, but it still provides signals that could interface with multiple motor tasks.
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ACKNOWLEDGMENTS |
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The authors thank Dr. S. Glasauer for helpful comments and for critically reading the manuscript, S. Langer for technical assistance, J. Benson and M. Seiche for editing the English text, and B. Pfreundner and I. Wendl for preparing the manuscript.
This work was supported by the Deutsche Forschungsgemeinschaft.
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FOOTNOTES |
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Address for reprint requests: U. Büttner, Neurologische Klinik, Klinikum Großhadern, Marchioninistr. 15, D-81377 München, Germany.
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 14 December 1998; accepted in final form 8 March 1999.
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REFERENCES |
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