A case of illusory own-body perceptions after transcranial magnetic stimulation of the cerebellum.

Abstract

Illusory own-body perceptions are 'body in space' misinterpretations of the brain and belong to the class of out-of-body experiences wherein the angular gyrus seems importantly implicated. In the present study additional cerebellum involvement in illusory own-body perceptions was investigated in a healthy young female right-handed volunteer. Transcranial magnetic stimulation (TMS) was applied over the cerebellum. Placebo cerebellum TMS and occipital TMS served as control conditions. Illusory own-body perceptions accompanied by electric brain activity over the somatosensory cortex were only observed after cerebellum TMS. The data provide the first evidence that the cerebellum might be involved in a neuronal network underlying illusory own-body perceptions.

Full text

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A case of illusory own-body perceptions after transcranial magnetic
stimulation of the cerebellum
DENNIS J. L. G. SCHUTTER, MARJOLEIN P. M. KAMMERS, DORIEN ENTER &
JACK VAN HONK
Experimental Psychology, Helmholtz Research Institute, Utrecht University, Utrecht, The Netherlands
Abstract
Illusory own-body perceptions are ‘body in space’ misinterpretations of the brain and belong to the class of out-of-body
experiences wherein the angular gyrus seems importantly implicated. In the present study additional cerebellum
involvement in illusory own-body perceptions was investigated in a healthy young female right-handed volunteer.
Transcranial magnetic stimulation (TMS) was applied over the cerebellum. Placebo cerebellum TMS and occipital TMS
served as control conditions. Illusory own-body perceptions accompanied by electric brain activity over the somatosensory
cortex were only observed after cerebellum TMS. The data provide the first evidence that the cerebellum might be involved
in a neuronal network underlying illusory own-body perceptions.
Key words: Cerebellum, illusory own-body perceptions, transcranial magnetic stimulation
Introduction
Out-of-body experiences (OBEs) have been consid-
ered as supernatural phenomena wherein the mind
detaches itself from the body. Illusory own-body
perceptions are ‘body in space’ misinterpretations of
the brain belonging to the class of OBEs wherein the
angular gyrus seems to be implicated (1–3). Here,
we report illusoryown-body
increased EEG activity in the vicinity of the angular
gyrus in a healthy young woman after transcranial
magnetic stimulation (TMS) over the cerebellum.
Illusory own-body perceptions are often peculiar and
short-lasting sensations that include reports on body
levitation, feeling of lightness and experiences of
falling. In recent years evidence has been accumulat-
ing that the occurrence of illusory own-body
perceptions has a neurophysiological rather than
supernatural origin (1,2). Interestingly, illusory own-
body perceptions were observed in an epileptic
patient after electric stimulation of the angular gyrus
(2). The angular gyrus is located near the vestibular
cortex, a brain structure concerned with the repre-
sentation of body orientation. Illusory own-body
perceptions are argued to result from a temporal
dissociation in the processing of somatosensory and
vestibular information. This assumption has found
support from recent functional neuroanatomical
studies. Interestingly, a brain structure located in
perceptionsand
the posterior parts of the head, contains somatoto-
pical organized nuclei of the body and is directly
involved in the processing of vestibular information
is the cerebellum (4,5). Correlational evidence for
a cerebellum-illusory perception relationship was
recently provided by a functional neuroimaging
study that showed cerebellar activity during the
illusion of touching one’s own hand (6). A technique
that may be able to address this issue more directly is
repetitive TMS (rTMS), a method that can tran-
siently interfere and disrupt neuronal processing
through Faraday’s principle of electromagnetic
induction. Thus, if illusory own-body perceptions
depend on distortions in brain regions related to the
processing of somatosensory input, vestibular and
temporal information, then the cerebellum might be
involved.
Method
Participant
A healthy young right-handed female volunteer, 21
years of age, participated. The subject had no history
of neurological or psychiatric conditions, was non-
smoking, used oral contraceptives, and had more
than 12 years of education. Standard safety-screen-
ing procedure did not yield contra-indications for
TMS (7). She was instructed to refrain from using
Correspondence: Dennis J. L. G. Schutter, Experimental Psychology, Helmholtz Research Institute, Utrecht University, Heidelberglaan 2, 3584CS Utrecht,
The Netherlands. E-mail: d.schutter@fss.uu.nl
(Received 9 March 2006; accepted 28 March 2006)
The Cerebellum. 2006; 5: 238–240
ISSN 1473-4222 print/ISSN 1473-4230 online # 2006 Taylor & Francis
DOI: 10.1080/14734220600791469

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psychotropic substances, including alcohol, choco-
late, tea and coffee, two hours before each session.
Informed consent was obtained and the participant
was blind to the aim of the study. The study was
approved by the medical ethical committee of the
Utrecht University and in accordance with the
declaration of Helsinki.
Transcranial magnetic stimulation (TMS)
Repetitive TMS (rTMS) was performed using a
biphasic magnetic brain stimulator (maximum out-
put 2300 A peak/1750 VAC peak) and iron core coil
with a current magnetic induction field of approxi-
mately 2 Tesla (Neotonus Inc., Atlanta). Placebo
rTMS was performed using an identical coil, but
with a metal plate built in directly under the iron-core
(Neotonus Inc., Atlanta). Although the coil mimics
the sound and sensation of real rTMS, the brain is
shielded from actual stimulation, Mean individual
motorthreshold(MT)ofthelefthemispherewas49%
and stimulation intensity was set at 45% maximum
machine output corresponding to 90%MT.
Structural MRI scan and stimulation targets
T1-weighted three-dimensional fast field echo (3D-
FFE) scans with 160 contiguous coronal slices
(TE54.6 msec, TR530 msec,
16161.2 mm3voxels) were acquired on a Philips
NT 1.5T scanner. The stimulation target site of
the cerebellum (Cb) was referenced to the inion (8–
10) and determined one centimeter below the inion.
Control sites included the occiput, located three
centimeters above the inion (Oc), and placebo
rTMS over the Cb region as illustrated in Figure 1.
flip angle530˚,
Electroencephalogram (EEG)
EEG was recorded from 32 scalp locations accord-
ing to the International 10–20 EEG System using
Ag–AgCl-tipped electrodes (sampling rate: 256 Hz).
Electro-oculogram (EOG) was recorded from a
bipolar montage from the sub- and supra-orbital
regions of the right eye and the outer canthi of the
eyes. Raw EEG recordings were made with the
ActiveTwo system (BioSemi, Amsterdam, The
Netherlands) relative to the common mode sense
(CMS). Raw EEG signals were referenced to the
vertex (Cz) electrode, chunked into 4-s epochs and
corrected for horizontal and vertical eye movements
using the Gratton & Coles method (BrainVision,
Munich). EEG epochs containing residual muscle
movements and other artifacts resulting in ampli-
tudes greater than +/2 50 mV were rejected prior to
further analysis. The designation of an artifact in one
of the leads resulted in removal of that epoch for all
channels in order to ensure that the remaining data
were identical for all sites in time. Chunks of
averaged artifact-free EEG were filtered by applying
a band-pass of 1–30 Hz (24 dB/octave) and a fast
Fouriertransformmethod
length: 10%) was applied to obtain estimates of
spectral power (mV^2) in the alpha (8–13 Hz)
frequency band.
(Hamming window
Procedure
In a randomly assigned counterbalanced order the
subject received 20 min of cerebellum, occipital and
placebo 1-Hz rTMS (1200 pulses p/session) on
three consecutive days. After rTMS the participant
was seated in a dentist chair in a darkened room for
4 min and was instructed to relax. During the 4 min
resting state period, the EEG was registered con-
tinuously. Stimulation parameters are in accordance
with the safety guidelines of the International
Federation of Clinical Neurophysiology (www.ifcn.
info). To prevent priming effects, the experimenter
simply asked the participant after completion of the
third session if she had felt or noticed anything
during the 4 min relaxation period in either of the
three sessions.
Figure 1. Upper panel: Midsagittal view depicting the target
positions areas for slow inhibitory repetitive transcranial
magnetic stimulation (TMS). TMS was performed using a
biphasic magnetic brain stimulator (maximum output 2300 A
peak/1750 VAC peak) and highly focal iron core figure of eight-
coil with a current magnetic induction field of approximately
2 Tesla (Neotonus Inc., Atlanta). Placebo TMS was performed
over the cerebellum target site using an identical coil, but with a
metal plate built in directly under the iron-core (Neotonus Inc.,
Atlanta). Although the coil mimics the sound and sensation of
real TMS, the brain is shielded from actual stimulation. Lower
panel: Topographical maps (top view) showing increased
parieto-temporal EEG activity in the alpha frequency range (a:
8–13 Hz) during illusory own body perceptions after 1-Hz
rTMS over the cerebellum. Cb: cerebellum; Oc: occiput.
Illusory own-body perceptions after TMS
239

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Results
Although blind to stimulation condition and aim of
the study the participant reported that after cere-
bellum rTMS there were several occasions during
the 4 min relaxation period in which she experienced
her body falling/drifting side wards and even out of
the chair, while the experimenter in the adjacent
room verified that she was sitting motionless.
Furthermore, the illusory body perceptions went
accompanied by physiological activity in the vicinity
of the angular gyrus as indexed by the electroence-
phalogram. Theparticipant
experiences were absent after occipital and placebo
rTMS, and in concordance no significant physiolo-
gical activity in the vicinity of the angular gyrus was
observed (Figure 1).
reportedno such
Discussion
The current results indicate that together with the
angular gyrus and vestibular cortex (1–3), the
cerebellum is directly implicated in a neural net-
work underlying illusory own-body perceptions.
Under regular conditions this network processes
information considering body orientation in three-
dimensional space, but when the circuit malfunc-
tions illusory own body perceptions can be triggered.
Interestingly, clinical research has provided some
support for the hypothesis that cerebellar dysfunc-
tion may be involved in psychotic symptoms,
subjective states wherein the external and internal
representations of one-self in the world become
disintegrated (11,12).
Alternatively, the cerebellum and in particular the
caudal vermis that is comprised of the uvula (IX)
and nodulus (X) are known subdivisions to receive
afferent otolith input. Several studies have recently
provided insights into cerebellar processing of
otolith information, showing involvement in inertial
motion detection and spatial orientation (13,14).
Disturbancesofotolith
within the vestibulocerebellum may explain the
present observations.
It should be mentioned that presently the method
for coil positioning was not optimal. However apart
from an anatomical scan to verify location of the
target region, the occipital rTMS condition was
included to dissociate cerebellar from cortical effects.
The possibility that in addition to the cerebellum
peripheral nerves were stimulated as well cannot be
completely ruled out. Furthermore, clinical TMS
trials have evidenced that the occurrence of phenom-
enological effects to TMS depend at least partially on
the individual neurophysiological state (15), thus
more objective behavioural assessments would be a
valuable addition to capture more subtle disturbances
in own-body perceptions across subjects (16).
To our knowledge, the current data provide the
firstelectrophysiological
informationprocessing
and phenomenological
evidence for cerebellar involvement in a neuronal
network underlying illusory own-body perceptions,
and legitimize further research to test the tenability
of this observation.
Acknowledgement
Dr D. J. L. G. Schutter was supported by an
Innovational Research Grant (# 451-04-070) and
Dr J. van Honk was supported by an Innovational
Research Grant (# 016-005-060) from the
Netherlands Organization for Scientific Research
(NWO).
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