Changes in autonomic and EEG patterns induced by
hypnotic imagination of aversive stimuli in man
Physiology and Biochemistry; and
Electric Systems and Automation, University of Pisa,
[Received 17 January 2000; Accepted 18 February 2000]
ABSTRACT: Autonomic and electroencephalographic (EEG) re-
sponses to aversive stimuli presented by means of hypnotic
suggestion have been studied in man. Healthy volunteers with
simple phobia were screened for susceptibility to hypnosis. The
experimental paradigm included periods of rest during which
the hypnotized subjects were asked to produce an emotionally
neutral mental image and periods of emotional activation in
which they were asked to image a phobic object. Heart rate
(HR), respiratory frequency (RF) and EEG were processed to
obtain the HR-related indexes of sympatho-vagal balance and
the EEG spectral components. The results showed a significant
increase in HR and RF with a shift of the sympatho-vagal in-
dexes towards a sympathetic predominance during the hyp-
notic emotional activation. EEG activity showed a significant
increase in the gamma band with a left fronto-central preva-
lence. There was also a less pronounced increase in the beta
In conclusion, by means of hypnosis, autonomic and
behavioral responses to fear-like stimuli can be induced in man
in a reproducible and controlled manner. Such a paradigm
could be applied in human neuroimaging studies to identify
central nervous structures that modulate stress and fear-re-
© 2000 Elsevier Science Inc.
KEY WORDS: Hypnosis, Emotions, Heart rate, Respiration, Be-
In animals, including humans, the engagement with emotionally
relevant environmental situations is always accompanied by dis-
tinct modifications of autonomic and behavioral variables. These
reactions usually fall into two main categories: one, consistent with
aggressive behavior, is represented by an active type of response to
a fearful stimulus and is characterized by a massive sympathetic
activation and by desynchronization of the electroencephalogram
(EEG); the other is typical of a passive response or withdrawal and
displays an opposite pattern of autonomic and behavioral response
. In general, these emotional reactions have evolved in the
different animal species to produce the optimal behavior to fulfill
basic defensive/offensive requirements or to cope with stressful
situations produced by physical (pain, exercise, postural adjust-
ments, etc.) or purely emotional (fear, anxiety, anger, etc.) stimuli.
The adaptation of the responses to different purposes is assisted by
the coordinated action of several central nervous structures. Ani-
mal studies have indeed shown that fear-related autonomic and
behavioral responses are under the control, besides the hypothal-
amus , of specific forebrain areas, such as the central nucleus
of amygdala [27,35], the medial prefrontal cortex  and specific
cerebellar lobules [29,59,65]. Although specific autonomic and
behavioral responses can be recorded in man when exposed to
noxious or stressful stimuli , very little is known about their
dynamics in controlled situations. Further, the role exerted in man
by these central nervous structures, identified in the animal, in the
integration of stressful stimuli and in the adaptation of these
responses to the environmental context, remains unknown.
Experiments on fear-related behaviours in man can be advan-
tageously performed using hypnosis as a cognitive tool to admin-
ister a complex stimulus to subjects whose attention can be strictly
focussed on the task. In fact, subjects highly susceptible to hyp-
nosis exhibit remarkable attentional and disattentional abilities
; their mental processing is strongly associated with vivid
imagery [16,17,71] and good visuo-spatial skills . They also
exhibit an all-encompassing involvement towards specific atten-
tional objects, which is defined as “absorption” , as well as a
“fantasy proneness” , involving immersion in a private world
of fantasy and vivid daydreaming. Furthermore, expectation of
hypnosis, in susceptible subjects, enhances the vividness of visual
imagery  and a hypnotic induction can improve some of their
cognitive abilities [12,13,40,63]. Hypnosis appears more effective
than simple suggestion in the regulation of some mind– body
relationships, like relaxation, vasomotor and pain control . Due
to the neuro-psychological traits of highly susceptible subjects and
to their possible amplification after a hypnotic induction, hypnosis
can be very useful in allowing subjects to accept complex cogni-
tive aversive stimuli, such as suggestion of fear, so that they can
experience their emotions very deeply and vividly [20,21,74].
It is known that marked changes in autonomic patterns are
present in subjects with a simple phobia when exposed to their
specific phobic object [18,44] and that these individuals display
cognitive capabilities very similar to those found in subjects highly
susceptible to hypnosis . Then, on the basis of the psycholog-
ical traits of phobic and hypnotizable subjects, a paradigm based
* Address for correspondence: Prof. Brunello Ghelarducci, Department of Physiology and Biochemistry, University of Pisa, Via S. Zeno 31, 56127 Pisa,
⫹0039-050-552183; E-mail: firstname.lastname@example.org
Brain Research Bulletin, Vol. 53, No. 1, pp. 105–111, 2000
Copyright © 2000 Elsevier Science Inc.
Printed in the USA. All rights reserved
0361-9230/00/$–see front matter
on the comparison between the autonomic and behavioral re-
sponses obtained during a hypnotic phobic and a neutral hypnotic
suggestion, offers many advantages. In fact, hypnosis allows us to
present a stimulus very similar to the natural one, to control the
cognitive channels involved in the requested imagery and the
duration of the stimulation, to avoid any effect of stimulus expec-
tation and to control both the long-lasting cognitive stimuli and the
baseline conditions. On the basis of the stereotyped reactions
exhibited by phobics  and controlled through hypnosis, the
present experiments were aimed to study the patterns of autonomic
and EEG responses evoked by fearful stimulation and to identify
the best markers to chose proper acquisition times in neuroimaging
MATERIALS AND METHODS
Five right-handed (Edinburgh Handedness Inventory Score
⬎16) volunteers (three females, 2 males, aged 21–30 years),
exhibiting a Diagnostic and Statistical Manual of Mental Disor-
edition  simple phobia, without any other psychiatric,
neurological and medical disorder, were selected. Each volunteer
signed a written consent approved by the local Ethical Committee
(IRCCS, Stella Maris Scientific Foundation, Pisa, Italy) describing
the procedures and the experimental risks and affirming his right to
withdraw from the experiment at any time. Subjects hypnotic
ⱖ10/12) was assessed through the Stanford Hyp-
notic Susceptibility Scale A and C [72,73] individually adminis-
tered. The neuropsychological correlates of hypnotizability related
to our task were tested through the Tellegen Absorption Scale
(TAS; score: 0 –34) , the Visual Vividness Imagery Question-
naire (VVIQ; score: 20 – 80)  and the Differential Attentional
Processes Inventory (DAPQ; score: 36 –252) .
During the experimental sessions, subjects sat in an armchair in
a semi-dark room. Only the hypnotist remained in contact with
them throughout the experiment. Recording instrumentation was
not visible and the room was lined with sound attenuating panels
to reduce the environmental noise. Experimental sessions con-
sisted of six conditions of 5 min each: (1) Quiet wakefulness (eyes
closed, QW); (2) neutral hypnosis (hypnosis without any sugges-
tion except relaxation, NH1); (3) suggestions of a neutral object
(NSH); (4) neutral hypnosis (NH2); (5) suggestions of a phobic
object (ASH); (6) neutral hypnosis (NH3). The neutral (NSH) and
phobic object (ASH) were suggested through the request of a
visual and auditory mental imagery; besides, subjects were told
that “they were clearly aware” of the presence of such objects in
the room. Neutral and phobic stimulation were obviously different
in their emotional valence but they were carefully balanced in
terms of their sensory-motor aspects. All experimental sessions
were carried out between 1500 1900 h. During sessions, EEG,
electroonlogram (EOG), frontalis electromyogram (EMG), elec-
trocardiogram (ECG) and respiratory trace were monitored con-
tinuously. After awakening, subjects underwent a structured inter-
view to collect experiential data. Subjects rated their negative
emotion using a numerical scale of 0 to 10 whose endpoints were
“ no fear-like involvement ” and “extremely intense fear-like
sensation”. To avoid a ceiling effect, subjects were instructed to
rate 5 an intense negative emotion, comparable to that usually
induced by the presence of the real phobic object.
The analysis was focused on the ASH condition and its NSH
control since they are the proper indicators of the methodolog-
ical efficacy of the present approach to the study of the auto-
nomic and behavioral responses described in typical fight or
flight reaction to fear.
ECG and Respiratory Trace Acquisition and Data Analysis
For ECG recording Red Dot™ Ag/AgCl electrodes were used
while the respiratory frequency (RF) was detected through a poly-
meric piezoelectric dc-coupled transducer wrapped around the
chest. Signals were amplified (ECG: gain
⫽ 1 K; RA ⫽ 10 K),
filtered (ECG: low pass
⬍100 Hz and high pass ⬎1 Hz) and
digitized at a 256 Hz.
From the ECG signal a derivative/threshold algorithm provided
the series of RR intervals (tachogram) and heart rate (HR). The
series of consecutive RR intervals were used to provide the power
spectral density using a Fast Fourier Transform (FFT)-based ap-
proach. It was evaluated on 128 beats (about 2 min) consecutive
epochs-length. This always provided two power spectrum values
(“a”, “b”) for each experimental condition (5 min). The duration of
the periodical phenomena in the cardiac signal was measured as a
function of cardiac beats, rather than seconds [49,66].
The respiratory frequency signal was sampled once for every
cardiac cycle, in correspondence with the R wave, thus obtaining
a respirogram synchronized with the tachogram. The two series
(tachogram and synchronized respirogram) are generally used for
further cross-spectral analysis .
Two major oscillatory components are usually detectable in RR
variability, one of which, synchronous with respiration, is de-
scribed as high frequency (HF; about 0.25 Hz and varying with
respiration), whereas the other, corresponding to the slow waves of
arterial pressure, is described as low frequency (LF; about 0.1 Hz).
Areas under the power spectra in LF (0.03– 0.15 Hz) and HF
(0.15– 0.4 Hz) were calculated and used for statistical compari-
sons. The LF and HF oscillatory components were both presented
in normalized units (nu). In addition, the LF-to-HF ratio has been
calculated to provide an indication of the sympatho-vagal balance.
EEG, EOG and EMG Acquisition and Data Analysis
For EEG, EOG and EMG, Ag/AgCl electrodes (d
⫽ 8 mm;
⬍10 K⍀) were used. Monopolar EEG electrodes were
placed bilaterally in frontal (F3–F4), central (C3–C4) and posterior
(O1–O2) scalp regions and referred to an indifferent electrode
(Cz). Signals were amplified (EEG: gain
⫽ 100 K; EOG: gain ⫽
1 K; EMG: gain
⫽ 1 K) and filtered (EEG: low pass ⬍100 Hz and
⬎0.3 Hz; EOG: low pass ⬍30 Hz and high pass ⬎0.3
Hz; EMG: low pass
⬍500 Hz and high pass ⬎1 Hz). The EEG
frequency bands considered were defined as follows: alpha (8 –13
Hz), beta (13–36 Hz) and gamma (36 – 44 Hz).
Digitized signals (sampling rate
⫽ 256 Hz), were divided in 2-s
epochs. Before performing FFT, data have been filtered by means
of a Hanning window. The auto-regressive power spectrum of the
signal has been calculated using a 1-s overlap and it was validated
by comparing collected data with a power spectrum calculated via
EEG periods altered by body and head movement artifacts have
been visually discarded, while the EOG and frontalis EMG arti-
facts have been automatically removed by means of the Indepen-
dent Component Analysis (ICA) .
Because the sample belonged to the same population, two-way
general linear model analysis of variance (ANOVA) has been
applied to normalized data. The descriptive data of HR and RF as
well as the spectral indexes of RR variability relative to the
different experimental conditions were analyzed by means of a two
way ANOVA. The EEG relative power over periods of five epochs
was evaluated and compared across experimental conditions and
GEMIGNANI ET AL.
channels for each frequency band by means of three separate
Post-hoc Bonferroni test has been performed and threshold for
significance has been set at p
All subjects exhibited remarkable imaginative and attentional
abilities as shown by the high scores obtained in the psychological
tests (TAS: 21.6
⫾ 3.9; DAPQ: 140.8 ⫾ 21.6; VVIQ: 61.2 ⫾ 8.3).
At the end of recording sessions, experiential data were collected
through a structured interview assessing that each subject had
experienced a good hypnotic response and had clearly visualized
both the neutral and phobic object. Moreover, it was ascertained
that after the phobic suggestion all subjects had felt an intense
negative emotion (mean score
⫽ 4.8 ⫾ 0.2), comparable to that
usually induced by the presence of the real phobic object.
Heart Rate and Respiratory Frequency
Heart rate was increased during aversive hypnotic stimulation
⫾ 8.4 beats/min) compared to the mean rate during the
baseline experimental conditions (79.0
⫾ 3.5 beats/min) and its
control during neutral hypnotic stimulation (80.2
⫾ 8.7 beats/min).
Respiration frequency also increased during ASH (19.3
resp/min) with respect to the mean frequency during baseline
⫾ 0.8 resp/min) and its NSH control (16.7 ⫾ 3.4
resp/min). To highlight the effect of the experimental conditions
on both HR and RF, data have been normalized. For each subject
the normalization has been obtained by subtracting from the values
of HR and RF in each condition, the mean value across the whole
session and dividing the result by the standard deviation .
These deviations are shown in Fig. 1.
For HR normalized values, ANOVA yielded a significant dif-
ference among conditions (F(5,20)
⫽ 13.33; p ⬍ 0.001) with ASH
different from all the other conditions as indicated by post-hoc test.
RF normalized values exhibited a similar pattern except for a slight
increase during NSH. When compared across experimental con-
ditions, the values were significantly different [F(5,20)
⬍ 9.001] and post-hoc test showed that in ASH they were
significantly higher than in the other conditions.
Power Spectrum Analysis of RR Variability
Figures 2A and B show the mean power of the LF and HF
components of the heart period variability in relation to the exper-
As can be noted in Fig. 2A, the LF component reached its
maximum in the second part of ASH (70.6
⫾ 3.5 nu) and in the
first part of NH3 (77.4
⫾ 7.9 nu). A similar behavior, although less
pronounced, could be observed during the second part of NSH
⫾ 4.7 nu). LF data calculated among conditions were sig-
nificantly different [F(11,44)
⫽ 4.45, p ⬍ 0.001]. Post-hoc test
revealed that both the first part of NH3 and the second part of ASH
were different from NH1 (43.3
⫾ 5.6; 46.1 ⫾ 8.7 nu) and NH2
⫾ 6.6; 48.2 ⫾ 4.7 nu)
The HF component depicted in Fig. 2B changed in a reciprocal
manner compared to LF, with the lowest values in the second part
FIG. 1. Heart rate (HR) and respiratory frequency (RF). The effects of each
experimental condition on HR (black bars) and RF (white bars), are shown
as deviations of the mean normalized values (mean
⫾ SEM) from the mean
across the whole session (zero line). Abbreviations: ASH, suggestion of a
phobic object; NH1, neutral hypnosis (hypnosis without any suggestion
except relaxation; NH2, neutral hypnosis; NH3, neutral hypnosis; NSH,
suggestion of a neutral ojbect; QW, quiet wakefulness (eyes closed).
FIG. 2. Spectral analysis of RR interval variability. For all the experimental
conditions the low frequency (LF) and high frequency (HF) components
and the LF-to HF ratio are shown in (A), (B), and (C), respectively. For
each condition, two consecutive spectral index values (a,b) are given (see
Materials and Methods). Abbreviations: ASH, suggestion of a phobic
object; NH1, neutral hypnosis (hypnosis without any suggestion except
relaxation; NH2, neutral hypnosis; NH3, neutral hypnosis; NSH, sugges-
tion of a neutral object; QW, quiet wakefulness (eyes closed).
AUTONOMIC RESPONSES, BEHAVIOR AND EMOTIONS
of ASH (27.4
⫾ 3.7 nu) and in the first part of NH3 (21.5 ⫾ 7.8
nu). Again, ANOVA showed a significant difference among con-
⫽ 4.27 p ⬍ 0.001] and post-hoc test indicated
that the first part of NH3 and the second part of ASH were
significantly different from NH1 (54.6
⫾ 5.8; 51.9 ⫾ 9.0 nu), the
second part of NH2 (49.0
⫾ 4.9 nu) and the first part of both NSH
⫾ 7.0 nu) and ASH (55.1 ⫾ 5.9 nu).
Figure 2C shows the LF-to-HF ratio in the same experimental
conditions. An increase of the ratio became evident in the second
part of ASH (3.4
⫾ 0.5 nu), reached its maximum in the first part
of NH3 (6.7
⫾2.2 nu) and decreased to baseline values during the
second part of this condition (2.1
⫾ 0.8 nu). The comparison
among LF-to RF ratios in the different conditions (ANOVA)
yielded significant differences [F(11,44)
⫽ 4.63, p ⬍ 0.001].
However, at variance with the behavior of the previous indexes,
post-hoc test revealed that only the ratio computed for the first part
of NH3 was different from that of NH1 (0.9
⫾ 0.2; 1.2 ⫾ 0.4 nu),
⫾ 0.4 nu; 1.1 ⫾ 0.2 nu), NSH (0.9 ⫾ 0.2 nu; 2.0 ⫾ 0.3
nu), the first part of ASH (0.8
⫾ 0.2 nu), the second part of NH3
and QW (3.6
⫾ 1.7 nu; 1.6 ⫾ 0.5 nu).
Power Spectrum Analysis of EEG Rhythms
ANOVA did not show any significant change for alpha and
beta bands in our experimental paradigm, even if a trend of beta
power to increase in NSH and ASH in fronto-central regions could
For gamma activity (Figs. 3A–C), significant interactions were
detected among hemispheres, lobes, channels and experimental
⫻ conditions ANOVA
⫽ 3.45, p ⬍ 0.001], showed in NSH (Fig. 3A) a
significant prevalence of gamma power in F4 vs. O2 on the right
side while in ASH (Fig. 3B) post-hoc tests indicated differences in
C4 vs. O2 on the right side and F3 vs. O1 and C3 vs. O1 on the left
⫻ conditions [F(10,4020) ⫽ 3.23, p ⬍ 0.001] interac-
tions were present and post-hoc comparisons showed in both ASH
and NSH a significant prevalence in frontal vs. posterior and in
central vs. posterior lobes. No differences were detected between
frontal and central regions.
⫻ conditions interactions were also
⫽ 5.77, p ⬍ 0.001].The comparison for
hemispheres in NSH and ASH revealed a significant left side
In NH3 (Fig. 3C), gamma power did not regain its baseline
value. A significant left hemisphere prevalence as well as a lobe
effect were present. In addition, comparisons between channels in
NH3 revealed a marked fronto-occipital gradient on the left side
⬎C3⬎O1), which was present, albeit attenuated, also on the
The results of the present study indicate that all subjects expe-
rienced an intense negative emotion, as shown by the high scores
of the structured interview and by the remarkable changes in the
cardiorespiratory output and in the EEG pattern after the hypnotic
suggestion of a phobic object. This cognitive tool has proved
useful both to amplify the basal psychological characteristics of
subjects in which the high hypnotizability was combined with a
simple phobia and to provide a reliable model of controlled cog-
nitive stimulation, even if the screening of subjects according to
the standard scales of hypnotic susceptibility is an extremely time
Results also show that the respiratory and cardiac frequencies
are significantly increased with respect to the basal condition
during the aversive suggestion. The observed changes in cardio-
vascular variables are strictly related to the suggestions received
by the subjects (relaxation during neutral hypnosis and fear during
the activation period) and do not depend on the hypnotic state. In
fact, when a standard hypnotic induction [72,73] is performed, the
effect of the suggested relaxation is a parasympathetic prevalence
[20,58], which is considered a simple relaxation response .
The comparison between neutral and aversive activation indi-
cated that the affective and cognitive components of the stimuli
were able to modulate differently heart and respiratory rates: the
former was more influenced by emotion, while the latter was
affected by both components of the stimulus. Changes in breathing
related to a cognitive task have been described when auditory
stimulation (i.e., listening to a story, as in our case) was added to
the baseline conditions with eyes closed and whenever a music
captured the respiratory rhythm. Such changes may be caused by
a volitional respiratory adjustment to the voice or music rhythm
The spectral analysis of the RR interval shows that the changes
in cardiac and respiratory frequencies observed during fear-like
stimulation are linked to changes in LF and HF components,
indicating a shift of the sympatho-vagal balance towards a sym-
pathetic prevalence. The time-course of such modifications
showed a delayed onset of the effect which was shifted towards the
end of the stimulation period reaching its peak in the first part of
the following control condition. These findings were confirmed by
the increase of the LF-to-HF ratio, which showed an equivalent
trend, and became statistically higher towards the first part of the
final baseline condition. These data suggest a sympathetic en-
hancement typical of an active response to an aversive situation
. This is in line with the well-known interaction between
cardiovascular and respiratory systems , which is even more
pronounced in extreme situations when the cooperation becomes
essential for survival .
An increased sympathetic background is also associated with
mental stress [7,33,50] as well as mental and motor imagery
[24,57] and it may represent an essential element in the preparation
for action as part of an integrated and purposeful behavior.
Our choice to limit the analysis to the alpha, beta and gamma
EEG activities rests on the classical assumption that a stressful
stimulus should induce a desynchronization of the EEG pattern,
with a reduction of the alpha and an increase of the beta and
gamma components. However, the interpretation of our results,
which showed the alpha rhythm largely unchanged throughout the
experimental conditions, is complicated by the co-existence of
hypnosis which can elicit, per se, characteristic EEG patterns .
In particular the lack of the expected alpha suppression  during
the activation periods could be linked to hypnosis. A similar result
has been reported by Orne and Paskewitz , who observed that
apprehension or heightened arousal did not always reduce alpha
The tendency exhibited by beta power to increase bilaterally in
fronto-central regions could be the consequence of a general
arousal due to the presentation of the cognitive stimulus which
appears further increased when it is charged by a negative emo-
tional content. The behavior of gamma activity is particularly
relevant to the aim of this study, because this frequency band has
been related to a series of higher cognitive processes, which
include focused attention [54,69], memory [51,61], linguistic pro-
cessing , behavioral and perceptual functions , emotional
states  associative learning  and preparation of motor
responses . In accordance with recent reports [39,45], our
results show a left gamma power increase during the neutral
cognitive activation which is further enhanced by the emotional
valence of the aversive condition. However, these observations
GEMIGNANI ET AL.
contrast with other studies  that report a right side lateraliza-
tion during negative experiences and with the observation of a
right hemisphere predominance of gamma density related to the
recalling of a negative emotion during hypnosis . The discrep-
ancy may be explained by the characteristics of the stimulus
employed in the different studies. In our case, the stimulus was
presented through the verbal channel, required a focused attention
and contained suggestions of a complex mental imagery. There-
fore, it was strongly directed to the activation of the left hemi-
sphere . Nonetheless, all subjects reported to have experienced
deep negative emotions that were accompanied by marked cardio-
respiratory changes. Particularly relevant for the aim of this study
is the similar behavior exhibited by the gamma EEG activity in the
left fronto-central regions (Fig. 3C) and the sympathetic compo-
nent of the heart period variability (Figs. 2A,C) which exhibited a
parallel increment during the aversive and the subsequent baseline
FIG. 3. Gamma rhythm power spectrum. Distribution of electroencephalographic gamma power within frontal, central and posterior
regions of both sides as a function of the three most relevant experimental conditions: suggestions of a neutral object (A), phobic
object (B) and the following neutral hypnosis (C).
AUTONOMIC RESPONSES, BEHAVIOR AND EMOTIONS
conditions, thus supporting the concept of a global involvement,
from central command to peripheral output, in human emotional
responses. The linkage between cerebral areas and autonomic
activities has been investigated in animals in which electrophysi-
ological and neuroanatomical data have shown that frontally lo-
cated cortical areas such as the medial prefrontal and insular cortex
 as well as the sensory motor areas [10,70] can modulate the
autonomic output by means of direct projections to areas of the
amygdala [36,37], and hypothalamus , as well as brain steam
[5,68] and spinal cord  that are involved in neurovegetative
control. Thus cognitive, autonomic and somatic-motor activities
are integrated in the production of patterned responses, which may
differ according to environmental situations. Such integrated re-
sponses may represent a reliable index of a specific emotional state
and could be used as time markers for scanning procedures in
neuroimaging experiments aimed to identify the central nervous
structures involved in the control of the different aspects of human
The research was funded by a grant of the M.U.R.S.T. (Italian Ministry
of University, Scientific Research and Technology).
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