Correlation between vestibular sensitization and leg muscle relaxation under weightlessness simulated by water immersion

Acta Astronautica Vol. 8, No. 5--6,pp. 461---468,1981

0094-57651811050461--08502.00/0

Printed in Great Britain

Pergamon Press Ltd.

Correlation between vestibular sensitization and leg muscle relaxation under weightlessness simulated by water immersion GENYO MITARAI,

T A D A A K I M A N O r AND Y O S H I H I K O YAMAZAKI

Department of Aerospace Physiology, Research Institute of Environmental Medicine, Nagoya University, Chikusa-ku, Nagoya 464, Japan (Received 23 January 1981) Abstract--The experiments were designed to determine the contribution of the leg muscle relaxation to the sensitization of the vestibular function under weightlessness. The neuromuscular unit (NMU) discharges were continuously recorded with microelectrodes from the anti-gravitational soleus muscle and its antagonist, the tibialis anterior, of a man standing first upright on the level floor of a dry water tank, and then gradually being immersed in water till it reached his neck; while he was buoyed with an airtube placed under his armpit. In each of the successive states, the caloric nystagmus was evoked, analyzed and compared with the NMU discharge as well as with subjective symptoms associated with the nystagmus. The results indicate that the nystagmogenic activity had a significant correlation with the appearance of the active NMU in the soleus, and they also suggest that the reduction of ascending signals from the antigravity muscles might be one of the causes of atypical vestibular responses occuring in weightlessness.

Introduction MOTION sickness in space is assumed to be caused by defective or lack of coordination between the visual and vestibular inputAt The primary cause of this affliction must be the atypical excitation of the vestibular receptors due to the absence of an environmental force, such as gravity. Guaitierotti et al. (1971) reported that in the bullfrog the vestibular neurons enhanced their spontaneous discharge and showed an increase of excitability when subjected to centrifuge stimulation during the initial days of an orbital flight. The effect of the centrifuge stimulation on the vestibular response, which they observed, may be explained by the fact that the ampullary receptors of the semicircular canals and the otoliths go'on transducing their respective angular and linear acceleration, even in weightlessness. This enhancement of the spontaneous discharge suggests that there is some intrinsic disturbance in the vestibular neuron. In our previous experiments,§ we found that the caloric nystagmus had a tendency to accelerate with the increasing submersion of the upright standing experimental subject. This finding led us to speculate that the reduction of tPresent address: Department of Physiology, Hamamatsu University School of Medicine, Hamamatsu 431-31, Japan. :~See, Benson, 1974; Graybiel, et al., 1975. §See, Mano et al., 1977; Mitarai et al., 1979. 461

G. Mitarai et al.

462

ascending signals from the antigravitational leg muscles under hypogravic conditions may result in vestibular activation. To verify this hypothesis, the present study was designed to examine the correlation between three parameters in the caloric nystagmus: the latency, the duration and beat number, and the active NMU number in the leg muscle, obtained in different states of water immersion. Methods

Our results were obtained from sixteen experiments with eight healthy, 25-38 year old males. In each experiment, the subject was standing upright on the level floor of a dry water tank before being gradually immersed in water up to his neck. During immersion the subject was buoyed with an airtube placed under his armpit. The water temperature was kept at 34°C all the time. During the immersion, the NMU activity was recorded with tungsten microelectrodes of a tip diameter of 2/xm from the antigravitationai gastrocunemius soleus and its antagonist, the tibialis anterior ot both legs (Fig. 1). In each of the following four states (1) standing dry, (2) immersion in water up to the navel level, (3) to the neck level and (4) buoyancy, the caloric nystagmus was induced by injecting 10ml of water (20°C) into the right external acoustic canal and recorded by means of electronystagmogram (ENG). The injection rate of water was kept constant at 1 cm3/sec. During the caloric test, the experimental subject was visually deprived, by wearing shadowed goggles, and he was requested to express the range of his subjective symptoms associated with the nystagmus. Results and discussion Leg muscle activity during water immersion The NMU

a c t i v i t y of the s o l e u s w a s c h a r a c t e r i z e d b y a n u m b e r of c o n -

CAL I

1-SOL

r

E.0

1-TA

/

J

Fig. 1. Method for recording etectronystagmorgrams (ENG) ind/aced by caloric stimulation and NMU discharges from the soleus (SOL) and the tibialisanterior (TA) of both the right (r) and left (I) leg.

Correlation between vestibular sensitization and leg muscle relaxation

463

tinuous discharges while the subject was standing in the dry. Inversely to the gradually increasing immersion in water, the discharges decreased in frequency until they disappeared at the breast or sometimes at the neck immersion level. In contrast, the N M U activity of the tibialis anterior which was minimal in the dry state, appeared and increased from the navel level on, and, with an increasing spike number, it became maximal at the neck level (Fig. 2). In the state of buoyancy all N M U stopped. In many cases, a NMU recording gave simultaneous discharges of four to six units through a single electrode. For example, in the recording from the right soleus under dry condition, six different units were encountered (Fig. 2). The discharge pattern as a whole appeared to be somewhat irregular, but most of the single N M U in the soleus generated tonic spikes with a constant interval and amplitude. Their decrease during gradual water immersion resulted from the falling off of the number of active N M U rather than from a degrading activity of a single NMU. The spikes behaved with a somewhat "all-or-none" characteristic (Fig. 3). The NMUs in the tibialis anterior gave rise to fast phasic discharges, corresponding to the changing number of units. In all the experiment the number of active NMUs in each muscle were added up with every 10% increase of the immersion level, up to the neck (100%). The results are shown in the histogram in Fig. 4. From the initial dry position to the breast immersion level (70-80%) the soleus showed a continuous and gradual reduction of the active NMU number. The immersion phase from the breast to the neck level was characterized by the reverse transition of the active unit number from the soleus to the tibialis anterior. A

r-SOL . l , ~ l l J t , ~ . l ~ J h L k LI~I dJ,i~ J.~ i~ r-TA 1-SOL

t

I

* t

I

6r;iT~-, ] , k, l xr]qT ~L i J , i~i.,-~ , a . ~ , . . .pa V ~=~i,~...I 4~,,,. I.r n u

1 -TA

r-TA

I-SOL

ttt

:

Jl I I I I 1 I r r ,

r ~i ; "

I-TA

C

r-SOL r.TA

1-SOL

lili rlT[

i l l l ~ i i ] r t g l : l l l

f

}11

iliElill

I

~ll

lll'llIl

I

!

1 -TA D

r-SOL r-TA 1-SOL 1-TA SO0 msec

Fig. 2. NMU discharge from the soleus (SOL) and the tibialis anterior (TA) of both legs while (A) upright standing in the dry, (B) at the navel, (C) the neck water immersion level, and (D) buoyancy.

464

G. Mitarai et al.

! r h l i i ! . i l l l lil l l i l l l l / iJ l l h i l liiJ u: ll.,~ iiAII I d i l l ,.Lli h l i l l ;

DRY

~ I Ill h'll~lil fp, IIl~ilrillfil~i~ ifll lPlli~l~, NyIII lr~ r

WATER i l / L i i Lili LLliilil [ lJ~ IJ LiiJ Ill lUd Ill dix I i]l|ii-lii~J I Llill,J tl-i.

40 cm

pIllm I,I,I1fll lfllll'1111llll I 1~I,'1;I ~i! I !111Ilill Ill~ 1fill,"i! 7, '

6 0 cm I l l b L I d i d ' ' l ' l l L l l l l l l l l u l u l l l l l L i ' l i l i l l i l i l l ' d l l i l l l j ~ l l

Mlllplllrllll~ll~ll~ltllfilllllll!llll~l~ll!111111 8 0 Clll

RII !

i l l l l l l | l l a l l l t l l l l l l l l l l l l l l l l l l l l l l l l l l l l l l l l u l i J l D i O l l

(THIGH) Nlllllii

I

IIIIIN~I lIITllrll

100 cm I ! I l l ! l l l l l l l (NAVEL) 1 r i ] 7 i ] l ~ i [ l ' l ]

120 cm , (BREAST)

IJ] I,II!lli

,

NIN~TT i 7 IHUil

,"~,i,,,[l ..... -* . . . . . .I,,l,,, . "

I

i iJ,

0.5 mv

1 sec

Fig. 3. Soleus N M U discharge in different states of water immersion.

Caloric nystagmus and N M U activity The individual susceptibility to caloric stimulation varied greatly from one test subject to the next; sometimes it rose so much with the increasing water immersion level that the test had to be discontinued. Consequently, the present data for the ENG were obtained from only six subjects. Figure 5 shows the ENGs for each of the three following states: standing dry (A), the navel (B) and the neck (C) level immersion. The slow, i.e. 1.5 sec time constant recording showed the direction of the eye movement, while the fast, i.e. 0.03 sec time constant recording gave the details of the latency, the number of beats and the duration of activity. Latency here means the delay that occurred between the end of the injection of cold water and the onset of the nystagmus. As Fig. 5 clearly demonstrates, the latency became shorter with the increasing SOII:IIS

TIRIALIS ANTERIOR

5O 4O

m m

m

10' u

,

,

,

,

,

,

,

,

,

.

0 1020 30 4050 50 7 0 8 0 90 100

F

60708090100

%

ll@qERSION LEVEL

Fig. 4. Histogram s h o w i n g total N M U n u m b e r in different states of water immersion.

Correlation between vestibular sensitization and leg muscle relaxation

B

465

~ -'-~ " " - ~ "

'~PlW'n[T~l" pp'eeel,r~l'qllr,,rl,l, r l l t l l ~ ' "'

~

c

~v Rt .

1

tt~

Caloric stim.

10

sec

Fig. 5. 1.5 sec (upper curve in each state) and 0.03 sec (lower) time constant recordings of ENG in dryness (A), neck immersion level (B) and buoyancy (C).

immersion level and reached a minimal value with buoyancy. This shortening of latency seemed to be concordant with the increase of the beat number and the duration of activity. Figure 6 shows further examples of ENGs and integrated electromyograms (EMG). First, the EMGs were obtained from the surface of the gastrocunemius, previously to each caloric test. Together with the EMGs, the NMU discharges were also recorded from the same soleus and tibialis anterior, and their total number, from six experiments, were added up for each of the four states: dryness, navel and neck immersion level and buoyancy (Fig. 7). The curves showing the changes of the NMU number had the same tendency already mentioned. Then, the mean values of latency, duration of activity and beat number of ENGs obtained from the six experiments were plotted against the total number of N M U given in Fig. 7. The results obtained from the soleus clearly showed a significant correlation between the NMU number and each of the latency and the beat number (Fig. 8). The correlation coefficient was 0.99 (p < 0.01) for the latency and -0.96 (p < 0.05) for the beat number. Only the A

ENG ~ ,

.d

EHG

tEMG

" 'q " _L

i

,

T

..........

T i,

:~ :

,,

,

ENG EMG

"

,i

....

i. .....

l

.

.

.

.

.

.

.

.

/

Left

D

~w

EMG "-" C a l ° r i c s l i m 30 F i g . 6. E N G

and integrated soleus EMG immersion

sec

in the dry (A), at the navel (B) and the neck (C)

level and the buoyancy

(D).

466

13. Mitarai et al.

30

,.o

0

A

I

I

DRY

I

I

l

NAVEL BREAST NECK

BUOYED

IMMERSION LEVEL Fig. 7. Changes of total number of active NMU in the soleus (filled circle) and the tibialis anterior (triangle) with increasing water immersion.

duration had no significant correlation with the NMU number resulting in a coefficient of -0.78. Yet, in the state of buoyancy, the duration was always prolonged distinctly in comparison with that in the state of dryness. In contrast to the NMU of the soleus, the N M U of the tibialis anterior bore no relation to any of those parameters. Though we have not been able to prove a direct mutual influence between the antigravity muscle activity and the vestibular system, the sensitization of the vestibular system observed in our experiments seems to indicate that the loss of the ascending signals from the antigravity muscles in hypogravic state, results in the release of the inhibitory effect which the signal usually has on the vestibular system under terrestrial gravitational conditions. It may well be that the same mechanism accounts for the increase of the spontaneous discharge of the vestibular nerve found by Gualtierotti, et al. (1977) in the bullfrog experiment during orbital flight. Subjective symptoms during caloric test The caloric nystagmus was usually associated with vertigo, nausea, tilt sensation and other autonomic symptoms. In all sixteen experiments, these A

B

C

sec t 15r

250

3O

I's

2oo~ 1 Or," ~ so

_

l's

2

~

30

ls

o

NMU NUMBER/SEC

Fig. 8. Relation of the latency (A), the duration (B) and the beat number (C) of ENG to the total number of active NMU in the soleus.

Correlation between vestibular sensitization and leg muscle relaxation

467

Table 1. Symptoms during caloric test Nausea

Tilt sensation

Conditions

Vertigo

Dryness

±

±

+++

Immersion

+

+

++

Immersion t o neck

++

++

+

Buoyancy

+++

+++

to navel

symptoms were registered in each of the four states from dryness to buoyancy, classified into four grades from the weakest (±) to the strongest (+ + +), and summarized in Table 1. The tilt sensation diminished with an increasing immersion level, possibly due to the relaxation of the antigravity muscles. Apparently, no change was found in the angle between the head and the rest of the body, because the experimental subject kept the straightening of the neck. On the other hand, the vertigo and nausea became more intense with an increased immersion level and reached their maximum intensity during buoyancy. This increasing sensation of vertigo and nausea corresponded well to the activation of the caloric nystagmus, a fact that supports the idea that the reduction of ascending signals from the antigravitational leg muscles results in the acceleration of the vestibular function. Conclusion From the present results, it can be concluded that in the state of weightlessness, the reduction of afferents from the antigravitational muscles contributes to the atypical vestibular activation. The interaction between the vestibular, and possibly or probably also the visual system, and the leg muscle activity seems to continue somehow in the state of weightlessness and in the correspondingly modified movements. The neuromuscular/vestibular reciprocity should, therefore, be considered as one of the important contributing factors in the etiology of motion and space sickness. Only appropriate experiments in space flight can prove or disprove this hypothesis. Acknowledgements--The authors want to thank The Educational Department for having supported

this research with a grant for Gravito-physiologicalStudy of Adaptation to Environment (No. 337007, 1977-79) and Mr. S. Takagi and Mr. M. Kono for their efficient technical assistance. References Benson A. J. (1974) Possible mechanisms of motion and space sickness. Proc. 12th Europ. Syrup. on Life Sci. Res. in Space, ESA pp. 101-108. Graybiel A., Miller E. F. and Homick J. L. (1975) Individual differences in susceptibility to motion-sickness among Skylab astronauts. Acta Astronautica 2, 155-174.

468

G. Mitarai et al.

Guartierotti T. and Bracchi F. (1971) Spontaneous and evoked activity of bullfrog's vestibular statoreceptors in weightlessness. Proc. Int. Union Physiol. Sci. 9, 222. Mano T., Nishimura T., Takagi S. and Mitarai G. (1977) Effects of partial body weightlessness on the vestibulo-ocular reflex in man. Proc. 12th Int. Syrup. on Space Tech. & Sci., Tokyo, pp. 809-814. Mitarai G., Mano T., Yamazaki Y., Mori S. and Takagi S. (1979) Compensatory leg muscle activity in man during adaptation to weightlessness simulated by water immersion. Proc. Ann. Sci. Meeting of ASMA, Washington, D. C., pp. 89-90.