Journal of Vestibular Research, Vol. 7, No.4, pp.

283-302,1997
Copyright © 1997 Elsevier Science Inc.
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Review

INTERACTION OF EYE-, HEAD-, AND TRUNK-BOUND INFORMATION

IN SPATIAL PERCEPTION AND CONTROL*

Horst Mittelstaedt
Max-Planck-Institut fOr Verhaltensphysiologi, 0-82319 Seewiesen, Germany
Reprint address: Horst Mittelstaedt, Max-Planck-Institute fOr Verhaltensphysiologie,
0-82319 Seewiesen, Germany. Tel: +49-8157-932371; Fax: +49-8157-932209;
E-mail: mittelstaedt@mpi-seewiesen.mpg.de

D Abstract- This article reviews the author's in-
vestigations on the perception and control of spa-
tial relations if the carriers of the relevant sense
organs are mobile and controlled independently of
each other. In the dragonfly, head rotation is con-
trolled by the head's inertia, as well as by cervico-
collic, optokinetic, and dorsal light reflexes and, in
turn, controls trunk rotation by means of neck
reflexes on the wings. In humans, invariance of
head-referenced visual direction under eye-to-head
rotation is attained by feedforward of an efference
copy. In the pigeon, invariance of responses to
trunk tilt under head-to-trunk rotation is, in
flight, achieved by feedforward of head-to-trunk
information yielded by neck receptors. But in
standing or walking, this is accomplished by
means of gravity sense organs in the trunk. Such
organs are also shown to exist in the human trunk
by means of experiments on a sled centrifuge.
From tests with paraplegic and neuromectomized
subjects, it is concluded that truncal graviception
1) is not influenced by mechanoreceptors in the
legs, the skin, and between the vertebrae but 2) is
j
affected by at least two afferent inputs, one origj·
nating in the kidneys, another in the tissues that
support the large blood vessels against the gravita-
tionalload. These conclusions are corroborated by
experiments with bilaterally nephrectomized sub-
jects and by means of positive air pressure to the
legs, respectively. Recent results under application
of positive and negative air pressure to the entire
*This is an autobiographical review based on a lecture at
the Third International Symposium on the Head/Neck
System, Vail, Colorado, July 2-6, 1995.
lower body indicate that yet another source of so-
matic graviception may exist, for example, one
that exploits the hydrostatics of blood pressure or
the inertia of the mass of the abdominal
viscera. © 1997 Elsevier Science Inc.
D Keywords - neck reflex; efference copy;
somatic graviceptor; lower body negative pressure
(LBNP); cervicocollic reflex; renal afference;
otolith.
From Eye to Head to Trunk
The Head as a Torsion Pendulum
It all began with a chance observation. Erich
von Holst, who had discovered the "dorsal light
reflex" in fishes, had accidentally seen a drag-
onfly landing upside down on a surface illumi-
nated from below. He supposed that orientation
to the luminance centroid of the sky might be
substituted for orientation in an animal
without statoliths, and suggested dragonfly ori-
entation as a topic for my doctoral thesis (1).
Instead of the then usual procedure, namely,
of observing the behavior of the freely moving
animal under stationary environmental condi-
tions, I restricted the dragonfly movement to
pure roll by means of a harness and a system of
strings, and rotated the visual environment
around it (Figure 1). Thus, the animal hovered
in the center of a cylinder that could be rotated
about an earth horizontal axis, collinear with the

283
284 H. Mittelstaedt

Lst

z
<

J F

l'----_I _I _ _Sf _ __

Figure 1. Harness consisting of a string and strips of linen, glued to the thorax and the first abdominal segment
of the dragonfly (Anax imperator Leach). By means of braces (Sb) and elastic strings (F) the harnessed animal
is hung in the axis of a rectangular wire frame (R), about which a contoured or plain white cylinder (Z), illumi-
nated by a shielded (P) light bulb, can be rotated.

insect's long axis, either homogeneously white
or half-black and half-white, or with longitudi-
nal stripes. Notably, this method has become
quite popular since, and much refined through
automatic control of the environment's move-
ment by feedback of the animal's movement.
But in 1947, I had to be the controller myself.
The dragont1y turned its back into the cen-
troid of the luminance indeed, irrespective of its
direction to gravity. It also followed the stripes
with very small retinal slip by head and trunk
movements (Figure 2a). Thus, if the dragont1y
was tilted in a structured environment, the head
remained virtually upright, while the wings
showed prompt and effective compensatory re-
t1exes. Yet, to my surprise, this also happened
in a perfectly homogeneous environment or in
darkness (Figure 2b). Even in an anesthetized
animal, the head remained briet1y in place when
the trunk was quickly tipped.
I found, then, that the head acted like a torsion
pendulum (Figure 2d), and its angular deviation
from the trunk elicited compensatory ret1exes
on the wings (Figure 2, panels a, b, and c) as
well as counter-rolling cervicocollic ret1exes on
the head. Subsequently, I discovered a complex
system of hair plates in the neck (Figures 3 and
4) and showed by means of nerve sections how
it released these two types of reflexes. I con-
cluded that the position of the head, controlled
by its own inertia and the cervicocollic ret1exes,
as well as by the optokinetic and the dorsal light
ret1exes, elicited neck ret1exes on the wings that
forced the trunk to follow suit.
The Principle of Reafference
Thus, from the very start, I found myself in-
volved in head-neck problems. In my thesis (1,
Spatial Perception and Control 285

a. 6Y-=-=

b.

:~:I~
---. " oS.. ~ ~ l\ ~

c.
Figure 2. The head of Anax as a torsion pendulum. (a,b,c) Experiments in the set-up of Figure 1: (a) If the
striped cylinder is rotated to the right, the head is rolled to the right and the wings twisted so as to produce a
rightward roll of the body; (b) its momentum of inertia lets the head lag behind movements of the body, eliciting
compensatory reflexes on the wings; (c) the body follows suit if the head, with a tiny iron filing glued to the
clypeus, is rotated by means of a magnet. (d) model of the head's mechanics, showing the laterocervical scler-
ites that carry' the head by means of minute twin joint (KG), as well the 6 head muscles, 4 recti (HM, 8M), and 2
obliqui (RM).

printed in 2) I discussed the question whether
dragonflies are able to make voluntary head
movements just to look around, that is, without
eliciting neck reflexes on the trunk. I realized
that this problem appears not only in the: case of
head movement, but also in the case of volun-
tary movements in general: How are voluntary
movements in spite of the opposing static and
dynamic reflexes at all possible? At that time,
the generally accepted solution for this problem
posited that during a voluntary movement all
opposing reflexes had to be shut off by inhibi-
tion. But I found it hard to believe that the ani-
mal should be deprived of all of its head refer-
enced information when it was most needed.
In order to put the inhibition hypothesis to
test, I rolled the head of a drone fly (Eristalis
tenax) by 180 0 and glued it to the prothorax in
that attitude (3). (Such large torsions are often
seen during eye cleaning!) As expected, rota-
tion of the striped drum about a vertical axis
caused the fly with inversed eyes to rotate in the
opposite sense of the drum. In a homogeneously
white cylinder, illuminated from below, such a
fly moves around quite normally. If the opto-
motor reflex were inhibited during voluntary
movements, the same normal behavior should
be seen when the homogeneous cylinder is re-
placed by a stationary striped drum. Yet now
the fly rotated or oscillated about its dorsoven-
tral axis as soon as it started to move. I con-
cluded (3) that within the fly, a central nervous
mechanism existed that coupled a voluntary
motor command with the optokinetic afference
caused by it. This idea was further elaborated in
my thesis (1,2), but I did not specify the mecha-
nism by which this coupling of the command
with its inevitable afferent echo might be ef-
286 H. Mittelstaedt

Figure 3. Lateral view of the dragonfly's head and prothorax. Only the head is bisected (somewhat to the left of
the median plane). 1: head jOint at the rostral tip of the laterocervical sclerite (22) of the prothorax which carries
the head; 32: tentorium, the central head skeleton to which the head joint is attached; 23: triangular pad at the
rear end of 22, which can be pressed into a fitting groove (40) at the head to fixate it, or to set it free by contrac-
tion of the 4 recti (41) or the 2 transverse muscles (42), respectively; 2: hair plate at the joint, stimulated by a
sclerite (3) during left roll; 11: its afferent nerve to the subesophageal ganglion (6); 4,43,45: ventral and dorsal
hair plates, innervated by the prothoracic (13) ganglion (for example, 4 by 15). Note that the largest masses
within the head, the compound eyes (39) and the mouth parts (57-61), are concentrated at the periphery, maxi-
mizing the momentum of inertia.

fected-quite wisely so, as we shall see pres-
ently.
But later in that propitious year, von Holst
ran into me one morning with a reprint of Korn-
muller's report (4) on the effect of eye paralysis
on his vision, and cried, "Here is what you al-
ways say should then happen: The entire visual
world moved to the right when he tried to look
to the right!" In our common article entitled
"Das Reafferenzprinzip" (5), we explained this
phenomenon and the behavior of the fly by as-
suming that a "copy" of the motor command to
the eye, named "Efferenzkopie," is added to the
visual afference caused by the command,
named "Reafferenz." The two signals are cali-
brated so as to annul each other if (and only if)
no externally caused visual afference, named
"Exafferenz ," is present. If the calibration is
Spatial Perception and Control
Figure 4. Ventral view of head and prothorax. The mouth parts are removed and the left side of the prothorax is
opened. For notation, see Figure 3 legend.
perfect, only the ex afferent part of the total af-
ferent inflow can pass the summation, and
hence that part which contains information is
separated from that which does not.
In the following years, I tried to formulate
this hypothesis in terms of control theory. In the
case of the invariance of headcentric visual di-
rection under eye rotation, the analysis showed
that, given the experimental evidence, ar: effer-
ence copy is indeed necessary to provide a co-
ordinate transformation of visual direction from
eye to head. HoweveL the oscillation and rota-
tion of the fly with reversed vision does not nec-
essarily imply an efference copy. Rather, it may
be due to the reversal of the sign of the optomo-
tor feedback loop alone. Thus, in the case of the
normal fly, addition of the command itself to
the optomotor feedback loop would suffice to
make voluntary movements of the fly possible
(see pages 155 to 157 and Abb. 7 in ref. 6). We
(5) did not realize this in 1950 because we be-
287
lieved that the permanent rotation could only be
provided by an internal positive feedback loop,
and we used, or rather misused, an efference
copy to that end in our model (see Abb. 4 and 7
in reference 5), just as did Roger Sperry (7) in
the case of a newt with reversed eyes. However,
although not necessary and rather unlikely, the
existence of such a positive internal loop has
beer~ ex::1Lldec1
neither in the fly nor in the newt.
Still later, in 1958, I found that, in order to an-
nul the reafference, the efference copy must em-
body the same transfer function as the product of
the transfer functions of all systems in the reaf-
ferent pathway from the efference it copies to the
reafference it annuls: An efference copy must act
like an internal model of the systems it bridges.
This then led to insights into the principles of the
information processing that yields invariance of
spatial perception and control under eye and head
movements (8, reviewed in 9 and 10).
288
1=-300
r = _30 0
(a)
v (b)
Figure 5. Wing responses of the pigeon to static roll tilt. I: angular deviation of the head from the vertical, h: an-
gular deviation of the head from the trunk, r: angular deviation of the trunk from the vertical. In (a) and (b), equal
but opposite wing reflexes are seen; in (c), no reaction.
The Head-to- Trunk Coordinate
Transfo rmation
When a sitting pigeon is passively roll tilted
with its long axis in an eru.ih horizontal position
under exclusion of visual cues, it makes prompt
balancing movements with its wings and legs
that would rotate it back if it were free to move.
The response is the same whether the head is
tilted with the trunk or kept horizontal during
trunk tilt. However, when the head is tilted while
the trunk stays horizontal, nothing happens (Fig-
ure 5). In 1906, Trendelenburg (11) had con-
cluded that these responses are released by grav-
ity sense organs in the trunk. In my thesis (1,2;
p. 439) I showed that they could be explained in
yet another way, namely, by subtraction of a
neck position signal from the otolithic signal
about head posture. When the entire animal is
tilted, the response is then released by the
otoliths; when only the trunk is tilted, then the
response is released by the neck receptors; when
only the head is tilted, then both cancel exactly,
provided the responses in the first two cases are
the same for the same tilt angle (Figure 6, upper
diagram; throughout this article "position"
means the angular relation of a part of the body
to another, whereas "posture" means its relation
to the direction of gravity, and "tilt" means a
deviation from its upright posture).
Later on, I found that this invariance of the
trunk response under head rotation is preserved
H. Mittelstaedt
I = -30'~
r = -;-.30" r= 0
0
(c)
at any trunk posture and even under an in-
creased G-load (12). Hence, the gravity infor-
mation could not be yielded by the utricles
alone. Rather, I suggested a cross multiplication
mechanism of the utricular and the saccular sig-
naIs \vith representations of the respective sine
and c9sine components of the angle between
neck and trunk (Figure 6, lower diagram), in
fact, a complete 3-dimensional vectorial coordi-
nate transformation from the head-bound infor-
mation to the trunk-bound motor control.
In order to test this hypothesis, I examined
three labyrinthectomized pigeons. These pi-
geons never flew again in the three years that
we observed them. However, some months after
the operation, they were indistinguishable from
the normals in the above-named tilt tests of the
wing reflexes. It turns out, then, that both Tren-
delenburg's and my own hypothesis are con-
firmed by these results: Pigeons need the vestib-
ular system (and, of course, the eyes) when they
are t1ying, and hence must then perform a com-
plete coordinate transformation from the head
to the trunk. Yet they also possess a second
gravity sense organ in the trunk which is used in
sitting and walking.
Thus, for gravity orientation in t1ight the
otoliths are necessary and, possibly, also suffi-
cient, whereas for gravity orientation in sitting
and walking, the truncal graviceptors are suffi-
cient and, possibly, also necessary.
From then on I wondered whether a similar
Spatial Perception and Control 289

f$ '* d = '*-h*

~
h w

h h*

h d = sin I . cos h-cos I . sin h

cos I . si n h

Figure 6. Models of the basic information processing structure of the wing reflexes of Figure 5. Upper diagram:
Subtraction of central representations I. and h. of the angles I and h, derived from the otolithic and the neck af-
ferences, respectively. Lower diagram: Cross-multiplication of utricular and saccular afferences with the re-
spective sine and cosine components of the neck afference and subsequent subtraction of the products. Note
that the resulting invariance of the wing response under head tilts is then preserved even under varying
G-Ioads.

situation might exist in other vertebrates as well
and, possibly, even in man. And this led to the
topic, taken up in 1988 (after investigations on
bicomponent control, idiothetic orientation, path
integration, and the visual vertical) that will
now be treated in some detail.
Somatic Graviceptors
a centrifuge that had been designed in the six-
ties by Howard C. Howland. He had provided it
with a horizontal platform" and this gave us] the
opportunity to fit it with a sled that can be
shifted radially by remote control (Figure 7).
In the traditional centrifuge paradigms, the
resulting force acts normal or parallel to the
subject's z-axis, that is, on the otoliths and the
putative somatic graviceptors in the same direc-

Existence Proof
I "We" in the following includes my longtime coworkers
Paradigms and methods. To prove the exist- Evi Fricke, Willi Jensen, Reinhard Strobele, and Karl
ence of graviceptors outside the labyrinth I used Fischer.
290
Figure 7. Subjective horizontal position (SHP) on a
rotating sled centrifuge. The subject is pi aced right
ear down on a sled that can be moved radially along
the subject's spinal (z-) axis via remote control by the
subject (as well as by the experimenter). Due to the
additional acceleration, the subject feels tilted de-
pending on the distance between the gravity sense
organ(s) and the centrifuge axis, and moves the sled
until she feels horizontal. In this subjectively horizon-
tal position (SHP), the distance d of the centrifuge
axis from the binaural axis is then recorded (negative,
if the former is caudal of the latter).
tion and by the same or nearly the same amount,
respectively. Hence, the resulting phenomena
do not tell us whether they are caused by the
otoliths or the somatic graviceptors or both.
But when subjects are oriented earth-hori-
zontally and (as in Figure 7) so that the centrifu-
gal force acts along their z-axis, extravestibular
graviceptors must reveal themselves if they
have any effect on the perception of posture.
If the centrifuge axis is collinear with the
binaural axis (see Figure 7, middle panel), the
otoliths are not affected by the centrifugal force;
hence they indicate a horizontal posture. Yet
graviceptors in the body are then, in addition to
gravity, subjected to a force that is directed to-
H. Mittelstaedt
wards the feet, and hence they indicate a head-
up deviation from the horizontal.
But we first need to know whether the sub-
jects are, in fact, able to estimate their subjec-
tive horizontal posture (SHP) accurately. To
that end we tested our subjects on a tiltable
board (Figure 8). The experimenter sets the ini-
tial tilt in total darkness to arbitrary, yet strictly
up-down alternating angles and then asks the
subject to rotate the board until she or he feels
horizontal. The angle E between the subject's
z-axis and the horizontal plane is measured by
means of a potentiometer.
The subject has been instructed not to make
cognitive inferences, but is told, "Just act as you
feel-as you are used to doing when sitting or
standing upright in the dark". At the start of a
session, the experimenter tilts the board (with
constant velocity of 0.5°/s) and signals the sub-
ject to take control of the board. When the sub-
ject has signaled that he or she feels horizontal,
the experimenter records the setting and tilts the
board by an arbitrary amount in the opposite
direction; and so forth. As a rule a session is ter-
minated after 8 pairs of settings, but only the
last 6 pairs are used to compute mean and vari-
ance of E as the "subjective horizontal position"
(SHP). On average, subjects are able to assume
their personal SHP with an SD of ± 1 degree.
In a subsequent session on the centrifuge, the
same procedure is followed with the subject
placed in the same way on the sled (Figure 7),
which can, by remote control, be moved radi-
ally over its horizontal surface (sled velocity:
2.2 crnls). In all experiments, the centrifuge is
run with w = 2 'IT times 0.6 rotations per second
and hence produces 0.0145 G per cm radius.
Sled position is measured as the distance d of
the centrifuge axis from the binaural axis, posi-
tive if the centrifuge axis is cranial of the binau-
ral axis (see Figure 7).
Basic results. On the tiltable board, most sub-
jects show an idiosyncratic deviation (E) of their
z-axis from the horizontal plane (upwards posi-
tive). These deviations are small, but fairly con-
stant even over years. In our 32 normal subjects
(leg position as in Figure 8) they are normally
distributed about a mean of zero with a standard
deviation of E = ±3.2°.
Spatial Perception and Control 291

Figure 8. The subjective horizontal position (SHP) on a tiltable board. The subject, head fixed by means of a
bite board, lies on a padded board that may be rotated by remote control. In total darkness, the subject, starting
from alternating head-up or head-down positions, rotates the board until he or she feels horizontal. The SHP is
measured as the elevation (€) of the subject's z-axis from the horizontal plane, head-up being positive.

Obviously, these deviations will also bias the
centrifuge data, hence, they must be accounted
for in their evaluation: Consider a subject who
feels horizontal at a positive elevation E on the
board. If the otoliths alone would determine the
perception of posture, this subject would feel
horizontal on the centrifuge at a positive dis-
tance d (as in the upper picture of Figure 7).
How do we determine that expected distance?
Our centrifuge produces 1G at 69 cm distance
from the centrifuge axis. Hence, at the site of
the otoliths, the vector resulting on the centrifuge
has the SaIne tilt angle as on the board at a distance
e of 69 em times tan E. Now we have good rea-
son to suppose that the subjects. when asked to
orient themselves horizontally, use only the z-axis
component of the vector and hence fee] hori-
zontal when e is equal to 69 cm times sin E. Be-
cause the sine and the tangent are virtually iden-
tical at the small elevations found in our subjects,
our conclusions are independent of whether the
former or the latter is actually realized.
In Figure 9, the distance d measured on the
centrifuge is plotted over the distance e ex-
pected under exclusively otolithic control.
Hence, if that would be the case, all points
should lie along the dotted line (d = e). Yet the
settings of only two subjects come near it. All
others set the sled more caudally than expected
under exclusively otolithic control. In normals,
the line of least square distance (LSD) crosses
the ordinate (e = E = 0) at d = -25 em, whereas
in bilaterally neuromectomized subjects, the
intercept of the LSD is at d = -45 cm, that is , in
the area of the last ribs (note that the LSD is to
apply here, instead of the regression line, because
e and d are both dependent variables).
The result proves the existence of somatic
graviceptors, and it indicates that their mass
centroid lies near the last ribs. Moreover, the
slopes of the LSD's in Figure 9 are near unity,
and, hence, become virtually zero if the e-val-
ues are subtracted from the d-values. and the
difference ~d - e) i~ plotted over l
Hence. this difference meaSlU'es an effect of the
somatic graviceptors that is independent of the in-
dividual deviation of the subjective from the ob-
jective horizontal: It measures the gain indepen-
dently of the bias. The relative weight W of the
somatic graviceptors in the perception of the
horizontal posture may thus be determined by
dividing the difference d - e by the distance de
of their mass centroid from the meatus. Thus W
is defined as ·(d - e)/de, with de assumed to be
on average at d = - 50 cm. It is a nondimen-
sional number expected to range from zero (ex-
292 H. Mittelstaedt

d [em]
.
20

10
."
.. -.. '
.' . .' . .+
.
.. ' .. '
~ o
•
- 0 - - S 113
Normal
Neuromect.

' . " " - " ' . x=y

-10

-20

-30

-40

-50

-60~----~----~----------~-------~----r-----r-----~--~

-10 -5 o 5 10 15 20 25 30
o
e [em]
o o o o
-8.3 o 8.3 16.5 25.8 E [deg]

Figure 9. SHP of 32 normal and 5 labyrinthine-defective subjects, right ear down, legs flexed, on a tiltable board
and on a sied centrifuge, which produces about 1.5 G per meter radius in the direction of the subject's spinal (z-)
axis. Ordinate: distance d of the centrifuge axis from the subject's binaural axis where he or she feels horizontal
(see Figure 7). Abscissa: distance e computed from the subjectively horizontal tilt angle E on the board; e 69 =
cm*sin(e), that is, the distance where the subjects would set their binaural axis if the otoliths alone would con·
trol the SHP. Brackets represent SO. Lines of least square distance (LSD) are fitted to the settings of the two
=
groups. Note that one subject (8113) sets herself almost at d e (in two sessions 4 years apart), 3 subjects be-
have like subjects without otoliths, and the rest show compromise positions.

clusive control of the SHP by otoliths) to unity
(exclusive control by somatic graviceptors). W
does not measure the efficacy of the gravicep-
tors in general however: On the subjective vi-
sual vertical (SVV), the somatic graviceptors
have no (or even a slight inverting) effect (13).
All 32 normal subjects, that is, also the three
who behave like the neuromectomized ones in
Figure 10, have a normal SVV, that is, well-
functioning otoliths.
Localization of the Somatic Graviceptors
Since the area of the last ribs is not too far
from the mass centroid of the entire body, the ef-
fect of centrifugation might be caused by mecha-
noreceptors in the skin or in the legs, affected by
the inevitable support forces. But if they are act-
ing exclusively on the soles, or exclusively on
the pelvis, thus stressing or straining the legs, no
change of the distance d on the centrifuge is ob-
served (13). When the legs are flexed, however,
that is, hips and knees bent by about 90 degrees,
subjects show a head-up increase of the elevation
E on the board and a decrease of the absolute dis-
tance between centrifuge axis and binaural axis
on the centrifuge (that is, an increase of the d-val-
ues and the e-values; compare Figure 11). Again,
this is not due to the support forces to buttocks or
soles, because the d-values are unaffected by the
addition of lead cuffs (13).
This result opens the possibility of manipu-
lating the effect of the somatic graviceptors. By
testing normals and selected patients with legs
extended and flexed on board and centrifuge,
Spatial Perception and Control 293

20 o Normal
d-e[cm] • Neuromect
- 0 - - S 113
10

o ------.----~---I·:--------------~-~-·----·--+-----------------.-­

~1 0
~ :f m~
~20

~30
:a~ t
-40

-50

-60-+----~-----+----~----~----~----~------~--~

-10 -5 o 5 10 15 20 25 30 e [em]
o o o o
~8.3 8.3 16.5 25.8 £ [deg]

Figure 10. The same tests and subjects as in Figure 9, but with the difference d - e plotted over e. The slopes
of all lines of least square distance (LSD) are now virtually zero, indicating that the force-dependent gain on the
centrifuge is largely independent of the force-independent bias on the board. Note that subjects without otoliths
set d - e between -45 and -55 cm, hence, at the site of the centroid of the mass(es) governing the somatic
graviceptors.

the location of the somatic graviceptors can be
narrowed down.
Paraplegic patients with total bilateral le-
sions from the 5th lumbar to the 6th cervical
segment (inclusive) divide into two groups
which are clearly different in their settings from
each other but homogeneous in themselves
(Figure 12). Subjects with lesion between the
5th lumbar and the 12th thoracic segment (in-
clusive) behave like normals in all four tests.
Subjects of the remaining group, with the le-
sion between C6 and Thll, called TC-paraple-
gics, do not show an effect of leg flexion on the
tiltable board (compare Figure 12), yet they still
exhibit a relatively large one on the centrifuge
(Figure 13). The mean relative weight W is
smaller than in normals, but far from zero. In
both groups there is no conelation between the
individual values of Wand the height of the
lesion.
These results afford the following conclu-
sions: Mechanoreceptors in the skin or between
the vertebrae are excluded as a source because
otherwise, due to the strictly segmental innerva-
tion of both, deficits should increase and the rel-
ative weight W should decrease with the height
of the lesion.
There are (at least) two separate graviceptive
inputs:
1. The first input enters the cord at the 1 ] th tho-
racic dorsaJ root. Since at this point the renal
nerve enters the cord, bilmeraliy nephrecto-
mized subjects were recruited, and indeed
found to behave, in all four tests, like TC-
paraplegics (Figure 14).
2. The second input enters the brain cranial of
the 6th cervical segment. Candidates for de-
livering information from the trunk to the
brain at a point higher than that are the N.
vagus and the N. phrenicus. So far no sub-
ject with lesions of these nerves has been
available.
294 H. Mittelstaedt

• board ......... y=1.52x+3.74

o centrifuge ------- y=1.20x+13.57

.. .'
•
: .
I

o ~'--------------~(~~J'----------~'--,r,~-----------------
'-' 0' :'.
0' (J.:'

-15

normal

-30

-45 ,,
,
, ,, <"0

If
e,d [em]
1ong
-60 ~.-~---'----"------'-----+----r-------"

-60 -45 -30 -1 5 o 15 30

Figure 11. SHP of normal subjects on the tiltable board (e) and on the sled centrifuge (d) with legs flexed (~ong,
d tong ) on the abcissa and with legs flexed (eShorh dshort) on the ordinate. Note that the d-values are far from the
e-values, the "short" values generally larger than the respective "long" values, and the slopes of the lines of
least square distance (LSD) larger than zero.

Hypotheses somatic graviceptors, the weight W would be-

The source of the input at the j 1th thoracic
segment. The results on the nephrectomized
subjects prove that the kidneys contribute to
gravity perception. It is an open question, how-
ever, whether they function like statoliths or af-
fect postural perception in another way, for ex-
ample, by changing the parameters of the
gravitational control systems. Yet, the prerequi-
sites for a measurement of inertial force are in-
deed given: A density difference between the
kidney and the surrounding adipose capsule and
a circumferential array of mechanoreceptors
that measure pressure towards the surface of the
kidney (14,15). If these receptors were the sole
come zero in nephrectomized and TC-paraple-
gic subjects. If not, it should at least be reduced,
and this is indeed the case. However, because
this reduction is significant only in TC-paraple-
gics with flexed legs, the hypothesis needs fur-
ther corroboration.
The source of the input cranial of the 6th cervi-
cal segment. The existence of a second input
follows from the residual weight (W > > 0) in
TC-paraplegics. A hypothesis about its origin is
suggested by the large significant effect of leg
flexion found on the centrifuge in these sub-
jects. Since it is still present when all afference
from below the 5th cervical segment is lost,
Spatial Perception and Control 295

Paraplegic Patients
C4
C5
C6
C7
C8
TH1
TH2
TH3
TH4
TH5
TH6
TH7
THB
TH9
TH10
TH11
"
~t.O-
TH12 "
~
L1 ,I

,:
L2 "
~
L3 "
~
L4 "

L5
~
I:
"

51
,:
"

Normal

-1 0 - 5 o 5 10 1 5 20
Figure 12. Dependence of the effect of leg flexion on the height of the lesion in paraplegics, compared to that in
normals (lowest line). Ordinate: Segments of the spinal cord; C: cervical, Th: thoracic, L: lumbar segments.
Points indicate site of lesion (hence an L 1 paraplegia is denoted by a point between Th12 and L 1). Abscissa:
eshort- el ong • Brackets represent SO. Note that this difference is virtually zero and is independent of the height of
lesion from C6 to Th11, yet is indistinguishable from normal, and is highly significantly different from zero in
subjects with lesion from Th12 to L5. An intermediate difference is shown by a paraplegic with loss at Th10 on
one side and Th12 on the other side, indicated by hemicircles.
296 H. Mittelstaedt

• board y=1,02x+O.34
o centrifuge --- .. -- y=O.75x+2.98
20

.'.,'
e,d short[cm]

~
10

•
0

-10
Te-paraplegics

o
-20 o
o
-30

-40

-50 V
-50 -40 -30 -20 -10 o
e,d 1o n 9 [cm]

10 20
Figure 13. SHP of subjects with complete paraplegia at Th11 to C6 (TC-paraplegics). All conditions and sym-
bols as in Figure 11. Note that 1) the differences eshort - elong are virtually zero, but 2) the d-values are still far
from the e-values, the dshort-values are larger than the dlong-values, and the slope of their LSD is less than that of
the normals. The first indicates the loss of a somatic graviceptive input entering the cord at Th11, the second
the existence of a second input entering the cord or the brain cranial of CG.

only a t1uid distributed throughout the body
could possibly produce it. I presumed that this
t1uid is the blood in the large vessels, and that
its mass exerts inertial forces on the ligaments
that support the vessels against the gravitational
load. When the legs are t1exed, the mass cen-
troid of the large vessels, necessarily, is shifted
craniad, and so is the centrifuge axis in TC-
paraplegics. But on the board, the force exerted
by the mass of the blood is independent of the
location of the centroid. Hence, leg flexion
should have no effect. As in the case of the kid-
neys, the prerequisites for graviception are
given: a density difference between the blood
and the surrounding medium, and mechanore-
ceptors of the required type m the ligaments
(16,17).
Crucial Tests of Vascular Graviception
Positive pressure to the legs (PPL). The pre-
sumed vascular graviception may be crucially
tested by shifting blood from the legs into the
trunk by means of an antishock suit that applies
positive air pressure of 45 mm Hg exclusively
to the legs (the procedure is named PPL). On
the centrifuge, the resulting shift of the mass
centroid should cause a shift of the centrifuge
axis towards the binaural axis. And, indeed, this
Spatial Perception and Control 297

• board ......... y=1 .01 x-0.07

o centrifuge ------- y=0.82x-1.43
20
e,ds ho rt [cm]

~
10
nephrectomized subjects

0
o
-10

o
-20

-30

-40

-50

-60~----~----~----~--~----~-----+----~--~

-60 - 5 0 -40 - 30 -20 -10 o 10 20

Figure 14. SHP of bilaterally nephrectomized subjects. Conditions and symbols as in Figure 11. Note that, as in
TC-paraplegics, leg flexion has no effect on the tiltable board, and the slopes of the LSD's are similar to those of
Figure 13, yet distinctly different from those of the normal subjects (compare Figure 11).

happens (Figure 15). But on the board, PPL,
just as leg flexion, should have no effect. This is
actually found in subjects who orient them-
selves accurately under normal pressure. How-
ever, as shown in Figure 15, whereas the inter-
cept of the LSD leads virtually througb the
origin, its slope is larger than unity, that is, de-
viations from e = 0 present at norma] pressure
are an1plified about 1.4 times by PPL. Rather
than due to an amplification of the bias, this
may be due to a reduction of the relative weight
of the vascular graviceptors, possibly caused by
a reduction of the force exerted by the blood's
mass, for PPL leads to outward filtration, and
this, in turn, reduces the relevant blood volume.
But a central nervous attenuation of the relative
weight is a possible (inclusive or exclusive) al-
ternative explanation. At any rate, the results
are well in agreement with the hypothesis that
the gravitational load on the large blood vessels
is used in graviception.
V\1 e should expect then, that negative pres-
sure to the 0;' to the entire lower
body (LBNP) elicits sensations of tilt in most
subjects. Astoundingly, in the numerous inves-
tigations under application of LBNP and NPL,
such experiences appear to have been noticed
and published only twice. In an experimental
study from 1971 (18), they are qualitatively de-
scribed, but not measured. A comprehensive re-
view (19; see page 578) relates, without citing
the source, that sensations of tilt have been re-
ported by some subjects under LBNP in a su-
pine posture. Therefore, it appears necessary as
298 H. Mittelstaedt

• board ......... y=1.35x-O.70

o centrifuge ------- y=O.82x+1.67

20
e,d pressu re[cm]
,. "
10

t subjects under leg pressure

o +-------------------------------~~..-----------
x=y

-10

o
:
-20

-40

e,dcontrol[cm]
-50~----~----~----~------~----+-----'-----~

-50 -40 - 30 -20 -10 o 10 20

Figure 15.. SHP of normal subjects, legs extended, under positive air pressure to the legs (PPL) of 45 mm Hg.
The control values under normal pressure (e,dcontrol) are plotted on the abscissa, the respective values with
pressure (e,dpressure) on the ordinate. Note that the result resembles that of the TC paraplegics (compare Figure
13), except that the slope of the LSD of the e-values is larger than unity.

well as promising to test the SHP under nega-
tive and positive pressure to the entire lower
body (LBNP and LBPP, respectively).
Pressure to the lower body (LBPPINP). This
project2 is not yet finished, but the effect of con-
stant LBPP and LBNP of 30 mm Hg on the SHP
is strong and significant, although, especially on
the tiltable board, the correlations are consider-
ably smaller and the variances greater than un-
der PPL (Figures 16 and 17): On the centrifuge
the slope of the LSD under LBPP is smaller
2This project has been planned and executed with the
collaboration of Dieter Vaitl and Friedhelm Baisch and
supported by the Deutsche Forschungsgemeinschaft.
than unity, namely, 0.85, hence virtually identi-
cal to that under PPL seen above; also, under
LBNP, it is not significantly different from that
seen under positive pressure. On the tiltable
board, the slope of the LSD is larger than unity
under LBPP, just as under PPL, and likewise,
albeit still somewhat larger, under LBNP. Thus,
not only positive but also negative pressure ap-
pears to reduce the relative weight of these
graviceptors. So far, the result not only con-
firms the above hypothesis, but also constrains
its specification.
However, to our surprise, the LSD does not
pass through the origin, but is shifted by a large
positive or negative amount, respectively, that
is, the e-values show a pressure-dependent bias,
even in subjects who oriented themselves hori-
:$patial Perception and Control 299

o o o o o
-5 0
o 5 10 15 20
3 0 -,---L...----+_ _ _--L-_ _ _ L-.._~---L---..L..,

,, Co
c:
w'"
c..
, 20 0 e;J
I

20
I

o
10

o
5

0
-r-------.~--+_~~------~--~----------~----------+_ 0

0
-5
n=21 II

-1 0 •
0
e pp } normal
e np
Ss

ep p =1.46*e zp 1 +6.37
enp =1.67*ezp2 -10,91

e z p 1 ,e z p 2

- 1 0 - 5 o 5 10 1 5 2 0 2 5

e pp}
en p
Nephrec. Ss •o :p p}
np
Lab.def.S

Figure 16. SHP on the tiltable board of normal, nephrectomized and labyrinthine-defective subjects under con-
stant positive (filled symbols) or negative (open symbols) pressure to the lower body (±30 mm Hg). The e-val-
ues under experimental pressure (epp , enp , respectively) are plotted over the e-values under normal pressure
(ezp 1, ezp 2, respectively) measured in a control series preceding each experimental series. Dotted and dash-dot-
ted lines represent LSD.

zontally under normal pressure (Figure 16). A mean total effect of the pressure difference on
similar bias appears also on the centrifuge (Fig- the board (e pp - e np ) is quantitatively similar to
ure 17). If both have a common cause they that on the centrifuge (dpp - dnp ), its individual
should be strongly correlated. Yet, although the value is not correlated to the latter's in our 21
300 H. Mittelstaedt

Co
2 0 c
"0
C-
o.
"0

1 0

o ~----------------------------~r---r-=-~----*---~-------------
/

- 1 0

- 2 0

/
- 3 0

d zp1 ,d ZP2
-5 O~~ro-r-r~~-r'-~-.-r.-.,-r~.-~-r.-~-r~.-~-r~~

- 5 0 - 4 0 - 3 0 - 2 0 - 1 0 o 1 0 2 0

dpp =O.8S*d zp1 +S.91

dn p =O.97*d zP2 -S.83

Figure 17. SHP on the centrifuge of the normal subjects of Figure 16 under the same protocol as there, exe-
cuted after a respite period on the same day, and plotted with the same outlay as there.

subjects. And this means, presumably, that still
other graviceptive inputs exist that are affected
by pressure to the abdomen and that act differ-
ently on board and centrifuge.
Two possible sources corne to mind: the hy-
drostatics of the blood and the mass of the entire
abdominal viscera. The latter has recently been
suggested by von Gierke and Parker (20), who
have also shown that its dynamic properties are
apt to entail interesting consequences for the
generation of motion sickness.
However that may turn out to be, the results
under altered air pressure show a strong influ-
ence of the inertia, the distribution, and possibly
also the hydrostatics of the blood on somatic
graviception. Thus, the well-known fact that
Spatial Perception and Control
posture affects the vascular system is comple-
mented by its reverse, namely, that the vascular
system, via perception and control, affects pos-
ture too.
Counterintuitive Insights and
Open Questions
The Visual and the Postural Vertical
In man the vertical is the quintessential ex-
trinsic reference for perception and action. Even
if its measurement, computation, and represen-
tation is based on many different sensory cues
and central nervous processes, all measure-
ments should be averaged to yield a single end
result for all modalities of perception, and this
is implicitly or explicitly assumed in the tradi-
tion. It turns out, however, that the visual and
the postural vertical are based on separate com-
putations leading to separate end results. Both
are sub served by the otoliths, but the visual ver-
tical is also largely affected by a tendency to
align with the z-axis (due to the idiotropic vec-
tor; compare reference 21), but not (or only
marginally and even inversely) by the somatic
graviceptors (compare reference 13); whereas
the postural vertical is also largely influenced
by the somatic graviceptors (compare refer-
ences 22 and 23 and above), but not by the idio-
tropic vector (compare reference 21). Except in
special cases, for example, at or near the upright
posture, the resulting directions differ, often by
large amounts.
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