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\begin{document}

\title{Influence of Vestibular Disorders on Tilt Perception and Short Term
Memory}



\author[1]{Atsushi Ochiai}%
\author[2]{Kimitaka Kaga}%
\affil[1]{Kitasato University School of Medicine}%
\affil[2]{National Hospital Organisation Tokyo Medical Center}%


\vspace{-1em}



  
  \date{May 18, 2024}


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\selectlanguage{english}
\begin{abstract}
Introduction: Spatial orientation refers to the fact that the brain
integratively recognizes its own position, posture and motion in space
through several sensory systems. Vestibular, visual and somatosensory
inputs with various motion are constantly integrated in central nervous
system to determine the spatial orientation. Among the various
parameters of spatial orientation, there has been no study about tilt
perception and the memory of tilt perception. Methods: The following
subjects participated in these experiments; normal volunteers under 65
years of age (Control group) and bilateral no response to the Caloric
test (Bilateral group). Procedure was measurement of the short term
memory of tilt perception that were reproduction of 0\selectlanguage{ngerman}°and reproduction
of right by 5°and left by 5°with improved electric goniometer. Results:
Control group: There were no significant differences in the time course,
or right and left direction of tilt for any of the age groups. Bilateral
group: There were no significant differences in any of the tasks in the
procedures between the control group and the bilateral group.
Conclusion: Although tilt perception is formed from the vestibular and
somatosensory input, it became clear that the vestibular are less
important than the somatosensory input, because the bilateral group
could also successfully remember tilt positions. It also is clear that
such information is remembered for at least a short period of time.%
\end{abstract}\selectlanguage{ngerman}%



\sloppy


\textbf{1 INTRODUCTION}

Spatial orientation refers to the fact that the brain integratively
recognizes its own position, posture and motion in space through several
sensory systems. Vestibular, visual and somatosensory inputs with
various motion are constantly integrated in central nervous system to
determine the spatial orientation.\textsuperscript{1}

Among the various parameters of spatial orientation, the measurement of
tilt perception for gravity was first done by Grahe in 1922, when he
measured the vertical position with a measuring
apparatus.\textsuperscript{2} He first tilted it manually and returned
the subject to the vertical position gradually. He made volunteers with
their eyes closed make a sign at the moment they accurately perceived
the vertical position. The results were from 2\selectlanguage{ngerman}\textsuperscript{°} to
3\textsuperscript{°}, thus indicating that they perceived it very
accurately.

Later, Israel et al had volunteers sit inside an opaque fiberglass
sphere.\textsuperscript{3,4} The sphere was mounted within two
motor-driven rings. The subjects were secured onto the chair with three
belts, and their head was fixed with a helmet to keep them in the same
position. The chair position was adjusted so that the head was at the
centre of rotation. Two push-buttons were fixed on the right side of the
chair, with which the subjects could control the position of the sphere.
The subjects were first required to position their body at an angle of
90\textsuperscript{°}, 180\textsuperscript{°} or 360\textsuperscript{°},
right or left, with the push-buttons, and then to rotate back to the
initial position after 3-6 s. The results were as follows; the mean
rotation from 0\textsuperscript{°}\selectlanguage{english}- 90\textsuperscript{deg} was
93.2\textsuperscript{deg}, for 0\textsuperscript{deg}\selectlanguage{english}-
180\textsuperscript{deg} was 169\textsuperscript{deg}, 0\textsuperscript{deg}\selectlanguage{english}-
360\textsuperscript{deg} was 313\textsuperscript{deg},
90\textsuperscript{deg}\selectlanguage{english}- 0\textsuperscript{deg} was 92.6\textsuperscript{deg},
180\textsuperscript{deg}\selectlanguage{english}- 0\textsuperscript{deg} was
157\textsuperscript{deg}and 360\textsuperscript{deg}\selectlanguage{english}-
0\textsuperscript{deg}was 293\textsuperscript{deg}. These results confirmed
that subjects accurately perceived their vertical position.

However, both of these previous studies were presented by analogue
displays.

Berthoz et al studied the memory of body linear
displacement.\textsuperscript{5} Volunteers were seated on a robot,
their head was fixed in place, and their eyes were covered. After
undergoing a displacement of 2, 4, 6, 8, or 10 m, they reproduced, as
accurately as possible, the distance that was imposed. Even when the
stimulus acceleration (range 0.06 to 1 m/s\textsuperscript{2}) was
changed or the stimulus duration was kept constant (16 s) over the
different distances, they could reproduce the distance very accurately.

Although these studies indicate the remarkable ability of the body for
special awareness, there has been no study about tilt perception and the
memory of tilt perception. We hypothesized that patients who have
vestibular dysfunction, especially bilateral vestibular dysfunction with
the Jumbling phenomenon, would have disorders in tilt perception and
memory.

Therefore, we developed an electric goniometer that enabled digital
display of the tilt angle for easy analysis of the results and we
studied the influence of vestibular disorders on the tilt perception and
short term memory of tilt perception in normal volunteers and patients
with no bilateral response to the caloric test.

\textbf{2 SUBJECTS AND METHODS}

\textbf{2.1 Subjects}

The following subjects participated in these experiments.

Normal volunteers under 65 years of age (control group)

N= 50, age: 21- 42 years, average age: 29 years, standard deviation
(SD): 5 years, and age distribution: second decade: 20, third decade:
22, fourth decade: 8. The definition of normal volunteers was that they
had no vertigo or past history of neurological disease.

Bilateral no response to the Caloric test (bilateral group)

N= 20, age: 18- 75 years, average age: 51 years, SD: 17 years, and age
distribution: first decade: 3, third decade: 4, fourth decade: 3, fifth
decade: 4, sixth decade: 3, seventh decade: 3. The details of the
underlying diseases in the 20 patients are as follows: idiopathic: 8,
meningitis: 5, neurofibromatosis type 2 (NF2): 4, auditory nerve
disease\textsuperscript{6}: 2 and syphilitic labyrinthitis: 1. The
Caloric test used irrigated cold water (4\selectlanguage{english}, 2 ml) for 20 seconds.

\textbf{2.2 Methods}

For this study, we improved the electric goniometer (NAGASHIMA MEDICAL
INSTRUMENTS co., Ltd.) so that we did not monitor any other position
(for example, up-and-down of the center of gravity) except for tilt
stimulation, and that the movement could be stopped with a joy-stick
immediately when volunteers perceived a level of tilt. We were also able
to measure the tilt angle from the standard level with a digital display
of the tilt angle.

There is a direct-current motor behind the tilt bedplate. This motor
connects a right and left changeover switch of the tilt direction, and
has a potentiometer that displays the angle and enables measurement to
0.1\textsuperscript{deg}.

It is possible to tilt the subject to a maximum of
20\textsuperscript{deg}on both sides, and to change the angular velocity.
This enabled us to maintain the experimental conditions better than the
past manual studies and allowed for easy and objective measurement, in
contrast to the past studies because of the digital display of the tilt
angle.\textsuperscript{2-4}

We studied the tilt perception and very short term memory of the tilt in
normal volunteers in standing and sitting positions as a pilot study. We
found that the sitting position to be more difficult than the standing
position. Therefore, we decided to study the patients in a sitting
position, and set up the chair on the tilt bedplate of the electric
goniometer (Figure 1). We made volunteers sit in the chair without
leaning against the backrest. We covered their eyes with goggles to
remove the visual input and used an instrument fixed to the trunk, and
fixed their head in place with ear pads attached to the chair. Patients
were also required to take off their shoes and float both of their legs
(Figure 2). We regulated the angular velocity of the tilt at
1\textsuperscript{deg}/sec.

\textbf{2.3 Experiment}

Procedure: Measurement of the short term memory of tilt perception
(Figure 2)

Reproduction of 0\textsuperscript{deg}

First, we ordered subjects to memorize their perception of
0\textsuperscript{deg} for 1 minute. We then tilted the subjects to the
right by 5\textsuperscript{deg} (R 5\textsuperscript{deg}) and asked them to
evaluate this position for 1 minute. Finally, we had them reproduce the
initial perception of 0\textsuperscript{deg} immediately, or 1, 3, 5 and
10 minutes later. We recorded tilt angle of their reported position. We
also studied the left condition (L 5\textsuperscript{deg}) in the same
manner.

Reproduction of R and L 5\textsuperscript{deg}

First we tilted the subjects to R 5\textsuperscript{deg} and asked them to
memorise the position of R 5\textsuperscript{deg} for 1 minute. We then
returned the subjects to 0\textsuperscript{deg} and asked them to accustom
themselves to this position for 1 minute. Finally, we asked the subjects
to reproduce the initial R 5\textsuperscript{deg} immediately, or 1, 3, 5
and 10 minutes later. We recorded tilt angle of their reported position.
We also studied the left condition (L 5\textsuperscript{deg}) in the same
manner.

\textbf{2.4 Statistical analysis}

With regard to the statistical analysis of the results, we performed an
analysis of variation (ANOVA) between each of the groups, for the time
course between each group, for the right and left directions of tilt
between the same group and for differences in age between each of the
groups. When a significant difference was observed, we added a t- test.

\textbf{3 RESULTS}

The results are shown in Table 1 and Figure 3, 4.

1. Control group

There were no significant differences in the time course, or right and
left direction of tilt for any of the age groups.

2. Bilateral group

There were no significant differences in any of the tasks in the
procedures between the control group and the bilateral group. There were
also no significant differences in the time course, right and left

direction of tilt or ages between the groups.

Furthermore, there were also no differences between the patients with (5
patients) and without (15 patients) Jumbling phenomenon.

\textbf{4 DISCUSSION}

The spatial orientation is formed from the vestibular, visual and
somatosensory inputs as mentioned above.\textsuperscript{1} In this
study, we covered the patients' eyes with goggles to remove the visual
input. Therefore, all of the patients had to rely on their vestibular
and somatosensory inputs when they tried to reproduce
0\textsuperscript{deg}, and right and left 5\textsuperscript{deg}in this
study.

There were no significant differences in any of the tasks during the
procedure between the bilateral group and the control group. There were
also no differences in the right and left direction of tilt within each
of the groups. The bilateral group do not receive vestibular input. But
there were no differences. Therefore, the somatosensory input is
sufficient to provide information about the spatial orientation.
Fitzpatrick et al and Horak et al reported that the contribution from
visual and somatosensory inputs are the most important, and that the
vestibular input is primarily used for balance control of normal
humans.\textsuperscript{7,8} Bronstein et al. reported that patients
with bilateral vestibular disorders are ``visually dependent'' soon
after the vestibular insult, but that they gradually learn to ignore
conflicting visual stimuli as compensation
develops.\textsuperscript{1}Nashner et al, Bles et al, and Peterka et al
reported that somatosensory input increases for balance control in
patients with bilateral vestibular disorders.\textsuperscript{9-12}
Nandapalan et al used the Sway Weigh balance platform to determine the
efficacy of a walking stick in 25 patients with peripheral vestibular
balance disorders.\textsuperscript{13} In their study, the patients were
tested with their eyes open and closed while they were standing on a
flat surface and on an air-filled bed (to alter limb proprioception) on
the Sway Weigh balance platform. All the tests were carried out with and
without a walking stick. They found that body sway decreased when the
subjects used a walking stick when they were standing on an air-filled
bed with their eyes either opened or closed, although there were no
differences with or, without the walking stick when they were standing
on a flat surface.

We suppose that humans form spatial orientation by effectively using
remaining information and control their balance according to this
information. Judging from these reports, and the tilt perception in this
study, it appears that while the contribution of vestibular input is
important, somatosensory input is more important (the source of
somatosensory input was the hip, because we studied subjects under the
condition that they had to sit in their chair without leaning against a
backrest).

Although the Jumbling phenomenon is able to occur when bilateral
vestibular function is disordered, there were no significant differences
between patients with and without it. There were also no differences
when we covered subjects' eyes with goggles to remove the visual input.
Therefore, we concluded that the somatosensory input is more important
than the other types of input.

Furthermore, we also tested a patient with multiple sclerosis (MS) who
had disequilibrium and dysbasia due to anesthesia of the hip and
bilateral lower legs and a lesion with contrastable effect in the spinal
cord under Th4 magnetic resonance imaging (MRI). The result was that the
patient was unable to correctly perceive a tilt over the mean tilt angle
+- 2 SD of control group in most of the task in the procedure (Table 1,
Figure 3, 4). The importance of somatosensory input was further
supported by this result.

Although we studied tilt perception immediately, and 1, 3, 5 and 10
minutes after changing positions in order to study the memory of tilt
perception, there were no significant differences in the both groups.

There have been reports showing that the hippocampus is involved in
memory and recognition of space by experiments on the rat
hippocampus.\textsuperscript{14, 15} Furthermore, it has been known that
there are neurons involved in movement and memory of space in the monkey
hippocampus.\textsuperscript{16, 17} In addition, there is a neuron
group which fires to synchronize a rat's movement that was demonstrating
by simultaneously recording freely moving rats' hippocampus, including
nearly a hundred neurons. These neuron groups react to differences in
position, and they are distributed like a belt in the
hippocampus.\textsuperscript{18} Based on these reports, it appears that
the information processing in the hippocampus facilitates memorization
of space and position, via groupable and cooperative neurons, and
dynamic change of many neuron circuits are likely involved in the memory
of space and position with action.

With regard to the spatial orientation and posture control, groupable
and

cooperative information processing of many neural circuits including the

hippocampus, vestibules, visual system, somatosensory system,
cerebellum,

limbic system and so on are done unconsciously. It is suspected that
many

cooperatively and functionally connected neuron circuits dynamically
change in

response to input of information for that purpose.

There were no abnormalities in tilt perception in the control and
bilateral

groups in the present study, because the vestibular and somatosensory
input

that are necessary to integrate spatial orientation function adequately.

Therefore, it is suspected that groupable and cooperative information

processing of the above-mentioned neuron circuits, as well as the

hippocampus-related memory of tilt perception, can be maintained for at
least

10 minutes.

\textbf{5 CONCLUSION}

Although tilt perception is formed from the vestibular and somatosensory
input, it became clear that the vestibules are less important than the
somatosensory input, because the bilateral group could also successfully
remember tilt positions. It also is clear that such information is
remembered for at least a short period of time, thus allowing for a
return to a normal position.

\textbf{6 ETHICAL CONSIDERATIONS}

This study was carried out in concordance with international ethical
standards and the World Health Organisation Helsinki Declaration. It was
approved by the institutional review board. Informed consent was
obtained from all of the subjects.

\textbf{Key points}

\selectlanguage{english}\textbf{} Tilt perception is formed from the vestibular and
somatosensory input.

\textbf{} \selectlanguage{english}We improved an electric goniometer that enabled digital
display of the tilt angle

for easy analysis of the results to study the tilt perception and short
term memory

of tilt perception.

\textbf{} \selectlanguage{english}It became clear that the vestibules are less important than
the somatosensory

input.

\textbf{} \selectlanguage{english}The bilateral group could also successfully remember tilt
positions.

\textbf{} \selectlanguage{english}It is clear that such information is remembered for at least
a short period of time.

\textbf{CONFLICTS OF INTEREST AND SOURCE OF FUNDING}

There was no financial and material support for this study.

The authors disclose no conflicts of interest.

\textbf{REFERENCES}

1. Bronstein AM, Yardley L, Moore AP, et al. Visually and posturally
mediated

tilt illusion in Parkinson\textsuperscript{'}s disease and in
labyrinthine defective subjects. Neurology 1996; 47: 651-656.

2. Grahe K. Uber Lageempfindungen und reflexe beim Menschen. Zeitschr.
f. Hals-,

Nasen-u. Ohrenheilk 1922; 12: 640-649.

3. Israel I, Fetter M, Koenig E. Vestibular perception of passive whole-
body

rotation about horizontal and vertical axes in humans: goal- directed
vestibulo-

ocular reflex and vestibular memory- contingent saccades. Exp Brain Res
1993;

96: 335-346.

4. Israel I, Sievering D, Koenig E. Self- rotation estimate about the
vertical axis.

Acta Otolaryngol 1995; 115: 3-8.

5. Berthoz A, Israel I, Francois PG, et al. Spatial memory of body
linear displacement: what is being stored? Science 1995; 269: 95-98.

6. Kaga K, Nakamura M, Shinogami M, et al. Auditory nerve disease of
both ears revealed by auditory brainstem responses, electrocochleography
and otoacoustic emissions. Scand Audiol 1996; 26: 233-238.

7. Fitzpatrick R, McCloskey DI. Proprioceptive, visual and vestibular
thresholds for

the perception of sway during standing in humans. J Physiol 1994; 478:
173-186.

8. Horak FB, Shupert CL, Dietz V, et al. Vestibular and somatosensory
contributions

to responses to head and body displacement in stance. Exp Brain Res
1994; 100:

93-106.

9. Nashner LM, Black FO, Wall C 3rd. Adaptation to altered support and
visual

conditions during stance. J Neurosci 1982; 2: 536-544.

10. Bles W, Roos JWP. The tilting room and posturography. Acta
Otorhinolaryngol

Berg 1991; 45: 387-391.

11. Peterka RJ, Benolken MS. Role of somatosensory and vestibular cues
in

attenuating visually induced human postural sway. Exp Brain Res 1995;
105:

101-110.

12. Peterka RJ. Sensorimotor integration in human postural control. J
Neurophysiol 2002; 88: 1097-1118.

13. Nandapalan V, Smith CA, Jones AS, et al. Objective measurement of
the

benefit of walking sticks in peripheral vestibular balance disorders,
using the

sway weigh balance platform. J Laryng Otol 1995; 109: 836-840.

14. Foster TC, Castro CA, McNaughton BL. Spatial selectivity of rat

hippocampal neurons: dependence on preparedness for movement. Science

1989; 244: 1580-1582.

15. Markus EJ, Qin YL, Leonard B, et al. Interaction between location
and task affect the spatial and directional firing of hippocampal
neurons. J Neurosci 1995; 15: 7079-7094.

16. Ono T, Nakamura K, Nishijo H, et al. Monkey hippocampal neurons
related

to spatial and nonspatial cues. J Neurophysiol 1993; 70: 1516-1529.

17. Eifuku S, Nishijo H, Kita T, et al. Neuronal activity in the primate
hippocampal formation during a conditional association task based on the
subject\textsuperscript{'}s location. J Neurosci 1995; 15: 4952-4969.

18. Hampson RE, Simeral JD, Deadwyler SA. Distribution of spatial and
nonspatial

information in dorsal hippocampus. Nature 1999; 402: 610-614.

\textbf{FIGURE LEGENDS}

Figure 1 Our improving electric goniometer.

We set up chair on the tilt bedplate of electric goniometer.

Figure 2 Tilt perception and memory.

We made subjects sit in the chair without leaning against the backrest,
covered

their eyes with goggles, fixed their trunk and head, and made them take
off their

shoes and let both of their legs hang freely from the chair.

Figure 3 Tilt perception and short term memory (R5\selectlanguage{ngerman}°\selectlanguage{english}- 0deg, L5deg\selectlanguage{english}- 0deg)

There were no significant differences in any of the tasks in the
procedures between the control group and the bilateral group.

vertical axis: tilt angle (deg), white bar: Control group, black bar:
Bilateral group, gray bar: MS

Figure 4 Tilt perception and short term memory (0deg\selectlanguage{english}- R5deg, 0deg\selectlanguage{english}- L5deg)

There were no significant differences in any of the tasks in the
procedures between the control group and the bilateral group.

vertical axis: tilt angle (deg), white bar: Control group, black bar:
Bilateral group, gray bar: MS

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