Vol. 281, Issue 2, R625-R634, August 2001
Muscle sympathetic outflow during horizontal
linear acceleration in humans
Jian
Cui1,
Satoshi
Iwase1,
Tadaaki
Mano1,
Naomi
Katayama2, and
Shigeo
Mori2
1 Department of Autonomic Neuroscience and 2 Space
Medicine Research Center, Research Institute of Environmental
Medicine, Nagoya University, Nagoya 464-8601, Japan
 |
ABSTRACT |
To elucidate the effects of linear acceleration on
muscle sympathetic nerve activity (MSNA) in humans, 16 healthy men were tested in a linear accelerator. Measurements of MSNA,
electrocardiogram, blood pressure, and thoracic impedance were
undertaken during linear acceleration. Sinusoidal linear acceleration
with peak values at ±0.10, ±0.15, and ±0.20 G was applied in
anteroposterior (±Gx, n = 10) or lateral
(±Gy, n = 6) directions. The total
activity and burst rate of MSNA decreased significantly during forward, backward, left, or right linear accelerations. The total activity of
MSNA decreased to 50.5 ± 6.9, 52.5 ± 4.4, 71.2 ± 9.6, and 67.6 ± 8.2% from the baselines (100%) during linear
accelerations with peak values at ±0.20 G in the four directions,
respectively. These results suggest that dynamic stimulation of otolith
organs in horizontal directions in humans might inhibit MSNA directly
in order to quickly redistribute blood to muscles during postural reflexes induced by passive movement, which supports the concept that
the vestibular system contributes to sympathetic regulation in humans.
muscle sympathetic nerve activity; vestibular stimulation; microneurography
| |
INTRODUCTION |
CHANGES IN MUSCLE
SYMPATHETIC nerve activity (MSNA) are important for maintaining
arterial blood pressure. Data from our previous study demonstrated that
changes in MSNA depend on the longitudinal body component of the
gravity vector from the head to legs during postural change
(10) and that MSNA was suppressed during short periods of
microgravity produced by parabolic flight (9).
The sympathetic nervous system is influenced by a number of reflex
mechanisms. Besides arterial and cardiopulmonary baroreflexes, there is
also considerable evidence that inputs from the vestibular system have
direct effects on the cardiovascular system (2, 7, 12, 21, 24,
25). The neurons in the nucleus tractus solitarius, rostral
ventrolateral medulla (RVLM), and parabrachial nucleus are involved in
the vestibuloautonomic reflex (1, 26-30). Yates et
al. (26) demonstrated that neurons in the RVLM,
which is a major source of excitatory inputs to sympathetic
preganglionic neurons, received vestibular inputs, and vestibular
inputs to the RVLM appear to come mainly from otolith receptors. Data
from animal studies have demonstrated that sympathetic outflow to
renal, splanchnic, and cardiac nerves is modulated by stimulation of the vestibular system (24). MSNA from the human tibial
nerve is enhanced after caloric vestibular stimulation (6,
11), whereas skin sympathetic nerve activity is suppressed and
then enhanced after caloric vestibular stimulation (5).
These results suggest that stimulation of horizontal semicircular
canals has effects on sympathetic outflows to muscle and skin in
humans. MSNA increases during sustained head-down neck flexion in
humans, which suggests that sympathetic outflow is influenced by inputs from otolith organs (13, 20). Furthermore, vestibular
stimulation during linear accelerations can produce responses in blood
pressure and heart rate in humans (25).
Although many studies in animals have focused on the
vestibuloautonomic reflex (2, 3, 13-15, 20), there
are insufficient data on this reflex in humans to elucidate the
response patterning. Sympathetic nerve traffic in the cat splanchnic
nerve was related to the direction of the acceleration of otolith
organs (29); therefore, MSNA response in humans to
stimulation of otolith organs in horizontal (nasooccipital axis or
interaural axis) directions may be different from that to stimulation
in the craniocaudal direction. Although preliminary data suggested that
alternating forward and backward linear accelerations of 0.10 and 0.20 Gx suppress mean MSNA, an insufficient number of subjects
was studied to reach definite conclusions (4). Moreover,
MSNA responses to lateral linear accelerations have not been reported.
The purpose of the present study was to determine the response of
muscle sympathetic outflow from the tibial nerve to dynamic stimulation
of otolith organs in the forward, backward, left, or right directions
in sitting humans.
| |
METHODS |
Subjects.
Sixteen healthy male volunteers [age 20.8 ± 0.9 (SE) yr; height
169.8 ± 5.6 cm; weight 64.3 ± 2.2 kg] participated in the study. Written informed consent was obtained from each subject. The
study was approved by the Human Research Committee, Research Institute
of Environmental Medicine, Nagoya University.
Experimental design.
All experiments were performed with subjects seated in a linear
accelerator capsule (sled) at the Research Institute of Environmental Medicine, Nagoya University. The design characteristics of the linear
accelerator are as follows: 1) a magnetic levitation system is employed; 2) the maximal acceleration is 0.5 G (4.9 m/s2); 3) the experimental capsule mounted on
the sled is shielded against outside light and any electromagnetic
field; 4) the moving distance is limited to 18 m, and
thus positive and negative acceleration occur alternately in one
movement; and 5) linear acceleration in a sinusoidal or step
mode can be selected.
Each subject was strapped into a chair in the capsule, and the body and
head were firmly restrained with Velcro tape (Fig. 1A). The legs were extended at
the knee joint in a horizontal position, and the ankles were supported
at the lower part of the calves. The subjects were in a dark
environment in the capsule.
View larger version (30K):
[in this window]
[in a new window]
|
Fig. 1.
A: experimental setup for the recording of
microneurography, blood pressure with a Finapres device, respiration
with a thermistor, electrocardiography (ECG), and thoracic impedance.
B: acceleration nomenclature: forward acceleration is
defined as +Gx, and the right lateral acceleration is
defined as +Gy. V, velocity.
|
|
Because the recording of MSNA was more stable during linear
acceleration in the sinusoidal mode than during that in the step mode,
linear acceleration in the sinusoidal mode was adopted with a fixed
moving distance of 14 m. The acceleration was applied along the
anteroposterior (±Gx, nasooccipital and occipitonasal) direction in 10 subjects and was applied along the lateral
(±Gy, interaural) direction in another 6 subjects. Forward
acceleration is defined as +Gx, which tends to displace
internal tissues such as eyeballs in the occipital direction (eyeballs
in), and the right lateral acceleration is defined as +Gy
(eyeballs left) (Ref. 8; Fig. 1B). Each
stimulation had five cyclic movements with the same peak acceleration
repeated continuously. There was an initial period of ~23 s before
starting of sinusoidal acceleration. During the initial period the sled
moved to one end of the rail at a constant speed of 0.33 m/s, but
subjects could feel a slight vibration and knew that the acceleration
would start. Three stimulations were applied with peaks of ±0.10 G
(0.98 m/s2), ±0.15 G (1.47 m/s2), and ±0.20 G
(1.96 m/s2) with total periods for the five cyclic
movements of 83.5, 66.5, and 58.0 s, respectively. The interval
between stimulations was 5 min.
Measurements.
The discharge from the postganglionic sympathetic nerve supplying the
triceps surae was recorded from the right tibial nerve by using
microneurography. A tungsten microelectrode with a shaft diameter of
120 µm, a tip diameter of 1 µm, and an impedance of 3-5 M
(26-05-1, Frederick Haer, Bowdoinham, ME) was inserted manually through
the skin without anesthesia into the muscle nerve fascicle of the
tibial nerve at the popliteal fossa. The sympathetic nerve signals were
fed into a high impedance preamplifier (Kohno II, Kohno Instruments,
Nagoya, ×20,000 in gain) and were monitored using a cathode ray
oscilloscope (VC-6524, Hitachi, Denshi, Tokyo, Japan) after band-pass
filtering with a bandwidth of 500-5,000 Hz (E-3201A×2, NF Circuit
Design Block, Yokohama, Japan). The filtered signals were rectified,
amplified, and integrated in a resistance-capacitance network with a
time constant of 0.1 s. The burst of MSNA was identified according
to the criteria of previous studies (10, 22, 23). The main
criteria for identification of MSNA were 1)
pulse-synchronous spontaneous and rhythmic efferent burst discharges
recorded from muscle nerve fascicle, 2) modulation by
respiration, 3) increase by a fall and decrease by a rise in systemic blood pressure, and 4) enhancement by maneuvers
increasing intrathoracic pressure such as Valsalva's maneuver.
Heart rate was monitored by electrocardiography (ECG) using a
bioelectric amplifier (AB-621G, Nihon-Kohden, Tokyo), and the blood
pressure waveform was recorded with a Finapres 2300 (Ohmeda, Louisville, CO) at the subject's left or right middle finger, which
was fixed with adhesive tape at the level of the right atrium. Subjects
were asked to control their respiratory rate at 0.25 Hz with a
metronome. Respiration was recorded with a thermistor at the nose. To
estimate changes in intrathoracic fluid volume, thoracic impedance was
measured using impedance plethysmography (AI-601G, Nihon-Kohden)
with the electrodes taped circumferentially around the neck and
chest at the level of the xyphoid process. All signals were stored
using a multichannel digital audio tape recorder (PC-216A, Sony
Precision Technology, Tokyo). All bioamplifiers and the tape
recorder were fixed in the sled (Fig. 1A). Signals were
monitored in the control room simultaneously.
Data quantification and analysis.
All data were digitized at 200 Hz (16 bits) by off-line processing and
analyzed using LabView software (National Instruments, Austin, TX) with
a computer (Power Macintosh, Apple, Cupertino, CA). Mean arterial
pressure (MAP) was calculated as the sum of the diastolic blood
pressure plus one-third of the pulse pressure in each beat.
Instantaneous heart rate was calculated from the R-R interval. Average
values of MAP, heart rate, and thoracic impedance during 1 min just
before the initial period of the sled motion served as baseline values
(Fig. 2).
View larger version (36K):
[in this window]
[in a new window]
|
Fig. 2.
Representative tracings obtained for 1 subject (subject
1) during sinusoidal linear acceleration in the anteroposterior
direction with peak value of ±0.15 Gx. The traces show the
acceleration (Gx), thoracic impedance (TI), respiration
(Resp), instantaneous heart rate (HR), blood pressure (BP), and
integrated muscle sympathetic nerve activity (IMSNA). The average
values of the variables during the 1 min just before the initial period
of the sled motion were used as baseline values. Acc, total period of
acceleration. First min, the 1st min after acceleration.
|
|
Figure 3 illustrates how each MSNA burst
was analyzed. The computer measured the burst peak latency of the
integrated neurogram from the ECG R-wave and beat-by-beat MAP
simultaneously. Referring to the burst peak latency from the ECG R-wave
and changes in blood pressure, the burst of MSNA was identified by
manual inspection of the beat-by-beat pattern (10, 23).
The burst area of the integrated neurogram was then measured (5,
6). The total activity of MSNA was defined as the burst area of
the full-wave rectified and integrated neurogram with a time constant
of 0.1 s (5, 6, 22). If there was no burst after a
beat, a "0" would be put in the MSNA data series of
beat-by-beat. The final data for the total activity of MSNA
were expressed in arbitrary units by setting the sum of the burst area
during the 1 min just before the initial period of the sled motion as
100%. MSNA was also expressed as burst rate (burst number per minute).
View larger version (36K):
[in this window]
[in a new window]
|
Fig. 3.
The signal processing for muscle sympathetic nerve
activity (MSNA). Recordings from a subject during sinusoidal linear
acceleration in the anteroposterior direction with peak value of ±0.1
G. The burst area of the full-wave rectified and integrated neurogram
was measured burst by burst with a computer. The sum of the burst area
during each phase of the sinusoidal acceleration was then calculated
according to the time segments of positive or negative acceleration.
Finally, the total activity of MSNA at each phase of the sinusoidal
acceleration was calculated as [(sum of burst area of the phase/phase
length)/(sum of burst area of baseline/60)] × 100. The sum of the
burst area during the 1 min just before the initial period of the sled
motion was used as the baseline value (100%).
|
|
To observe dynamic responses during the five cyclic movements, the sum
of the burst area of the integrated neurogram at each phase of the
sinusoidal acceleration was calculated according to the time segments
of the positive or negative phases of the five cyclic sinusoidal
accelerations. The total activity of MSNA at each phase of the
sinusoidal acceleration was calculated as MSNA% = [(sum of burst area
of the phase/phase length)/(sum of burst area of baseline/60)] × 100. The algorithm is illustrated in Fig. 3. Relative changes of mean heart
rate, MAP, and thoracic impedance to baseline values at each phase of
the five cyclic movements were also calculated.
To observe the responses to the direction of the acceleration, the
total activity of MSNA, relative changes of mean heart rate, MAP, and
thoracic impedance during the sum of the periods of positive or
negative acceleration were calculated, respectively, using similar
methods. MSNA bursts during the total period of each direction of
linear acceleration were also counted and expressed as burst number per
minute (burst rate).
Cross-correlograms were used to identify whether a sinusoidal response
was elicited by the sinusoidal stimulus, which were also used to
observe the phase relationships between the acceleration and responses
of hemodynamic parameters (5, 6, 22). After the
hemodynamic beat-by-beat data series were interpolated to equidistant
1-s intervals by a cubic spline function, the cross-correlograms between the sinusoidal acceleration and MSNA, MAP, heart rate, and
thoracic impedance were calculated. The responses to the five cyclic
sinusoid stimuli for each subject were averaged into a single
cross-correlogram.
Values are expressed as means ± SE. We applied a one-way ANOVA to
assess the changes of the variables during baseline, negative acceleration, and positive acceleration, and after acceleration. P < 0.05 was considered as significant.
| |
RESULTS |
MSNA, blood pressure, heart rate, thoracic impedance, and
respiratory flow were obtained for all 16 subjects. Original recordings of thoracic impedance, respiration, instantaneous heart rate, blood
pressure, and integrated MSNA from the tibial nerve during anteroposterior sinusoidal acceleration with a peak value of ±0.15 G
in a representative subject are shown in Fig. 2. There was no complaint
of motion sickness symptoms such as nausea, dizziness, or cold sweating
in any of the subjects.
Hemodynamic responses to the four linear accelerations.
A significant decrease in MSNA was observed during forward, backward,
left, and right acceleration in all subjects. Figure 4 shows original recordings of integrated
MSNA in six different subjects during anteroposterior sinusoidal
acceleration with a peak value of ±0.15 G. Averages of burst rate of
MSNA, MAP, heart rate, and thoracic impedance before and during forward
and backward linear accelerations are shown in Table
1. The results with lateral sinusoidal
accelerations are shown in Table 2. The
total activity of MSNA during the four linear accelerations is shown in
Fig. 5.
View larger version (61K):
[in this window]
[in a new window]
|
Fig. 4.
Array display of changes in MSNA during sinusoidal linear
acceleration in the anteroposterior direction with peak value of ±0.15
Gx. Observations of MSNA suppression were made during
forward and backward linear acceleration. Sub 1-Sub 6, subjects 1-6.
|
|
View this table:
[in this window]
[in a new window]
|
Table 1.
Average burst rate of MSNA, HR, TI, MAP, and respiration rate before,
during, and after anteroposterior acceleration
|
|
View this table:
[in this window]
[in a new window]
|
Table 2.
Average burst rate of MSNA, HR, TI, MAP, and respiration rate before,
during, and after lateral acceleration
|
|
View larger version (30K):
[in this window]
[in a new window]
|
Fig. 5.
Changes in total activity of MSNA during forward,
backward, left, and right linear acceleration with peak values of
±0.10, ±0.15, and ±0.20 G. The total activity of MSNA during 1 min
just before the initial period of the sled motion was used as the
baseline value (100%). Bars: 0.10 G, 0.15 G, 0.20 G, sinusoidal
acceleration with peak values of ±0.10 G, ±0.15 G, ±0.20 G,
respectively. Subject nos.: n = 10 for anteroposterior
acceleration (±Gx), n = 6 for lateral
acceleration (±Gy). * P < 0.05 vs.
baseline value.
|
|
Burst rate and total activity of MSNA decreased significantly during
forward, backward, left, or right linear accelerations at peak values
of ±0.10, ±0.15, and ±0.20 G compared with baselines. The decrease
in MSNA tended to be more apparent with stronger acceleration. Although
there were individual differences in the extent of MSNA decrease (Fig.
4), no MSNA increase was observed in any subject. For a given
stimulation level, there was no significant difference in MSNA between
the forward and backward, or left and right linear accelerations. The
average burst rate and total activity of MSNA recovered to the baseline
level in 1 min.
There were large individual differences in responses of heart rate and
blood pressure during the linear accelerations. Heart rate increased in
some individuals, whereas it decreased in others. MAP increased in some
subjects, but it did not change or decreased slightly in others.
Average heart rate was not changed significantly during forward or
backward accelerations with peak values of ±0.10 or ±0.15 G. Heart
rate was significantly greater than baseline during forward and
backward acceleration with a peak value of ±0.20 G. Average heart rate
was not changed significantly during left or right accelerations with
peak values of ±0.10, ±0.15, or ±20 G. There were no significant
differences in heart rate between forward and backward, or left and
right, linear acceleration. Average MAP during the four accelerations
with peak values of ±0.10, ±0.15, or ±20 G was not significantly
changed compared with baseline. There was no significant difference in
MAP between forward and backward, or left and right, linear
accelerations. Thoracic impedance during the period of 
Gx
was significantly greater than that during the period of
+Gx. There was no significant difference in thoracic impedance during the periods of +Gy and Gy.
Respiratory rates were controlled successfully at 0.25 Hz in all experiments.
Dynamic responses.
Average results of total activity of MSNA, relative changes of mean
heart rate, MAP, and thoracic impedance at each phase of the sinusoidal
acceleration of the five cyclic movements are shown in Fig.
6. The results in Fig. 6 were averaged
responses in each positive or negative phase. Each point in Fig. 6 was
calculated according to the time segments of the positive or negative
phase of the sinusoidal acceleration and is expressed as the change relative to the baseline value. The method of signal processing is
illustrated in Fig. 3.
View larger version (42K):
[in this window]
[in a new window]
|
Fig. 6.
Dynamic changes of the mean arterial pressure (MAP), HR, TI, and
total activity of MSNA during the sinusoidal linear acceleration of
anteroposterior (A) and lateral (B) direction.
The variables were averaged according to time segments of the positive
or negative phase of the sinusoidal acceleration. The periods for one
cyclic movement with peak acceleration of ±0.10, ±0.15, and ±0.20 G
were 16.7, 13.3, and 11.6 s, respectively. Average values of the
variables during 1 min just before the initial period of the sled
motion were used as the baseline values (100%). Graphs: ±0.10 G,
±0.15 G, ±0.20 G, the sinusoidal acceleration with peak values
of ± 0.10 G, ± 0.15 G, ± 0.20 G. Subject nos.:
n = 10 for anteroposterior acceleration (A),
and n = 6 for lateral acceleration (B).
* P < 0.05 vs. baseline value.
|
|
During anteroposterior movement, the sinusoidal acceleration induced
clear rhythmic responses in thoracic impedance, which could be observed
in original recordings and averaged results. The rhythms in thoracic
impedance tended to be more apparent with stronger anteroposterior
acceleration. In the first cyclic movement, heart rate increased
significantly (P < 0.05), while MAP did not change
significantly (Fig. 6). MSNA decreased significantly (P < 0.05) in the first cyclic movement (Fig. 6).
The sinusoidal rhythms in responses of thoracic impedance, MAP, heart
rate, and MSNA can be observed more clearly in cross-correlograms (Fig.
7A). The cross-correlograms
show the extent of the influence of the anteroposterior sinusoidal
acceleration on MAP, heart rate, and thoracic impedance and reveal the
phase relationships between the stimulus and subsequent response. For
the anteroposterior sinusoidal acceleration with peak of ±0.10 G, all
of the correlation coefficients were between +0.5 and 0.5. For the
anteroposterior acceleration with peak of ±0.15 G, the
correlation coefficient between the sinusoidal acceleration and
thoracic impedance had a negative peak (about 0.55) near +1 s. This
result demonstrates that a fluid shift was evoked by the
anteroposterior acceleration at this level. This fluid shift was
delayed by ~1 s relative to the acceleration of the sled. During the
anteroposterior acceleration with peak of ±0.20 G, the correlation
coefficient between the acceleration and thoracic impedance had a
negative peak (about 0.65) near +1 s. The correlation coefficient
between the acceleration and MAP had a positive peak (about +0.75) near
+5 s. Although the correlation coefficient between the acceleration and
MSNA was between 0.4 and +0.4 during the three levels of
anteroposterior acceleration, the cross-correlograms were also in
sinusoidal shapes.
View larger version (30K):
[in this window]
[in a new window]
|
Fig. 7.
Cross-correlograms between the anteroposterior (A) and
lateral (B) sinusoidal accelerations and MAP, HR, TI, and
MSNA. The shift correlation was calculated in the time range of ±1
cyclic movement with sinusoidal acceleration. The scales of the
abscissa expressed in phase are the same for the 3 panels; ±0.10 G,
±0.15 G, ±0.20 G, the sinusoidal linear acceleration with peak values
of ±0.10, ±0.15, ±0.20 G, respectively. Subject nos.:
n = 10 for anteroposterior acceleration (A);
n = 6 for lateral acceleration
(B).
|
|
Heart rate increased significantly (P 
0.05) in the
first cyclic movement during the lateral acceleration with peak values of ±0.10 and ±0.15 G (Fig. 6), while MAP did not change
significantly. During lateral accelerations, all of the correlation
coefficients between the sinusoidal acceleration and MSNA, MAP, heart
rate, and thoracic impedance were between 0.5 and +0.5. The
cross-correlograms showed sinusoidal characters in the lateral
direction with peak of ±0.20 G (Fig. 7B).
| |
DISCUSSION |
The present study was undertaken to examine sympathetic neural
responses to dynamic stimulation of otolith organs in the forward, backward, left, and right directions and to elucidate the sympathetic nerve response to physiological vestibular stimulation. We employed moderate stimulation and avoided evoking motion sickness symptoms. The
present data showed that MSNA expressed as either burst rate or total
activity in sitting humans was suppressed significantly during
sinusoidal acceleration in the four directions.
Possible mechanisms for the decrease in MSNA during linear
acceleration in horizontal directions.
Because average MAP did not change significantly, the average decrease
in MSNA in sitting subjects during the four linear accelerations could
not be considered as a response related to arterial baroreflexes.
Average heart rate increased in some cases, especially in the first
cycle of the sinusoidal linear acceleration. The result was consistent
with a previous study (25), which suggested that the
increase of heart rate was elicited by the otolith stimulation during
linear acceleration. Mental stress might have also contributed to the
heart rate increase that began from the initial period. However, it is
unlikely that the suppression of MSNA during the acceleration was
mainly caused by the increase of heart rate in the present study
because 1) the decrease in MSNA was significant during all
of the four accelerations with the peak values at ±0.10, ±0.15, and
±0.20 G, whereas a significant increase in heart rate was only
observed during forward and backward acceleration with the peak value
of ±0.20 G; and 2) the increase of heart rate during the
first cyclic movement did not induce a significant increase in MAP that
could inhibit MSNA via arterial baroreflexes. The decrease in MSNA was
not attributable to a change in respiration because it was controlled
at 0.25 Hz. Therefore, the suppression of MSNA could not be considered
as an effect of changes in MAP, heart rate, or respiration.
The difference in thoracic impedance between the forward and backward
accelerations indicates that a fluid shift between the legs and trunk
was induced by anteroposterior acceleration. Moreover, the
cross-correlograms between thoracic impedance and sinusoidal acceleration in anteroposterior direction showed very clear sinusoidal mode, whereas the cross-correlation coefficients were low when the
acceleration was in a lateral direction. These results suggested that
fluid shift could be induced even by low-level acceleration when the
trunk and/or legs were in the direction of the acceleration. The
sinusoidal rhythms in MAP and heart rate during anteroposterior acceleration could be considered as resulting from the fluid shift. However, the decrease in MSNA during the four accelerations could not
have been caused by the fluid shift, because 1) although
+Gx acceleration produced a transient fluid shift into the
central compartment and might have produced sympathoinhibition due to loading of cardiopulmonary baroreceptors, Gx acceleration
produced a transient fluid shift into the legs and should have produced sympathoexcitation due to unloading of all subtype baroreceptors, which
was not observed in the present study; and 2) the decrease of MSNA was also observed during left or right linear acceleration, which did not induce the fluid shift.
The correlation coefficients between the sinusoidal acceleration and
MSNA were low. Because MSNA burst rates were low, there were many
cardiac cycles with no MSNA burst. This low burst frequency might
contribute to the low correlation coefficients. Even though the
cross-correlograms between the sinusoidal acceleration and MSNA were
also in sinusoidal shapes, the sinusoidal characters tended to be more
apparent with stronger acceleration.
Vestibular stimulation during linear acceleration can produce
cardiovascular responses in humans (25). There is also
considerable evidence that stimulation of the vestibular system affects
sympathetic preganglionic neurons in animals and postganglionic nerves
in animals and humans (1, 2, 7, 12, 13, 20, 24, 26-30). Therefore, the decrease in MSNA during
±Gx or ±Gy acceleration in sitting subjects
could be a response evoked by stimulation of otolith organs.
Linear acceleration in a sinusoidal mode, used in the present
experiments, was a dynamic stimulation which would induce postural reflexes through the vestibular input in wakeful subjects. The skeletal
muscle pump may be enhanced during the passive reciprocating movement,
but average thoracic impedance and average MAP did not change
significantly, unlike those caused by light dynamic and static exercise
(16-18). It is possible that the dynamic stimulation of otolith organs in the horizontal direction might inhibit MSNA directly. The physiological significance for the decrease of MSNA during the passive movement might result in a quick redistribution of
blood to muscles. A suppression of MSNA induced by vestibular stimulation would decrease the peripheral resistance and increase the
blood flow to muscles that are involved in postural reflexes. The
suppression of MSNA by vestibular stimulation during passive movement
might be a type of feedforward regulation, as hypothesized by Yates and
Miller (29). The contribution of this pathway to cardiovascular regulation would be expected to be smaller than that of
the baroreflex. The individual differences in hemodynamic responses
might be related to intersubject variability in postural reflexes.
Characteristics of MSNA responses to dynamic stimulation of otolith
organs.
The decrease in MSNA observed in the present study was different from
the MSNA responses that were enhanced after a delay of 30-60 s
after the onset of nystagmus induced with caloric vestibular stimulation (6, 11). Because caloric vestibular
stimulation has an effect on the unilateral semicircular canals and
evokes motion sickness symptoms, the enhancement of MSNA in previous experiments (6) could be considered as
vestibulosympathetic responses related to motion sickness, caused
partly by an imbalance between the bilateral semicircular canals.
Linear acceleration stimulated bilateral otolith organs, and no motion
sickness symptoms were observed. This MSNA decrease can be considered a
physiological vestibulosympathetic response in sitting humans
during horizontal movements. Thus the moderate horizontal linear
acceleration applied to sitting subjects induce different MSNA
responses than those induced by caloric vestibular stimulation.
Our finding of a decrease in MSNA in sitting subjects during sinusoidal
acceleration in horizontal directions is different from the significant
increase in MSNA found by Ray et al. (13, 20) during
sustained passive head-down neck flexion in a prone position in humans.
These differences may be explained by three hypotheses: 1)
the utricular afferents were likely altered in the present experiments,
whereas saccular and utricular afferents should be altered by the
head-down neck flexion (19); 2) dynamic stimulation might cause different responses from sustained stimulation; and 3) the changes in acceleration on otolith organs during
the static head-down neck flexion should have been stronger than those in our experiments.
In summary, we found that MSNA was suppressed significantly during
moderate sinusoidal linear acceleration in the forward, backward, left,
or right directions in sitting human subjects. The findings support the
concept that otolith organs contribute to sympathetic regulation in humans.
Perspectives
Data from the present and previous studies have demonstrated that
vestibular inputs, especially from otolith organs, affect the
sympathetic nervous system, which supports the hypothesis that the
vestibular inputs are involved in the regulation of the cardiovascular
system. Different directions of linear acceleration activate different
populations of vestibular receptors. However, the present data show
that MSNA recorded in tibial nerves in humans was suppressed during
linear acceleration in the four directions. MSNA suppression during
linear acceleration may help to redistribute blood to muscles that are
involved in postural reflexes. Because postural reflexes will be
induced when one slips and falls in any of the four directions, and the
muscles in lower legs and feet will be used in the postural reflexes,
the responses of sympathetic outflow to the muscles in legs and feet
should be similarly suppressed during activation of any group of
utricular receptors. However, the responses of sympathetic outflow to
other muscle groups might be different from that recorded from tibial
nerves during horizontal linear acceleration, which could be identified
in further experiments.
| |
ACKNOWLEDGEMENTS |
We are greatly indebted to Dr. M. Saito and Dr. C. G. Crandall
for helpful comments on the manuscript. We also thank H. Kitazawa, C. Sudoh, Q. Fu, and K. Mori for technical support.
| |
FOOTNOTES |
Address for reprint requests and other correspondence: S. Iwase, Dept. of Autonomic Neuroscience, Research Institute of
Environmental Medicine, Nagoya Univ., Furo-cho, Chikusa-ku, Nagoya
464-8601, Japan (E-mail: iwase{at}riem.nagoya-u.ac.jp).
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 6 December 1999; accepted in final form 12 April 2001.
| |
REFERENCES |
1.
Balaban, CD.
Vestibular nucleus projections to the parabrachial nucleus in rabbits: implications for vestibular influences on the autonomic nervous system.
Exp Brain Res
108:
367-381,
1996[ISI][Medline].
2.
Biaggioni, I,
Costa F,
and
Kaufmann H.
Vestibular influence on autonomic cardiovascular control in humans.
J Vestib Res
8:
35-41,
1998[ISI][Medline].
3.
Costa, F,
Lavin P,
Robertson D,
and
Biaggioni I.
Effect of neurovestibular stimulation on autonomic regulation.
Clin Auton Res
5:
289-293,
1995[ISI][Medline].
4.
Cui, J,
Iwase S,
Mano T,
Katayama N,
and
Mori S.
Muscle sympathetic nerve response to vestibular stimulation by sinusoidal linear acceleration in humans.
Neurosci Lett
267:
181-184,
1999[ISI][Medline].
5.
Cui, J,
Iwase S,
Mano T,
and
Kitazawa H.
Responses of sympathetic outflow to skin during caloric stimulation in humans.
Am J Physiol Regulatory Integrative Comp Physiol
276:
R738-R744,
1999[Abstract/Free Full Text].
6.
Cui, J,
Mukai C,
Iwase S,
Sawasaki N,
Kitazawa H,
Mano T,
Sugiyama Y,
and
Wada Y.
Response to vestibular stimulation of sympathetic outflow to muscle in humans.
J Auton Nerv Syst
66:
154-162,
1997[ISI][Medline].
7.
Doba, N,
and
Reis DJ.
Role of the cerebellum and vestibular apparatus in regulation of orthostatic reflexes in the cat.
Circ Res
34:
9-18,
1974[Abstract/Free Full Text].
8.
Glaister, DH.
The effects of long duration acceleration.
In: Aviation Medicine (2nd ed.), edited by Ernsting J,
and King P.. London: Butterworths, 1988, p. 139-158.
9.
Iwase, S,
Mano T,
Cui J,
Kitazawa H,
Kamiya A,
Miyazaki S,
Sugiyama Y,
Mukai C,
and
Nagaoka S.
Sympathetic outflow to muscle in humans during short periods of microgravity produced by parabolic flight.
Am J Physiol Regulatory Integrative Comp Physiol
277:
R419-R426,
1999[Abstract/Free Full Text].
10.
Iwase, S,
Watanabe T,
Saito M,
Kobayashi F,
and
Mano T.
Age-related changes of sympathetic outflow to muscles in humans.
J Gerontol
46:
M1-M5,
1991[ISI][Medline].
11.
Mano, T,
Iwase S,
Saito M,
Koga K,
Abe H,
Inamura K,
Matsukawa Y,
and
Hashiba M.
Somatosensory-vestibular-sympathetic interactions in man under weightlessness simulated by head-out water immersion.
In: Basic and Applied Aspects of Vestibular Function, edited by Hwang JC.. Hong Kong: Hong Kong University Press, 1988, p. 193-203.
12.
Megirian, D,
and
Manning JW.
Input-output relations in the vestibular system.
Arch Ital Biol
105:
151-164,
1967.
13.
Ray, CA,
and
Hume KM.
Neck afferents and muscle sympathetic activity in humans: implications for the vestibulosympathetic reflex.
J Appl Physiol
84:
450-453,
1998[Abstract/Free Full Text].
14.
Ray, CA,
Hume KM,
and
Shortt TL.
Skin sympathetic outflow during head-down neck flexion in humans.
Am J Physiol Regulatory Integrative Comp Physiol
273:
R1142-R1146,
1997[Abstract/Free Full Text].
15.
Ray, CA,
Hume KM,
and
Steele SL.
Sympathetic nerve activity during natural stimulation of horizontal semicircular canals in humans.
Am J Physiol Regulatory Integrative Comp Physiol
275:
R1274-R1278,
1998[Abstract/Free Full Text].
16.
Ray, CA,
Rea RF,
Clary MP,
and
Mark AL.
Muscle sympathetic nerve responses to dynamic one-legged exercise: effect of body posture.
Am J Physiol Heart Circ Physiol
264:
H1-H7,
1993[Abstract/Free Full Text].
17.
Ray, CA,
Rea RF,
Clary MP,
and
Mark AL.
Muscle sympathetic nerve responses to static leg exercise.
J Appl Physiol
73:
1523-1529,
1992[Abstract/Free Full Text].
18.
Saito, M,
Tsukanaka A,
Yanagihara D,
and
Mano T.
Muscle sympathetic nerve responses to graded leg cycling.
J Appl Physiol
75:
663-667,
1993[Abstract/Free Full Text].
19.
Schor, RH,
and
Tomko DL.
The vestibular system.
In: Vestibular Autonomic Regulation, edited by Yates BJ,
and Miller AD.. Boca Raton, FL: CRC, 1996, p. 7-24.
20.
Shortt, TL,
and
Ray C.
Sympathetic and vascular responses to head-down neck flexion in humans.
Am J Physiol Heart Circ Physiol
272:
H1780-H1784,
1997[Abstract/Free Full Text].
21.
Spiegel, EA,
and
Démétriades TD.
Der zentrale Mechanismus der vestibulären Blutdrucksenkung und ihre Bedeutung für die Entstehung des Labyrinthschwindels.
Pflügers Arch
205:
328-337,
1924.
22.
Sugiyama, Y,
and
Mano T.
Spectral analysis of muscle sympathetic nerve activity in humans.
In: A Recent Advance in Time Series-Series Analysis by Maximum Entropy Method, , edited by Saito K.. Sapporo: Hokkaido University Press, 1994, p. 305-314.
23.
Sugiyama, Y,
Matsukawa T,
Suzuki H,
Iwase S,
Shamsuzzaman AS,
and
Mano T.
A new method of quantifying human muscle sympathetic nerve activity for frequency domain analysis.
Electroencephalogr Clin Neurophysiol
101:
121-128,
1996[Medline].
24.
Yates, BJ.
Vestibular influences on the sympathetic nervous system.
Brain Res Rev
17:
51-59,
1992[Medline].
25.
Yates, BJ,
Aoki M,
Burchill P,
and
Bronstein AM.
Cardiovascular responses elicited by linear acceleration in humans.
Exp Brain Res
125:
476-484,
1999[ISI][Medline].
26.
Yates, BJ,
Goto T,
and
Bolton PS.
Responses of neurons in the rostral ventrolateral medulla of the cat to natural vestibular stimulation.
Brain Res
601:
255-264,
1993[ISI][Medline].
27.
Yates, BJ,
Grelot L,
Kerman IA,
Balaban CD,
Jakus J,
and
Miller AD.
Organization of vestibular inputs to nucleus tractus solitarius and adjacent structures in cat brain stem.
Am J Physiol Regulatory Integrative Comp Physiol
267:
R974-R983,
1994[Abstract/Free Full Text].
28.
Yates, BJ,
Jakus J,
and
Miller AD.
Vestibular effects on respiratory outflow in the decerebrate cat.
Brain Res
629:
209-217,
1993[ISI][Medline].
29.
Yates, BJ,
and
Miller AD.
Properties of sympathetic reflexes elicited by natural vestibular stimulation: implications for cardiovascular control.
J Neurophysiol
71:
2087-2092,
1994[Abstract/Free Full Text].
30.
Yates, BJ,
Siniaia MS,
and
Miller AD.
Descending pathways necessary for vestibular influences on sympathetic and inspiratory outflow.
Am J Physiol Regulatory Integrative Comp Physiol
268:
R1381-R1385,
1995[Abstract/Free Full Text].
Am J Physiol Regul Integr Comp Physiol 281(2):R625-R634
0363-6119/01 $5.00
Copyright © 2001 the American Physiological Society
TOP
ABSTRACT
INTRODUCTION
