Journal of Vestibular Research, Vol. 3, pp. 307-314, 1993 Printed in the USA. All rights reserved.

0957-4271193 $6.00 + .00 Copyright © 1993 Pergamon Press Ltd.

CRUCIAL EFFECTS OF WEIGHTLESSNESS ON HUMAN ORIENTATION

H. Mittelstaedt* and S. Glasauert

*Max-Planck-Institut fOr Verhaltensphysiologie, Seewiesen, Germany; tLaboratoire de Physiologie Neurosensorielie, Paris, France

Reprint address: Prof. Dr. Horst Mittelstaedt, Max-Planck-Institut far Verhaltensphysiologie, D-82319 Seewiesen, Post Starnberg, Germany

o Abstract - This contribution examines the con-sequences of two remarkable experiences of sub-jects in weightlessness, 1) the missing of sensations of trunk tilt and of the respective concomitant re-flexes when the head is tilted with respect to the trunk, and 2) the persistence of a perception of "up" and "down," that is, of the polarity of the subjec-tive vertical (SV) in the absence of, as well as in con-tradiction to, visual cues. The first disproves that the necessary head-to-trunk coordinate transforma-tion be achieved by adding representations of the respective angles gained by utricles and neck recep-tors, but corroborates an extant model of cross-multiplication of utricular, saccular, and neck receptor components. The second indicates the ex-istence of force-independent components in the de-termination of the SV. Although the number of subjects is still small and experimental conditions are not as homogeneous as desired, measurements and/or reports on the ground, in parabolic, and in space flight point to the decisive role of the saccu-lar .t-bias, that is, of a difference of the mean rest-ing discharges of saccular units polarized in the rostrad and the caudad (±.;;-) direction.

o Keywords - interactioli of otoliths anc; neck receptors: sUb.iective verticai in weightlessness; saccular bias; force-independent components.

This comriou"ior: Geal~ WEf: :W( :-esult~ 0: space flight tna, are crucia: f 0:- specific iS5uef of human oriematior.. One has come as 2. sur-prise, the other passed almost unnoticed. We should like to begin with the latter.

Effect of Weightlessness on Head-to-Trunk Coordinate Transformation

A vertebrate that can move its head inde-pendently of its trunk must somehow allow for

the angle between head and trunk if the trunk's position is to be controlled by information from sense organs in the head. This is true for passive as well as for active head movements since in most vertebrates head position can be altered passively without upsetting trunk con-trol. As early as 1949 (1-3) it was suggested that a representation of the deviation (Phead) of the head from the vertical, gained by the otoliths, is added to a representation of the an-gle Pneck between head and trunk, gained by neck receptors, so that a measure of the devi-ation Ptrunk of the trunk from the vertical re-sults (Figure 1, panels a through d). This idea has since been followed up in various ways (4,5). Moreover, neurons in the vestibular nu-clei have been found (6,7) that show the en-visaged relation between head and neck tilt.

There is an obvious consequence of the hy-pothesis that representations of these two an-gles are added. If one of them is eliminated, mere head tilt will cause sensations of trunk tilt. as well as the respective postural responses (Figure;, panel e). Now, i: may be a:-gued t~a: bilale,al section of the VlII th nerve may not vield incontrovertihle proof ir: thi~ : ase . j r -

. - . ___ S~ . .. . ~ ~ ':":;~ 'j-': "': ~-I. ':'_ : ~ : ,G._5 : JJ·:; ':" j c.. ", u G. Ca~ .)e :-

G r:1assiv~: b ;-ea l~ dovl,t ~. 0: o ",,'e:--aE a ,::!\,ity ir: t ne vestibular nuele: , b li owec:. by the much-stud-ied adaptation processes. However, weight-lessness will do, because the entire information processing system is in perfect shape when it enters zero g.

This, then, is the crucial result that passed almost unnoticed: We have no reports of (il-lusory) sensations of trunk tilt upon mere head tilt (of equal amplitude!), let alone of the re-spective reflexes, after entry into weightless-

307

308 H. Mittelstaedt and S. Glasauer

Phead 0°

Pneck 0°

Pttllnk 0°

(labyrinthectomized)

~ (I " ~

I

}\ ~ \ (f \

b c d

i=lgure 1. (a, ~,c,d) ?ostural limb reilexes upon trunk tilt (Ptrunk) are independent of head position (Phead), if neck ;eceptor signals coding neck ;ilt (Pneck) are subtracted from otolith signals coding Phead, since Ptrunk = Phead - Pnack' If otolith signals are missing, however, mere head tilt should cause "neck reflexes" (e). This prediction is clearly falsified by the absence of "neck reflexes" and of perceptions of trunk tilt upon head tilt in weightlessness (after reference 3, modified).

ness - events that could not possibly have been overlooked.

This negative result is in fact predicted by an alternative model developed some time ago (8-10). It is shown in Figure 2. In this model the neck receptor messages are first trans-formed into sine and cosine components and then multiplied crosswise with the respective utricular and saccular messages before the products are summed. In weightlessness both products are zero or, in Ss with an additive saccular bias, very nearly zero. Such a small deviation may be subthreshold for an illusory sensation of trunk tilt, but still sufficient to cause, or to contribute to, the well-known pro-"n,,.

Ii

Weightlessness and Human Orientation

Head pos. program

309

-Figure 2. Head-to-trunk coordinate transformation by way of cross-multiplication. For definition of roll angles see upper pictograph (ane' ~igurE i) g : normalizec' amoun' 0 ' gravit ' "e::to~ : U; sin ~'he"": res:>:mSE 0; the utricles to heac~ rolf : Sg::::lS.lJhClH ~E'SO~H1S: 0.': sc?c~Ldef ;c "ec~ .. :-j ' " ", 5'" A. t'lP':: ." :.- ~~!7 l .,~ ~ · "'eS:l~n~e: · =- ' thE neel: receptors to neel; roli: U. E. Ny. I\:z : gains. r : efierent commanc:.: prociucin£ trunf. counter-roiL Nots tha'. neck tilt has no effect on r. and thus does not produce neck reflexes or. the trunr. a: any r-Ioad, if UfI!z = SNy. hence also ir. weightiessness where f is zero.

Theory

It is therefore of theoretical as well as of practical interest to explore the cause(s) of those illusory experiences of verticality. Ac-cording to an extensively validated model of the subjective visual vertical (SVV) (14,15),

they are the necessary consequence of a dif-ference between the resting discharge activi-ties of otolith units polarized in a rostrad ( + z) and those polarized in a caudad (-z) direc-tion, termed z-bias. Briefly, in the model the otolithic afferences are summed according to the direction of their polarization vectors. This

j. i· .

\ I t ~ I· .\t . . ,. :. j ~.' i

310

yields three components that are then normal-ized. Finally, an idiosyncratic egocentric vec-tor (termed "idiotropic vector") is added, and the resultant is cross-multiplied with the vec-torial components of the visual field's polar-ity. (In our standard test the visual field consists of a well-polarized display, namely a rotatable luminous pendulum in otherwise to-[ai dar:mess. J

~ n weighriessness. oniy :he f()r:'~- indepe!1-·te "1i 'Jar· ~· :- j' -~1e . 1n:~ ~.:('mr !~ ner1 i S .vi P ''=lo_

. . .'"!l :l::-:' . :1 ~ :7:": •. f _ ".: !::- .- :~~ -:=; -= :,:; .:-: ~: :'S l ; : ::.:. :; !. x =l-aias ~ ..lr'tc the cict!-(;pic \'ec~cr . In : :g-ure 3 we shall :.l.ssume chat zhe utric:.uar y-bias is zero, as indicated by the above mentioned absence of a roll deviation of the SV at g = O. For the sake of simplicity, the pitched-up ori-entation of the labyrinth in the head is ne-glected (for a detailed treatment see reference [15]) as well as a possible x-bias. As graphi-

\-1 . Mi' J staedt and S. G:asauer

cally and formally shown in Figure 3, visual "up" or "down" will be determined by the id-iotropic vector and the z-bias. However small the z-bias may be, normalization will amplify it to unity. Hence, its sign will determine the polarity of the illusion if, as usually the case, the idiotropic vector is smaller than unity .

Ways )/ Validariil'J

-:-';.' .~::. ~c ~:;r :; c:~c:lOn. ao':.' :0 ';erir"it::uicn -Ji ~ejec::c!1: It ~ l~:; oe::::1 sho'N:} :::~per:men-tally (l6) ~i1at the SV''; obtains its gravity information exclusively from the otoliths-without any noticeable effect of somatic gravi-ceptors. Thus, we need to know the sign of the otolithic z-bias and the amount of the idio-tropic vector in order to predict the SVV in weightlessness.

R=M-l= -0,5

9=1

Uo=O ...•.....•......

u =0

s=l:-l 1501

~ _____ --------v-------------J 9=0

Figure 3. Prediction of SV at g = 0 from a model of the SVV. The saccular component s of the phYSiological gravity vector (s = So + 51 gcosp), its utricular component u (u = U1 gsinp) and the idiotropic 'lector (M; here assumed to be 1/2 of U1 ) are combined in the CNS by a process that is formally identical to vector addition. The resultant R points toward the subjective zenith (SZ), which deviates from the physical zenith (PS) as de-termined by the parameters (So, 51, U1, and M). Note that, before summation with the idlotropic vector, the otolith signals are normalized by the divisor N. With g = 0, the divisor N becomes equal to the absolute value of So, and hence the Z-axis component of the gravity vector s = 50 /150 I will be minus or plus unity, depend-ing on the sign of So. A negative saccular RD-bias So will cause an inversion illusion (CFI) if M < 1. Note that the larger M and, hence, the smaller the resultant R, the perception of inversion becomes the more unstable (whereas, with a positive So, the perception of uprightness is apt to become the more dominant).

1 I

~htt~E~ssnel:;S and Human Orientation

, the subjective body position 'fIIiiSl:'been shown to depend on both otolithic

_ _ .'t·1rt somatic graviceptors, but not on the id-lOtropic vector (17,18). Thus, in order to pre-dict subjective body position, we need to know the sum of the otolithic and somatic z-bias. Now, this sum could be determined from a measurement of the subjective horizontal po-

::Sition (SHP) on a tiltable board, provided the ~ feels horizontal if and ,:,hen the joint z-com-_~·~o"'''c of the two gravIty systems are zero,

z = So + Bo + (S 1 + B d g cos Ph = 0 [1]

where So is the saccular bias, Bo the somato-sensory bias, SI and BI the gains (sensitivities) of the two systems, g the magnitude of the normalized force vector, and Ph the angle of roll tilt at which the S feels horizontal. Clearly then

... (So + Bo)/(SI + Bd = -g cos Ph' [Ia]

Whether equation (1) is valid can obviously be ...tested by increasing the force load on a gon-;aola centrifuge: At g = 2 the absolute devia-tion of Ph from 90° should be about halved (COSPhlg/COSPh2g = 2).

Evidence

We have checked this by combining mea-surement~ 0; the SHP and the SVV on a tilt-able board, a sled centrifuge, and a gondola centrifuge 2nd com narec. then; witi': mea.:;ure-ments of tne S\'\' anCc estimaie~ 0: bod:' po· sition ir ~ .. - . r' "' •. -' ~ - . 'r_ .... . ~ :-Ja.l aU .. )lJ ~ .1, :::-,. 1. \.'!' ....... ... ..J....: ... .. showed thf exnectec idiosyncrasies: Inversion, uprightness. and indifferen:::e. OD the centri-fuge, however , the absolute deviations of the SHP from 90° were not halved at 2g. More-over, the sign of the joint z-bias failed to al-ways predict the polarity of the illusion in parabolic flight under visual occlusion. We therefore tried to modify the model of equa-tion (1) under the assumption that the otolithic afference is normalized whereas the somato-

311

sensory afference is not, that is, by assuming that Ss feel subjectively horizontal if

=0 [2]

where N is defined as in Figure 3. Hence at g = 0,

Z = So/ISol + Bo. [2a]

body position is exclusively determined by the sign of So.

In fact, the body position estimaces at g = 0 could be qualitatively predicted by the modi-fied model from the SHP at g = 1 and g = 2. However, it failed to predict the position es-timates quantitatively. The following caveats should therefore be kept in mind:

1. The number of Ss is small (8), and some of the Ss were insufficiently trained.

2. For technical reasons the flat surface of the tiltable board could not be installed in the gondola centrifuge. This may have caused the large deviations of the SHP data in the tiltable gondola of the standing centrifuge from those on the tiltable board.

3. The duration of micro gravity in a parab-ola may be too short for completion of all orientation processes.

On the other hand, several results are in ac-cordance with the original model (Eq . 1) , but at va,;ance wi:h the Olociifiec. \ e~s ior ..

J) The latzer (compart:! equa!ioli : anci _'::;'ig-

cal predictionc /cjr ir version i/h!SlOns oj .- m l'isua!/ielcl ;:nd ihr: hody posiTion. ELl.' the'·c were devialionsjrol17 lhis ruie in parricipanzs of our parabolic flights. This has also been found by Lackner (20) in the reports of Ss who were seated and strapped by lap belts, with eyes open during the period of weightlessness of the parabola. Of his 68 probands, 58 felt either self and plane both upright (23 Ss) or both inverted (35 Ss), yet 10 felt either self

,

-.

~ " ~ ' " " r"

L.

312

upright and plane inverted (2 Ss) or vice versa (8 Ss), at least during the first 5 parabolas.

According to equation 1 and Figure 3, the two opposite orientations would happen when the somatic bias Bo had a sign different from, and an absolute magnitude larger than, the saccular bias So. With equal distributions of the two biases, each rype of opposite orienta-tion ,vG!I!d be expec:f![i ,n ! :;,Y110 of 5s, the two ai/zers ,:n 37,': 1110 e!1L'.''l, ;:{olVeVel', in experi-"0''"': ,,17 , hv 'i!trth1e h OI/I'd (18), rhe somatic

tVi1en Ss ~lre 'n.l :.;it ~: ::g .Josi!iofl. Thl~ ,ne.." ;:!!!J(! lO :'he shifr fa ""I'd II verSlOil ?/ ;e!f, ,vhich ,:S Gcnlally found in {he -!l1nre paltern cited above, But the smaller number 0/ opposite ori-entations (10 compared with the 17 expected) may be due to the well-known circumstance that it takes keen and unabashed observers to acknowledge experiences that defy all reason. In fact the paradoxical phenomena almost vanished in the subsequent parabolas, what with increasing dominance of visual cues and cognitive censure (a process that may be termed Palmstrom's razor: "weil nicht sein kann was nicht sein darf"; for translation see Appendix).

2) Under prolonged weightlessness in or-

H, Mittelstaedt and S, Glasau,

bital flight, the SHP on the tiltable bOQl turned out to yield a satisfactory prediction I the polarity of the illusion with thejoint z-bi, determined from equation 1 a as minus cos, (Figure 4). The orbital data in these 6 cas stem from in/light and postflight reports ( the polarity of the subjective vertical in /1 view 0/ the well-known interior of the spa vehicle (for details see reference II). Tn Oli aile of these cases do :ve also /1I1ve a repo/'{ , the s/lbjec!fve body ,'Josition under DCc/Lid ' ;5io /l: ,-:e!''! : i !1! P I) /uF' [:: :.:r' r,'!i:! :) V ;ur.'1ed 0

!o ,)eJeen fieal :tnt! :;1f.iepe.'1den [ of : he S's Q

ss and Human Orientation

~s respect it is pertinent that Diamond and ~kham (21 ,22) have found a correlation be-It;Ween ocular disconjugacy and space sickness lilata. In their experiments, changes in ocular disconjugacy are brought about by changes of the z-force component from 1.8 g to zero g and hence, presumably, by the z-component of the .otolith system. It is remarkable that ap-proaches from such different directions ap-pear to converge on the same point.

ditions of Figure 3, with utricles lying in the x-y plane and saccules parallel to the x-z plane, onIy the saccules would be affected by the z-component of the force, and hence would yield a z-bias if the mean resting discharge of the units polarized in the plus z-direction dif-fered from that of their minus z opponents. The utric1es, however, could then be affected only by the x- andy-components of the force, rand hence would yield a y-bias as a conse-'quence of a bilateral asymmetry of the mean 'RDs. If such ay-bias would exist, or reappear atmicrogravity, as hypothesized byv. Baum-garten (23), a roll tilt of SVV and subjective body position must ensue, in contrast to all known reports from Ss in orbit.

Yet, if the planes of the two utricles were

313

roll tilted with respect to each other, either sides up ("" /) or sides down (/ ""), infor-mation about the z-force component could be extracted from them in the same way as from the saccules, resulting in a negative z-bias in the sides-up or a positive one in the sides-down case. Also, a positive or negative disconjugacy of ocular roll tilt upon change of force load (21) could result from such an arrangement, for instance, if each utricle would predomi-

eye. Clearly, then, data on the arrangement of the otoliths and their interindividual variations in man are urgently needed. By means of high resolution NMR-tomography, it may soon be-come possible to determine the plane of the horizontal semicircular canals, which are par-allel to the utricle's main plane (24) and, thus, to compare the anatomical with the physiolog-ical and psychophysical data in the same proband.

Acknowledgments-We thank the members of our staff in Seewiesen, foremost Evi Fricke and Willi Jensen, the crews of ESA, NASA, DLR, and the Fliegerhorst Fiirstenfeldbruck, as well as, last but not least, the probands who carefully indicated their SV under the stress of various G-Ioads.

REFERENCES

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2. Mlii~ist~ed. i-i. Dh ~'s!Oiogit' ae, Gl tichge\\ icnt ssinne~ be: f1legenaen :" i{1elier :;: .. e~f: :> i' '' ·SI0. '5".::' 4::-63.

3. von ~~ols : E. iV' lti';."'lsi aed : ~: JC! F~ ~ c.!f re r·: ;-] Z l'~ l rl :::lr' (Vvecnse! wln: ull t.- z.wischen Zentralnc:-\'en ~\'SlCn' t!;lC. Penpheriel. !'>ialU"wiss. 1 ~5()::- :464- 7o.

4. Lmdsay KW, Roberts TDM. Ro~enberg JR. Asym-metric tonic labvrinth reflexes and their interaction with neck reflex"es in the decerebrate cat. J Physiol (Lond). 1976;261 :583-601.

5. Kornhuber HH. The vestibular system and the gen-eral motor system. In: Kornhuber HH, ed. Handbook of sensory physiology, G (Chapter 2, esp. p. 583-585). Berlin, Heidelberg, New York: Springer-Verlag; 1974.

6. Pompeiano 0, Manzoni D, Srivastava Uc. Responses of medullary reticuiospinal neurons to natural stim-ulation of labyrinth and neck receptors. Neurosci Lett (Suppl). 1982; 10:393.

7. Wilson VJ, E7ure K, Timerick SJB. Tonic neck re-

fle:; of the decerebral~ cat : response of spinal inte. -neurom to natural sllmulation or neel an,: vestibula rccernor, .. "'l~uronh \·sio .. ~

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MIT Canadian vestibular experiments on Spacelab-l mission; 4: space motion sickness: symptoms, stim-uli, and predictability. Exp Brain Res. 1986;64:316-34.

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14. Mittelstaedt H. A new solution to the problem of the subjective vertical. Naturwissenschaften. 1983 ;70: 272-81.

5. :v1ittelstaedt :-f. T~e role or' :he pit.:hed-up orienta-,ion or ' he ,)[olirhs n .wo -ecenr !TIouels of he ,ub-jective .. e:-;ical. Bioi C/bem. :989:ol:405-i6 ,

n: _ ~ :lrJ.shi \,II. 31aL.~ -=. x.s. ~/c~t::ou!ar :.lnc ·.:~ 3 U :.i! ~onlro i on posture ami :ocomo!Or :::quilibrium. 7th ;memational SympOSIUm ,ll !nte;national Society tor Posturography. Houston -:'e:;as. Basel: Karger; 1983: 139-50.

17. Mittelstaedt H, Fricke E. The relative effect of sac-cular and somatosensory information on spatial per-ception and control. Adv Oto-Rhino-Laryngol. 1988;42:24-30.

18. Mittelstaedt H. Somatic versus vestibular gravity re-ception in man. Ann NY Acad Sci. 1992;656:124-39.

19. Glasauer S, Mittelstaedt H. Determinants of orienta-tion in microgravity. Acta Astronautica. 1992;27: 1-9.

20. Lackner J. Sense of body position in parabolic flight. Ann N Y Acad Sci. 1992;656:329-39.

21. Diamond SG, Markham CH. Otolith function in hypo- and hypergravity: relation to space motion sick-ness. Acta Otolaryngol (Stockh). 1991; 481(Suppl): 19-22.

H. Mittelstaedt and S. Glasauer

22. Diamond SG, Markham CH. Prediction of space mo-tion sickness susceptibility by disconjugate eye tor-sion in parabolic flight. Aviat Space, Environ Med. 1991 ;62:201-5.

23. von Baumgarten RJ, Vogel H, Kass JR. Nausogenic properties of various dynamic and static force envi-ronments. Acta Astronautica; 1981;8:1005-13.

24. Takagi A, Sando I. Computer-aided three-dimen-sional reconstruction and measurement of the vestib-ular end-organs. Otolaryngol Head Neck Surg. 1988; 98: ! 95-:02.

Palmstr6m is a crearion of [he German ;:>oet Christian Morgenstern. P., a suave elderly gen-tleman with a lively mind and a philosophical sense of humor, a sort of latter-day lichten-berg, is, in the poem to be cited, run over by a car, and finds out afterward that motor vehicles were not allowed by law on that part of the road. The poem goes on as follows:

And he arrived at the conclusion that the event was mere illusion because, he argues cuttingly, it cannot be what mustn't be.