Functional Neuroanatomy of Hypnotic State

Functional Neuroanatomy of Hypnotic State
Pierre Maquet, Marie Elisabeth Faymonville, Christian Degueldre, Guy Delfiore,
Georges Franck, Andre´ Luxen, and Maurice Lamy

Background: The aim of the present study was to describe the distribution of regional cerebral blood flow during the hypnotic state (HS) in humans, using positron-emission
tomography (PET) and statistical parametric mapping.
Methods: The hypnotic state relied on revivification of pleasant autobiographical memories and was compared to imaging autobiographical material in “normal alertness.�
A group of 9 subjects under polygraphic monitoring received six H2
15O infusions and was scanned in the following order: alert–HS–HS–HS with color hallucination–HS with color hallucination–alert. PET data were analyzed using statistical parametric mapping (SPM95).
Results: The group analysis showed that hypnotic state isrelated to the activation of a widespread, mainly leftsided, set of cortical areas involving occipital, parietal, precentral, premotor, and ventrolateral prefrontal cortices and a few right-sided regions: occipital and anterior cingulate cortices.
Conclusions: The pattern of activation during hypnotic state differs from those induced in normal subjects by the simple evocation of autobiographical memories. It shares many similarities with mental imagery, from which itdiffers by the relative deactivation of precuneus. Biol Psychiatry 1999;45:327–333 © 1999 Society of Biological Psychiatry
Key Words: Cerebral blood flow, positron-emission tomography,statistical parametric mapping, hypnosis, mentalimagery

Introduction
Hypnosis has been used as a therapeutic tool since mankind’s early history (De Betz and Sunnen 1985).
Nevertheless, its acceptance by the scientific communityremains limited. Consequently, the neural correlates of hypnotic state (HS) remain poorly understood. One field where the efficacy of HS has been objectively evaluated and validated is pain control (Faymonville et al 1995).
Since 1992, more than 1350 patients underwent surgical procedures with a specific anesthetic method combining local anesthesia, conscious sedation, and hypnosis (Faymonville et al 1995, 1996, in press). This procedure was proposed instead of general anesthesia. We showed that
the HS procedure significantly increased patient (and surgeon) comfort.
To better understand what happens in patients in the HS during surgery, we decided to explore the brain mechanisms underlying the HS in healthy volunteers by determining the distribution of regional cerebral blood flow (rCBF), taken as an index of local neuronal activity. The HS was induced in the same way as it is in patients during surgery (eye fixation, progressive muscular relaxation, and evocation of pleasant life experience). Regional cerebral perfusion was determined by positron-emission tomography (PET), with H2 15O infusions. Data were analyzed using statistical parametric mapping (SPM).
The study reported here should be considered as a first step in our approach to HS; it focuses on HS processes per se. The analgesic effects of HS are specifically explored in another experimental protocol.
Methods and Materials
Subjects’ Selection
This study was approved by the Ethical Committee of the Faculty
of Medicine of the University of Lie`ge.
Young healthy right-handed subjects were considered for
selection, after they gave their written informed consent. All of
them were people working in the operating theater, and they
applied spontaneously to participate to the experiment. From a
cohort of 30 screened subjects, 15 were selected because they
were scored as highly hypnotizable subjects (score .8) on the
Stanford scale–form C (Hilgard et al 1963). During the selection
procedure, which took place several weeks before the experimental
session, subjects were asked to recall souvenirs they
wanted to be used on the scanner.
PET Acquisitions
EXPERIMENT 1. Nine subjects (7 female, 2 male; mean age
30.7 years; age range 23–38) participated in the study. Before the
scanning session, electrodes were put in place to monitor
electroencephalogram (EEG) (C3–A2 and C4–A1), horizontal
From the Cyclotron Research Center (CRC), University of Lie`ge, Lie`ge, Belgium
(PM, CD, GD, GF, AL); Department of Neurology, CHU Sart Tilman, Lie`ge,
Belgium (PM, GF); and Department of Anesthesiology and Intensive Care
Medicine, CHU Sart Tilman, Lie`ge, Belgium (MEF, ML).
Address reprint requests to Dr. Pierre Maquet, Cyclotron Research Center (B 30),
University of Lie`ge, 4000 Lie`ge, Belgium.
Received May 20, 1997; revised November 25, 1997; accepted December 11, 1997.
© 1999 Society of Biological Psychiatry 0006-3223/99/$19.00
PII S0006-3223(97)00546-5
electro-oculogram (EOG), and chin electromyogram (EMG). A
venous catheter was inserted under local anesthesia in a left
antebrachial vein. The subject’s head was stabilized by a thermoplastic
face mask secured to the head-holder (Truscan imaging,
MA). Earphones were adapted to the subject’s head. Verbal
communications were made at a distance via a microphone at all
times. A transmission scan was performed to allow a measured
attenuation correction. In both experiments, six emission scans
were acquired. Each consisted of two frames: a 60-sec background
frame and a 120-sec frame. The slow intravenous water
(H2
15O) infusion was begun just before the second frame to
observe the head curve rising within the first 10 sec of this frame.
Thirty millicuries (1110 MBq) were injected for each scan, in 10
cc saline, over a period of 60 sec. The infusion was totally
automated so as not to disturb the subject during the scanning
periods. Data were acquired by a Siemens CTI 951 R 16/31
scanner in 2D mode. Data were reconstructed using a Hanning
filter (cutoff frequency: 0.5 cycle/pixel) and corrected for attenuation
and background activity. The final in-plane image resolution
was 8.7 mm full width at half maximum (FWHM)
(Degueldre and Quaglia 1992).
Each subject was scanned twice in each of three conditions,
under continuous polygraphic monitoring. In the first condition
(I: alert state with autobiographical information), the subjects
were studied while listening to sentences containing pleasant
information taken from their own past. Subjects were instructed
to imagine what happened to them in the described situations.
The subjects were urged not to try to enter a hypnotic state. In the
second condition (II: hypnotic state), the subjects were scanned
after the hypnotic state was induced. Hypnotic state was considered
to be present when roving eye movements were observed on
oculography and if, just before the scan, the subject responded by
a foot movement that he felt in HS. During the hypnotic state,
subjects were invited to have revivification of pleasant life
experiences. In the third condition (III: hypnosis with forced
color hallucinations), while in hypnotic state, the subject was
asked to focus on their preferred colors and to view settings and
objects in these colors. Scan was also acquired after the subject
manifested by a foot movement that he actually succeeded in
attaining the targeted colors.
To avoid multiple hypnotic inductions that would have unduly
lengthened the experimental procedure, the acquisitions during
HS were blocked in the middle of the session. In consequence,
the order of injections was I, II, II, III, III, I for all subjects.
Subjects were scanned with eyes closed throughout the experimental
procedure. Ambient noise was reduced to a minimum,
and ambient light was dimmed. The same experimenter (MEF)
spoke to the subjects in all conditions.
EXPERIMENT 2. This experiment was designed to evaluate
the distribution of regional cerebral blood flow during revivification
of personal memories, which served as the control
situation in experiment 1.
Six subjects (4 female, 2 male; mean age 29.3 years; age range
24–39) participated in this experiment, during which we contrasted
the autobiographical condition to a resting condition. In
the first condition (IV: rest), subjects were scanned in a resting
state and were asked to empty their mind. The second condition
(V: autobiographical) exactly replicated the control condition of
the first experiment. The third condition (VI) was part of a larger
study on language processing and will not be discussed here. In
this condition, the subjects heard the auditory stimuli presented
during condition V, played backward on a tape.
The order of injection respected a Latin square design (IV, V,
VI, VI, V, IV) and was counterbalanced over subjects. Subjects
were scanned with eyes closed throughout the experimental
procedure. Ambient noise was reduced to a minimum, and
ambient light was dimmed. Data acquisition was identical to
experiment 1, except that no polygraphic recording was obtained.
Data Analysis
PET data were analyzed using the statistical parametric mapping
software (SPM95 version; Wellcome Department of Cognitive
Neurology, Institute of Neurology, London, U.K.) implemented
in MATLAB (Mathworks Inc., Sherborn, MA). In short, data
from each subject were realigned using a least square approach
and the first scan as a reference (Friston et al 1995a). Following
realignment, all images were transformed into a standard space
(Friston et al 1995a; Talairach and Tournoux 1988) and then
smoothed using a 12-mm FWHM isotropic kernel. A design
matrix was specified, according to the general linear model
(Friston et al 1995b). It included the global activity as confounding
covariate (Friston et al 1990). The condition effects were first
estimated at each and every voxel. The analysis used linear
contrasts to identify the brain regions where rCBF was significantly
increased (II1III2I) or decreased (I2II2III) in hypnosis
as compared to normal alertness. The areas more active during
hypnosis with color hallucination than during hypnosis alone
(III2II) were also looked for. Finally, the analysis looked for
areas more active while listening to autobiographical evocation
than at rest (V2IV).
The resulting set of voxel value for each contrast constituted a
map of the t statistic (SPM{t}). The SPM{t} were then transformed
to the unit normal distribution (SPM{Z}) and thresholded
at p , .001 (Z 5 3.09). The resulting foci of activation were
finally characterized in terms of peak height over the entire
volume analyzed, [p(Zmax . u)], which corresponds to a corrected
p value , .05 (Friston et al 1991, 1994, 1995b).
Results
Experiment 1
All subjects readily entered the HS when HS induction
was begun. They remained in the HS until the end of the
fifth scan, as requested by the experimental protocol.
During the experimental session, EEG recordings did
not show any sign of sleep (spindles, K complexes).
During HS, the waking alpha rhythm was fragmented and
replaced by periods of slower (theta) activities. Oculograms
systematically showed slow roving eye movements.
EMG recordings were characterized by a decreased muscular
tone.
During HS with color hallucination, all subjects reported
having successfully obtained the desired color.
328 P. BIOL PSYCHIATRY Maquet et al
1999;45:327–333
Significant increases in rCBF during hypnosis (conditions
II and III) as compared to normal alertness (condition
I) were observed in four regions (Table 1, Figure 1A). The
largest excursion set was left-sided and involved extrastriate
visual cortex [Brodmann’s area (BA) 18, 19, 37],
inferior parietal lobule (BA 40), precentral and adjacent
premotor (BA 6) cortex, and the depth of ventrolateral
prefrontal cortex (BA 45), close to the insular cortex. The
second area was right-sided and involved deep cerebellar
nuclei and prestriate cortex (BA 18). The two last areas are
the right anterior cingulate cortex (BA 24/32) and left
occipitotemporal cortex (BA 37). Significant decreases in
rCBF during hypnosis as compared to normal alertness
(Table 1, Figure 1B) were observed in left temporal cortex
(BA 20, 21, 38, 39), right temporal cortex (BA 21, 22),
medial prefrontal cortex (BA 8, 9, 10), posterior cingulate
(BA 39) and adjacent precuneus (BA 7), right premotor
cortex (BA 6/8), and right cerebellar hemisphere. No
significant rCBF variations were detected between hypnosis
with and without forced color hallucination.
The comparison of conditions III and II (effects of color
hallucinations during HS) provided no significant results.
Table 1. Localizationa and Statistical Resultsb Concerning the Local Maxima of the Brain Areas Where rCBF Is Significantly
Higher or Lower in Hypnotic State than during Imaging Autobiographical Material in “Alert� State
Side Cerebral area BA x y z Z score p (corrected)
Increases in HS
Left Occipital cortex 18 224 296 24 4.30 .032
230 276 0 4.71 .006
224 282 0 5.05 .001
19 230 268 24 4.37 .024
220 262 36 5.37 ,.001
37 250 256 220 4.92 .002
Right Occipital cortex 18 2 278 24 4.73 .006
6 270 28 4.24 .039
Left Inferior parietal lobule 40 224 248 28 5.66 ,.001
240 234 32 4.88 .003
Left Precentral cortex 4 248 28 32 4.63 .008
4/6 236 24 32 4.39 .022
4/43 242 210 20 4.27 .035
226 222 36 4.44 .018
Left Prefrontal cortex 45 228 26 8 5.45 ,.001
224 22 16 5.16 .001
228 12 20 4.61 .009
Right Anterior cingular cortex 24/32 14 32 16 4.43 .019
Right Cerebellum 16 252 228 5.85 ,.001
10 264 212 4.96 .002
Decreases in HS
Left Temporal cortex 20 256 216 20 4.71 .006
21 246 0 20 4.91 .003
260 234 8 4.23 .041
38 226 16 20 5.29 ,.001
240 8 20 4.47 .017
39 246 264 4 4.41 .021
Right Temporal cortex 21 48 0 16 7.11 ,.001
60 224 4 5.28 ,.001
22 56 230 4 5.12 .001
Medial Prefrontal cortex 8 26 34 4 5.10 .001
24 26 8 4.86 .003
26 12 8 4.17 .050
9 24 50 4 4.82 .004
10 0 50 8 4.22 .042
Right Premotor cortex 6 42 2 4 5.64 ,.001
Medial Precuneus 7 22 256 4 5.70 ,.001
Right Cerebellum 18 282 228 4.35 .026
aCoordinates are defined in the stereotactic space of Talairach, relative to anterior commissure. x represents the lateral distance from midline (positive 5 right); y is the
anteroposterior distance from anterior commissure (positive 5 anterior); z represents the rostrocaudal distance from the bicommissural plane (positive 5 rostral).
bThe areas are significant at a threshold of p 5 .001, by reference to unit normal distribution (Z 5 3.09), and at a threshold of corrected p , .05 (corrected p, the
probability that the regional rCBF variation could have occurred by chance over the entire volume analyzed).
Functional Neuroanatomy of Hypnotic State BIOL PSYCHIATRY 329
1999;45:327–333
Experiment 2
Significant increases in rCBF (Table 2) during the autobiographical
condition (condition V) as compared to rest
(condition IV) were observed bilaterally, in temporal poles
(BA 38), superior (BA 42) and middle (BA 21 and 22)
temporal gyrus, and a region located near the basal
forebrain. On the left side, significant increases were
observed in the left entorhinal cortex, and in the premotor
cortex (BA 6).
Discussion
Assessment of the Hypnotic State
The critical issue in this experiment was that the hypnotic
state was internally generated, and that no output was
required from our subjects. In consequence, we had to
resort to all sorts of precautions to ascertain, as objectively
as possible, the presence of the hypnotic state during
scanning. First, the subject’s behavior and clinical appearance
was identical to that routinely observed in patients
undergoing surgical interventions or burn debridement
under hypnosis (Faymonville et al 1995, 1996, in press).
Second, oculograms showed slow eye movements, intermingled
with ocular saccades. It should be emphasized
that slow roving eye movements cannot be willingly
mimicked (Plum and Posner 1980). Their presence rules
out any simulated state. Third, if polygraphic recordings
sometimes showed a fragmentation of a rhythm and the
outbreak of slow (theta) rhythm bursts during hypnosis,
overt signs of sleep (K complexes or spindles) never
occurred. Fourth, the subjects were requested, just before
each scan, to manifest they actually felt themselves to be
in a hypnotic state. They were also interviewed afterwards
about their hypnotic experience. All subjects admitted that
they readily fell into a hypnotic state at the induction and
remained in this state as long as requested. They usually
reported having experienced vivid, detailed, and colorful
revivifications of pleasant memories, having actually mentally
reenacted them.
Each of these points, taken in isolation, does not prove
there was a hypnotic state in our subjects, but together they
form a body of arguments that, by their co-occurrence,
strongly suggest that this was the case.
Comparison with Previous Neuroimaging Data in
HS
Only a handful of neuroimaging studies using PET or
single photon emission computed tomography (SPECT)
have explored the hypnotic state. Their results did not
Figure 1. Projections in the Talairach’s stereotactic space of brain areas where rCBF is significantly increased (A) or decreased (B)
during hypnosis, as compared to normal alertness with autobiographical information. Functional PET results are displayed at threshold
of Z 5 3.09 (p , .001). VPA and VPC identify anterior and posterior commissural planes, respectively.
330 P. BIOL PSYCHIATRY Maquet et al
1999;45:327–333
succeed in sketching a consistent metabolic pattern for the
HS. During hypnosis, increases in rCBF of various cerebral
regions (right frontal, orbitofrontal, temporal, motor,
and somatosensory areas) were reported in SPECT studies
(Crawford et al 1993; Diehl et al 1989; Halama 1989;
Meyer et al 1989). Using PET, it was observed that the
glucose metabolism was decreased in occipital regions and
was increased in sensorimotor areas during HS (Grond et
al 1995).
The diversity of results is in part due to the experimental
conditions that explored various aspects of hypnosis
(mainly hypnotic analgesia and cataleptic hypnosis). Furthermore,
in many of these studies, the spatial resolution
of the technique was not sufficient to yield a detailed map
of the HS metabolic pattern.
rCBF Distribution during HS
The choice of the control task was a difficult one for, a
priori, no cerebral state was close to the HS. Because the
induction and maintenance of HS relies on revivification
of pleasant autobiographical memories, the closest situation
was the evocation of autobiographical information, in
the absence of the hypnotic state. To better understand the
comparisons made for HS, we set up experiment 2,
investigating the control condition of the first experiment.
The results showed that listening to autobiographical
material activates the anterior part of both temporal lobes,
basal forebrain structures, and some left mesiotemporal
areas. This metabolic pattern is in excellent agreement
with a recent PET study of autobiographical memory
(Fink et al 1996).
In contrast, during HS, a vast activation was observed
that involved occipital, parietal, precentral, prefrontal, and
cingulate cortices. The metabolic distributions due to
hypnotic state and to evocation of autobiographical information
did not overlap. These results show that HS relies
on cerebral processes different from simple evocation of
episodic memory and suggest that HS is related to the
activation of sensory and motor cortical areas, as during
perceptions or motor acts, but without actual external
inputs or outputs. In this respect, hypnosis is reminiscent
of mental imagery (Kosslyn 1993). The imagery content in
HS was polymodal. Although subjects predominantly
reported visual impressions, somesthetic and olfactory
perceptions were also mentioned. A lot of actions also
appeared in the hypnotic experience of most of our
subjects. In contrast, none of the subjects reported auditory
imagery. When sounds were mentioned, they came from
the actual experimental environment (mainly, the experimenter’s
voice).
The visual mental imagery might take into account the
activation of a set of occipital areas. The activation of
early visual areas (BA 18, occipital pole) has been
proposed as a visual buffer organizing visual information
(Kosslyn et al 1993). Ventral regions (lingual and fusiform
gyrus, BA 37) would reflect the recognition and discrimination
of face and object features (Haxby et al 1991;
Sergent et al 1992), whereas more dorsal activation (BA
39 and 40) would be related to the spatial organization of
visual imagery (Kosslyn et al 1996). The left-sided predominance
of the activation has previously been reported
in visual mental imagery. Left hemisphere would be more
able to generate and arrange parts of mental images (Farah
1984), although both hemispheres have specific imagery
capacities (Kosslyn et al 1993). More anteriorly, the
activation of precentral and premotor cortices is similar to
that observed during motor imagery (Decety et al 1994),
which could also have participated in the parietal activation
(Stephan et al 1995). The activation of ventrolateral
prefrontal cortex has also been observed in mental imag-
Table 2. Localization and Statistical Results Concerning the Local Maxima of the Brain Areas Where rCBF Significantly
Increases during Evocation of Autobiographical Memories, as Compared to “Rest�
Side Cerebral area BA x y z Z score p (corrected)
Left Temporal cortex 21 256 226 0 6.34 ,.001
22 258 240 4 5.01 .002
250 22 24 4.85 .003
38 246 6 212 4.50 .014
42 238 228 8 4.61 .009
Right Temporal cortex 21 52 210 24 5.25 .001
48 22 212 4.96 .002
22 52 228 4 7.17 ,.001
38 40 12 212 5.30 ,.001
Left Premotor cortex 6 238 22 44 4.87 .003
Left Mesiotemporal 28 222 10 220 4.41 .021
Left Basal forebrain 210 2 28 4.66 .007
Right Basal forebrain 22 4 28 5.39 ,.001
Coordinates and statistical results determined as in Table 1.
Functional Neuroanatomy of Hypnotic State BIOL PSYCHIATRY 331
1999;45:327–333
ery tasks (Kosslyn et al 1996) and would be involved in
the programming of the building up of the mental image or
in the maintenance of image in memory. In this respect,
the left-sided lateralization is not easily explained. We do
not feel that prefrontal activation could reflect subvocal
subjects’ vocalization, because orofacial movements are
usually less frequent in hypnosis. Finally a right-sided
activation of anterior cingulate cortex would probably
reflect the attentional effort necessary for the subject to
internally generate mental imagery (Devinsky et al 1995;
Posner and Petersen 1990).
Some cortical areas are significantly less active during
hypnosis that during the alert state. These temporal deactivations
might simply emphasize that autobiographical
evocation is, in contrast to HS, characterized by a prominent
activation of anterior temporal lobe structures (experiment
2 and Fink et al 1996). Alternatively, the deactivation
of anterior parts of both temporal lobes could also
indicate that subjects did not resort to auditory mental
imagery, which is known to activate temporal areas
(Zatorre et al 1996). It could also be explained by the
experimental conditions. The examiner’s speech rate was
lower during the hypnosis than during alert conditions.
This parameter is known to influence the activity of left
superior temporal cortex (Price et al 1992). Likewise,
processing of pitch (which was lower and more monotonous
during HS) depends on right hemisphere structures
(Zatorre et al 1992; Zatorre and Samson 1991).
The deactivation of precuneus has been reported during
visual discrimination tasks, when visual stimulus is physically
present (Shulman et al 1996). In contrast, precuneus
is usually activated in tasks requiring mental imagery
(Kosslyn et al 1996), long-term memory (Grasby et al
1993), and visual attention (Corbetta et al 1993). The
deactivation of precuneus is certainly an important metabolic
feature distinguishing hypnotic state from alert
visual mental imagery.
The mesial frontal deactivation remains speculative, as
the function of this part of the prefrontal cortex remains
fragmentary. Such deactivation has been reported in several
tasks, such as visual discrimination (Shulman et al
1996) and mental arithmetics (Ghatan et al 1996). It would
reflect the interruption of tasks going on during alert
condition, irrelevant to the HS, such as unconstrained
monitoring of environment, emotional state, or thought
processes.
Comparison with Other Internally Generated
Mental Experiences
Hypnotic state should be distinguished from other types of
internally generated, polymodal perceptuomotor experiences,
the functional anatomy of which has recently been
approached with PET: dreams during REM sleep in
normal subjects (Maquet et al 1996), and hallucinations in
schizophrenic patients (Silbersweig et al 1995).
In the present study, no subjects presented polygraphic
evidence of slow sleep (sleep spindles, K complexes, or
large-amplitude slow waves) or REM sleep (especially
complete atonia). The distribution of regional cerebral
blood flow during HS is mainly cortical and does not seem
to activate the pons, the thalami, and amygdaloid complexes,
in contrast to what has been observed in REM
sleep with dreaming (Maquet et al 1996).
Likewise, HS differs from the schizophrenic hallucinations
(estimated on a group of patients) by the absence of
subcortical and paralimbic activation and by the activation
of lateral prefrontal cortex (Silbersweig et al 1995).
Conclusions
Taken together, these results suggest that, in our experimental
conditions, HS is a particular cerebral waking state
where the subject, seemingly somnolent, experiences a
vivid, multimodal, coherent, memory-based mental imagery
that invades and fills the subject’s consciousness.
PM is Research Associate at the Fonds National de la Recherche
Scientifique de Belgique (FNRS). This research was supported by FNRS
grant number 3.4553.95.
The authors are greatly indebted to Professor R.S.J. Frackowiak and
Doctor K.J. Friston (Wellcome Department of Cognitive Neurology,
Institute of Neurology, London, U.K.) for having kindly provided the
statistical parametric mapping software, and to Mrs. Christiane Meesters,
Mr. Patrick Hawotte, and Mr. Marcel Pie´rrard for their technical
assistance.
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