learning in trance: functional brain imaging studies and neuropsychology

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Learning in trance: Functional brain imaging studies and neuropsychology Ulrike Halsband * Neuropsychology, Department of Psychology, University of Freiburg, Engelbergerstrasse 41, D-79085 Freiburg, Germany Abstract This study examined the fundamental question, whether verbal memory processing in hypnosis and in the waking state is mediated by a common neural system or by distinct cortical areas. Seven right-handed volunteers (25.4 years, sd 3.1) with high-hypnotic susceptibility scores were PET-scanned while encoding/retrieving word associations either in hypnosis or in the waking state. Word-pairs were visually presented and highly imaginable, but not semantically related (e.g. monkey-street). The presentation of pseudo-words served as a refer- ence condition. An emission scan was recorded after each intravenous administration of O-15 water. Encoding under hypnosis was asso- ciated with more pronounced bilateral activations in the occipital cortex and the prefrontal areas as compared to learning in the waking state. During memory retrieval of word-pairs which had been previously learned under hypnosis, activations were found in the occipital lobe and the cerebellum. Under both experimental conditions precuneus and prefrontal cortex showed a consistent bilateral activation which was most distinct when the learning had taken place under hypnosis. In order to further analyze the effect of hypnosis on imagery-mediated learning, we administered sets of high-imagery word-pairs and sets of abstract words. In the first experimental condition word-pair associations were presented visually. In the second condition it was found that highly hypnotisable persons recalled significantly more high-imagery words under hypnosis as compared to low-hypnotisables both in the visual and auditory modality. Furthermore, high-imagery words were also better recalled by the highly hypnotisable subjects during the non-hypnotic condition. The memory effect was consistently present under both, immediate and delayed recall conditions. Taken together, the findings advance our understanding of the neural representation that underlies hypnosis and the neuropsychological correlates of hypnotic susceptibility. Ó 2006 Elsevier Ltd. All rights reserved. Keywords: Hypnosis; Positron emission tomography; Paired word association learning; Occipital cortex; Prefrontal cortex 1. Introduction From a neurobiological point of view, hypnotic trance induction can be interpreted as a modified state of con- sciousness (Rainville et al., 2002). This reflects a dynamic change of brain activity. In this exciting field of current brain research, the goal is to disentangle the neural mech- anisms of hypnosis and to examine whether learning can be improved under hypnosis. A major break-through in the study of the cortical plas- ticity during hypnosis was the use of modern brain imaging techniques. In this fascinating world of neurosciences, efforts for an improved understanding of the brain mecha- nisms involved were made by the use of positron emission tomography (PET) and functional magnetic resonance imaging (fMRI). The PET tomograph is an external detec- tion system that maps the distribution of an injected radi- otracer in three-dimensional space. The masses of the positron and electron are converted into two photons emit- ted in directly opposite directions (180°) with the same energy. By contrast, fMRI is a non-invasive method based on the increase in blood flow to the local vasculature that accompanies neural activity in the brain. Changes in the oxygenation level of the blood, the so-called BOLD (blood oxygenation level dependent) effect, occurs as a 0928-4257/$ - see front matter Ó 2006 Elsevier Ltd. All rights reserved. doi:10.1016/j.jphysparis.2006.03.015 * Tel.: +49 761 203 2473; fax: +49 761 203 9438. E-mail address: [email protected] www.elsevier.com/locate/jphysparis Journal of Physiology - Paris 99 (2006) 470–482

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    be improved under hypnosis.A major break-through in the study of the cortical plas-

    ticity during hypnosis was the use of modern brain imaging

    ted in directly opposite directions (180) with the sameenergy. By contrast, fMRI is a non-invasive method basedon the increase in blood ow to the local vasculaturethat accompanies neural activity in the brain. Changes inthe oxygenation level of the blood, the so-called BOLD(blood oxygenation level dependent) eect, occurs as a

    * Tel.: +49 761 203 2473; fax: +49 761 203 9438.E-mail address: [email protected]

    Journal of Physiology - Paris1. Introduction

    From a neurobiological point of view, hypnotic tranceinduction can be interpreted as a modied state of con-sciousness (Rainville et al., 2002). This reects a dynamicchange of brain activity. In this exciting eld of currentbrain research, the goal is to disentangle the neural mech-anisms of hypnosis and to examine whether learning can

    techniques. In this fascinating world of neurosciences,eorts for an improved understanding of the brain mecha-nisms involved were made by the use of positron emissiontomography (PET) and functional magnetic resonanceimaging (fMRI). The PET tomograph is an external detec-tion system that maps the distribution of an injected radi-otracer in three-dimensional space. The masses of thepositron and electron are converted into two photons emit-Abstract

    This study examined the fundamental question, whether verbal memory processing in hypnosis and in the waking state is mediated bya common neural system or by distinct cortical areas. Seven right-handed volunteers (25.4 years, sd 3.1) with high-hypnotic susceptibilityscores were PET-scanned while encoding/retrieving word associations either in hypnosis or in the waking state. Word-pairs were visuallypresented and highly imaginable, but not semantically related (e.g. monkey-street). The presentation of pseudo-words served as a refer-ence condition. An emission scan was recorded after each intravenous administration of O-15 water. Encoding under hypnosis was asso-ciated with more pronounced bilateral activations in the occipital cortex and the prefrontal areas as compared to learning in the wakingstate. During memory retrieval of word-pairs which had been previously learned under hypnosis, activations were found in the occipitallobe and the cerebellum. Under both experimental conditions precuneus and prefrontal cortex showed a consistent bilateral activationwhich was most distinct when the learning had taken place under hypnosis.

    In order to further analyze the eect of hypnosis on imagery-mediated learning, we administered sets of high-imagery word-pairs andsets of abstract words. In the rst experimental condition word-pair associations were presented visually. In the second condition it wasfound that highly hypnotisable persons recalled signicantly more high-imagery words under hypnosis as compared to low-hypnotisablesboth in the visual and auditory modality. Furthermore, high-imagery words were also better recalled by the highly hypnotisable subjectsduring the non-hypnotic condition. The memory eect was consistently present under both, immediate and delayed recall conditions.Taken together, the ndings advance our understanding of the neural representation that underlies hypnosis and the neuropsychologicalcorrelates of hypnotic susceptibility. 2006 Elsevier Ltd. All rights reserved.

    Keywords: Hypnosis; Positron emission tomography; Paired word association learning; Occipital cortex; Prefrontal cortexLearning in trance: Fustudies and ne

    Ulrike H

    Neuropsychology, Department of Psychology, University of0928-4257/$ - see front matter 2006 Elsevier Ltd. All rights reserved.doi:10.1016/j.jphysparis.2006.03.015ctional brain imagingropsychology

    sband *

    iburg, Engelbergerstrasse 41, D-79085 Freiburg, Germany

    www.elsevier.com/locate/jphysparis

    99 (2006) 470482

  • ioloconsequence of neuronal activity. The magnitude of changein signal intensity can be used as an indirect measure ofexcitary input to neurons (Logothetis et al., 2001). Adetailed description of brain imaging tools was given byOtte and Halsband (2006).

    The decision to choose one or the other neuroimagingmodality depends on the task of interest. Although onemajor advantage of fMRI is that this technique does notneed radioactive tracers, fMRI has rarely been appliedin the study of the neurobiology of hypnosis. This showsthe limitation of fMRI in relaxation conditions due tothe noise of the scanner and the inconvenient trance condi-tion. By contrast, PET imaging has been more frequentlyapplied as volunteers can be injected with a radiopharma-ceutical while they are deeply relaxed in trance and scannedat another time while they are awake. In contrast, a subjectin an fMRI apparatus is constantly exposed to a noise levelof approximately 100 decibels. Although it is possible toreduce this noise level to about 70 decibels with the helpof a special fMRI-compatible headset, this backgroundnoise remains an inadequate interference. In this studywe used PET as a suitable brain imaging technique. Earlier,we reported a preponderance of commonalities in the acti-vation patterns yielded with fMRI and PET (e.g. Halsbandet al., 1998, 2002; Krause et al., 1999a,b; Mottaghy et al.,1999a,b, 2000; Schmidt et al., 2002); these ndings wereconrmed by other studies (e.g. Schall et al., 2003).

    Several authors have shown that plastic changes in neu-ronal activity occur after hypnotic trance induction (e.g.Crawford et al., 1998; Faymonville et al., 2000; Grondet al., 1995; Halsband, 2004; Kosslyn et al., 2000; Maquetet al., 1999; Rainville et al., 1997, 1999, 2002; Spiegel andKosslyn, 2004; Szechtman et al., 1998). Trance is character-ised by focused attention and ones awareness of internalimages. This altered state of consciousness extends to dif-ferent aspects of the subjects personal awareness. It hasbeen reported that volunteers experience events as beingmore colourful and intense and which may turn this kindof experience into a dierent form of reality (Revenstorf,1999). Special emphasis has been placed on the nding thatvolunteers reported that their personal experience underhypnosis was more colourful as compared to their wakingstate. Most interestingly, the subjective experience to per-ceive objects as more colourful was conrmed by ndingsusing PET as a brain imaging technique. PET studies indi-cate an increased left-sided activation in the fusiform(Brodmann area 19) and in the inferior temporal cortex(Brodmann area 20) (Kosslyn et al., 2000). In a welldesigned study by Kosslyn et al. (2000) it was investigatedwhether hypnosis can modulate colour perception. It wasfound that colour areas were activated under hypnosiswhen subjects were asked to perceive colour, whether theywere actually shown the colour or a grey-scale stimulus. Itwas concluded that among highly hypnotisable subjects,observed changes in subjective experience reached during

    U. Halsband / Journal of Physhypnosis were reected by changes in brain function simi-lar to those that occur in perception. These ndings sup-port the claim that hypnosis is a psychological state withdistinct neural correlates. Neural changes under hypnosisare not restricted to the visual modality, but were alsofound in other sensory modalities (e.g. Szechtman et al.,1998; Walter et al., 1990). Taken together these ndingsargue for a better utilisation of multimodal sensory pro-cessing strategies under hypnosis.

    A key question to be addressed is whether an enhancedutilisation of high-imagery associations positively aectslearning under hypnosis (Bongartz, 1985; Crawford andAllen, 1996; Halsband, 2001, 2004). Crawford and Allen(1996) systematically investigated the relationships betweenthe recall of low- and high-imagery word-pair associationsand hypnotic susceptibility. Forty-one low and 41 highlyhypnotisable college students were assigned to one of fourexperimental groups: wakinghypnosis, hypnosiswaking,wakingwaking, or hypnosishypnosis. In general, recallwas signicantly better for high-imagery compared tolow-imagery words. In a more sensitive within-subjectsdesign, high-hypnotisables recalled more paired associationwords during hypnosis than waking. In contrast, lows didnot dier. However, in a between-subjects design, hypnoticlevel was not a moderator of performance during hypnosisand it was found that low-hypnotisables recalled morewords in the within-subjects design. Taken together, thendings by Crawford and Allen (1996) are controversialand do not allow a general conclusion that the use of imag-ery strategies in high-hypnotisables increases their learningability. Furthermore, the neural correlates of learningunder hypnosis remained unclear.

    The aim of our study was to use O-15 water PET look atdierences in cerebral activation patterns associated withthe verbal memory processing of high-imagery wordsunder hypnosis and in the waking state. In a within-subjectdesign we tried to disentangle the neural mechanisms ofencoding and retrieval in high-hypnotisables under hypno-sis and in the waking state. This is the rst study lookinginto shared and non-shared neural substrates in a word-pair association paradigm for the two experimental condi-tions (hypnosis vs. waking).

    Furthermore, we addressed the question whether recallwas signicantly better for high- as compared to low-imag-ery words in highly hypnotisable subjects. This was testedin the waking state and under hypnosis. We examinedwhether subjects reached a superior performance of learn-ing words with high-imagery content under hypnosis. Forthis purpose, volunteers had to encode and retrieve setsof visually presented high-imagery words and sets ofabstract words which were not semantically related. Itwas further examined whether a dierence in performancewas modality specic or whether it also occurred in othersensory modalities. In comparison, high- and low-hypnot-isables were presented high-imagery and abstract wordsin an auditory condition both in the waking state andunder hypnosis. Finally, we addressed the question

    gy - Paris 99 (2006) 470482 471whether the learning eect would remain stable underdelayed conditions.

  • iolo2. Experiment 1: Visual word-pair association learning

    2.1. Methods

    2.1.1. Experimental subjects

    This study was based on 15 right-handed volunteers.Subjects were assessed on the German version of theHarvard Group Scale of Hypnotic Susceptibility (HGSHSForm A). Seven highly hypnotisable subjects with a suscep-tibility score >7 were assigned to the PET study. Theirmean age was 25.4 years (sd 3.1). Volunteers had no knownhistory of neurological or psychiatric illness. Each subjectgave informed, written consent for participation in thestudy according to the declaration of Helsinki.

    All volunteers had undergone an MRI examination(1.5 T) of the brain, where no structural abnormalities werefound.

    2.1.2. Positron emission tomography imaging

    PET makes an absolute quantication of the regionalcerebral blood ow (rCBF) possible (Frackowiak et al.,1980; Herzog et al., 1996). The rCBF value was determinedby means of an intravenous injection of the positron emit-ting tracer O-15H2O and its dispersement in the brainmeasured over 2 min.

    The O-15-labeled water was produced with the low-energy deuteron accelerator Cyclone 3 (Ion Beam Applica-tion, Inc., Louvain-la-Neuve, Belgium). Cyclone 3 is acompact cyclotron which produces oxygen-15 (15O) forPET-applications by accelerating positively charged deute-rons up to 3.8 MeV. This gas was processed to watervapour with hydrogen gas on the palladium catalyst. Watervapour was mixed with a sterile saline solution using dial-ysis technique in a continuously working water module(Clark et al., 1987). The half-life of oxygen-15 is 123 s.

    PET measurements were obtained for each subject usinga GE Advance PET Scanner (General Electric MedicalSystems, Milwaukee, Wisconsin, USA). The scanner has18 detector rings and provides 35 transverse sectionsthrough the brain spaced 4.25 mm apart (centre to cen-tre/axial sampling interval). The physical characteristicsof this scanner have previously been described (Lewellenet al., 1996). Transmission scans performed with a 68Ga/68Ge rotating line source were used for measured attenua-tion correction. The head of the subject was placed cor-rectly using a laser positioning system according to thecantho-meatal reference line. The laser positioning systemhelped to obtain images parallel to end 27 mm above thecantho-meatal line. Emission scans were recorded in listmode starting at the intravenous bolus administration of300 MBq O-15-labelled water (10 ml in 1015 s).

    The list mode data was framed into a single frame of40 s starting at the entry of the tracer into the brain andcomprising all 15 image planes. Using ltered back projec-tion, the reconstructed image resolution was about 8 mm

    472 U. Halsband / Journal of Phys(full width at half maximum). A Gaussian lter with a fullwidth half maximum (15 mm) was applied to smooth eachimage to compensate for inter-subject dierences and tosuppress high-frequency noise in the images.

    2.1.3. Experimental set-up: word-pair association learning

    A verbal episodic memory task was used. During encod-ing subjects were visually presented 12 word-pairs. Wordsimplemented in the study were two-syllable German high-imagery nouns that were of high frequency (Meier, 1964).Afterwards, the subjects were asked to retrieve the corre-sponding word-pair associate after having been randomlypresented the rst of the two words of each word-pair(retrieval). Two reference conditions were used, either con-taining 12 single nonsense words (two-syllable pseudo-words that obey German spelling rules) or 12 nonsenseword-pairs.

    The word-pairs were semantically unrelated and there-fore dicult to associate (e.g. monkey-candle). Dicultword associations (as introduced by Wechsler, 1945, inhis Wechsler Memory Scale, Subtest VII) were used toincrease the amnestic demands. Word-pairs were of high-imagery according to a German linguistic database of800 nouns on a scale between 6 and 7 (Baschek et al.,1977). The stimulus words were presented on a 17 in. com-puter monitor placed at a distance of about 70 cm from theeyes (font: Times New Roman; size: 72 points). The letterswere black on a white screen, and were centred. In order toavoid lateralisation eects the second word was writtenunder the rst word. Volunteers were instructed to memo-rise the paired associations (encoding phase). During retrie-val scans, only the rst word was presented and subjectshad to retrieve the associated word from memory.

    2.1.4. Analysis of data

    The data were rst transformed into the ANALYSEformat using a converter program. The actual quantitativeanalysis of the 90 s images was carried out with StatisticalParametric Mapping (SPM96, The Welcome Departmentof Cognitive Neurology, London, UK) software on aSPARC 20 workstation (Sun Microsystems) (Fristonet al., 1994, 1995). Calculations were performed with Mat-lab version 4.2c. Each reconstructed O-15 water scan wasrealigned according to the bi-commissural line into a ste-reotaxic space corresponding to the atlas of Talairachand Tournoux (1988) using a PET template and norma-lised according to Friston et al. (1994). A Gaussian lterwith a full width half maximum (15 mm) was applied tosmooth each image to compensate for inter-subject dier-ences and to suppress high-frequency noise in the images.Dierences in global activity within and between subjectswere removed by the analysis of covariance (ANCOVA)on a voxel by voxel basis with global counts as covariateof regional activity across subjects for each task, as inter-and intra-subject dierences in global activity may obscureregional alterations in activity following cognitive stimula-tion. For each pixel in stereotactic space the ANCOVA

    gy - Paris 99 (2006) 470482generated a condition-specic, adjusted mean rCBF value(normalised to 50 ml/100 ml per minute) and an associated

  • adjusted error variance. The ANCOVA allowed compari-son of the means across the dierent conditions using t-sta-tistics. The resulting map of t values constituted a statisticalparametric map (Friston et al., 1994). Voxels were identi-ed as signicantly activated if they passed the heightthreshold of Z = 3.72 (p < 0.0001) and at least belongedto a cluster of 33 activated voxels (p < 0.05, corrected formultiple comparisons) (Fletcher et al., 1995b).

    2.2. Results

    2.2.1. Encoding of high-imagery word-pairs

    Table 1 shows that during the encoding phase, bilateralactivation was found in the prefrontal cortex (Brodmannareas 9/45/46) and in the anterior cingulate cortex in bothexperimental conditions (hypnosis and waking state). Aninteresting nding was that only under hypnosis a mostpronounced occipital activation was observed. Further-more, in the hypnotic state an increased prefrontal activitywas found (see Fig. 1a, c, and Table 1).

    2.2.2. Retrieval of high-imagery word-pairsTable 2 and Fig. 1b and d show the increase in rCBF

    during retrieval of word-pairs compared with the referencetask. The key ndings indicate signicant increase in blood

    ow in the bilateral prefrontal cortex and bilateral precu-neus (Brodmann area 7 in the medial parietal cortex). Inaddition, a left-sided activation in the anterior cingulumand a right-sided activation in the cerebellum wereobserved under both experimental conditions. The key

    Table 1Encoding of high-imagery word-pairs MINUS the reference

    Talairachcoordinates

    Z BA Region

    x y z

    Hypnosis

    36 56 18 8.09 19 Occipital cortex, left15 74 4 7.73 18 Occipital cortex, right36 42 36 7.46 10 Prefrontal cortex, right26 54 12 6.90 10 Prefrontal cortex, left63 21 38 4.36 46 Lateral frontal cortex, left6 14 39 3.95 32 Anterior cingulum, left

    Wake state

    10 96 4 5.13 17/18 Occipital cortex, left and right18 52 4 4.08 10/11 Prefrontal cortex, right21 48 0 3.71 10 Prefrontal cortex, left12 24 21 4.39 32 Anterior cingulum, leftCoordinates (x,y,z) taken from the atlas of Talairach and Tournoux(1988); the regions are named after Brodmann (BA).

    U. Halsband / Journal of Physiology - Paris 99 (2006) 470482 473Fig. 1. PET activation during encoding and retrieval of high-imagery word-paiWaking condition: (c) encoding (waking state), (d) retrieval (waking state).rs.Hypnosis condition: (a) encoding (hypnosis), (b) retrieval (waking state).

  • nding of this study was that when word-pairs were

    recollection of high-imagery word-pairs (Halsband, 2001,2004) (see Fig. 3).

    2.3. Conclusion

    Volunteers benet from hypnosis when they have toacquire word-pairs with high-imagery content. Resultsindicate an increased involvement of occipital and prefron-tal structures while encoding high-imagery word-pairs dur-ing hypnotic trance. The same structures are also involved

    Table 2Retrieval of high-imagery word-pairs MINUS the reference

    Talairach coordinates Z BA Region

    x y z

    Hypnosis

    12 71 0 8.72 18 Occipital cortex, left43 84 8 8.34 19 Occipital cortex, right20 48 0 8.92 10 Prefrontal cortex, right14 57 12 6.68 10/11 Prefrontal cortex, left

    9 68 40 6.95 7 Precuneus, right12 69 42 6.23 7 Precuneus, left

    2 53 8 5.50 Cerebellum, right20 30 16 4.97 29 Anterior cingulum, left

    Wake state

    0 79 44 5.19 7 Precuneus, bilateral36 48 33 5.94 9 Prefrontal cortex, right36 46 32 4.37 9 Prefrontal cortex, left2 44 19 4.13 29 Anterior cingulum, left2 53 8 4.03 Cerebellum, right

    Coordinates (x,y,z) taken from the atlas of Talairach and Tournoux(1988); the regions are named after Brodmann (BA).

    Fig. 3. Correct answers in % when retrieving high-imagery/easy toassociate compared to high-imagery/dicult to associate word-pairs. Theword-pairs were encoded either during hypnotic trance or in the wakingstate.

    474 U. Halsband / Journal of Physiology - Paris 99 (2006) 470482retrieved which were previously learned under hypnosis, astronger activation in the prefrontal cortex and cerebellum,as well as an additional bilateral activation in the occipitallobe were found (see Fig. 1b, d, and Table 2).

    Our volunteers reported that they had learned the pairedwords in form of images. In a separate behavioural studythe learning performance of high-imagery word-pairs com-pared to abstract word-pairs was examined (Fig. 2).

    It was shown that under hypnosis the retrieval ofabstract word-pairs decreased, as opposed to an increasedFig. 2. Experimental set-up: learning of visually presented word-pair associations.

  • to associate (examples: FriedeAdel: peacenobility, IdeeSitte: ideatradition).

    ioloDuring the retrieval phase only the rst word of eachword-pair was presented in random order. Subjects werewhen retrieving high-imagery word-pairs which were previ-ously learned in trance.

    3. Experiment 2: Auditory word-pair association learning

    3.1. Introduction

    Our previous ndings raise the question, to what extenta better recall of the visual representation of high-imageryword-pairs learned under hypnosis has to be interpretedas a modality-specic phenomenon or whether it alsooccurs in other sensory modalities. In order to investigatethis question, a new set of experiments was designed toexamine the learning and retrieval of word-pairs that werepresented in the auditory modality. As described in theexperimental condition above, volunteers were tested whileawake or in hypnotic trance. It has been hypothesised, thatour ndings are not modality specic, but that an improvedlearning performance of high-imagery word-pairs underhypnosis can also be found in the auditory modality.

    3.2. Preliminary test: methods

    3.2.1. Experimental subjects

    The sample for the pre-test consisted of 34 right-handedstudent volunteers with German as their mother tongue(age 24, sd 6.2). None of the volunteers had a known his-tory of neurological or psychiatric illness. All of our sub-jects were open towards hypnosis and can thus beconsidered as a highly motivated group. The level of hyp-notisability (high or low) was assessed with a modiedversion of the Harvard Group Scale of Hypnotic Suscepti-bility (HGSHS form A). The depth of trance was measuredusing a level rating scale from the HGSHS form A.

    Volunteers with a mean score on the HGSHS scale of>7.0 were classied as high-hypnotisable and those witha score of 7) and 11 low-hyp-notisables (HGSHS-value < 4). The mean age of the volun-teers was 25.5 years (sd 6.8).

    3.3.2. Experimental set-up

    Subjects were tested in single sessions of 90 min. Theexperimental procedure consisted of six steps: (1) focussingand trance induction, (2) step-wise induction, (3) meta-phoric story, (4) preparation for the learning phase, (5) oralpresentation of the paired words, (6) termination of tranceand return to the waking state.

    Trance was initiated using a modied version of theinduction by Revenstorf (personal communication). Thehypnotic session began with the focussing of attentionthrough xation of an object on the ground or on the sub-jects body. Verbal induction in the form of suggestions ofrest and relaxation was also implemented. Next, a step-wiseinduction was used in which the subjects were instructed togo into deeper trance in 10 steps. For the step-wise induc-tion the following mental images were used: (1) ballooninduction: ascending in a hot air balloon in 10 steps; (2)staircase induction: imagining taking 10 steps down a staircase; (3) boat induction: drifting away from the shore of abeautiful lake in 10 steps; (4) diving induction: experiencinga dive in 10-m steps in the South Seas (see Fig. 4). The step-wise inductions were presented in randomised order. Inorder to further deepen the state of trance one of the fol-lowing metaphorical stories was presented in randomorder. Afterwards, a graphically well mediated and allegor-ical story was read aloud thus deepening the state of trance.These stories included:

    Die Weisheit des Meisters (The Masters Wisdom)(from Peseschkian, 2003, Der Kaufmann und derPapagei (The merchant and the parrot) (Frankfurt:Fischer),

    Die Lowengeschichte (The lion story) (Trenkle, 2002,Die Lowengeschichte. Heidelberg: Auer),

    Die Geschichte vom Adler, der sich fur ein Huhn hielt(The story of the eagle which thought it was a chicken)(taken from Revenstorf, personliche Kommunikation)and

    Der Schatz des Wissens (The treasure of knowledge)(also Peseschkian, as mentioned above).

    Next, a standardised preparation for the upcominglearning phase with suggestive strategies was used. Subjects

    gy - Paris 99 (2006) 470482 475were reminded of their deep state of relaxation and wereinstructed that they will experience great ease and little

  • wi

    ioloeort in their learning capacity when presented with lists ofpaired words. After this, the subjects were brought backfrom the hypnotic state by counting backwards from threeto one. The rst word of a word-pair was presented andsubjects were asked to retrieve the associated word frommemory (immediate recall). Thereafter, subjects were askedto ll out a 10-min questionnaire. This was followed by

    Fig. 4. Overview of the experimental set-up

    476 U. Halsband / Journal of Physasking them a second time to retrieve the associated wordsfrom memory and express them verbally (delayed recall)(see Fig. 4). All induction procedures were randomised inorder to rule out possible artefacts, that a specic combina-tion of the trance elements would result in a deeper tranceaccompanied by an enhanced learning eect as comparedto another combination.

    The trance condition and the waking condition (withouttrance) took place on two consecutive days. The durationof time spent with the volunteers by the experimenter wasthe same in both the trance condition and the control con-dition. In the latter condition subjects were presented withsimple problems of arithmetic (example: 8 + 5 = 13) readaloud to them. Thereafter, a story of a short travel reportwas orally presented. The randomisation and the question-ing proceeded in the same way as in the trance condition(high-imagery: easy/dicult to associate; abstract: easy/dicult to associate). Fifty percent of our volunteers wererst subjected to the control condition followed by theexperimental condition, while the other half did the samein the reverse order.

    3.4. Results

    An ANOVA for a repeated measurement design wasperformed.3.4.1. Immediate reproduction

    3.4.1.1. High-imagery word-pair associations. As resultsshow, highly hypnotisable subjects learned paired wordsin the high-imagery/dicult to associate condition intrance better than did the low-hypnotisable subjects(p < 0.05). Furthermore, the high-hypnotisables showedbetter learning eects in trance than they did in the waking

    th orally presented word-pair associations.

    gy - Paris 99 (2006) 470482state (p < 0.05). Thus, in the recollection of high-imagery/dicult to associate word-pairs under hypnosis, the highlyhypnotisable subjects showed an average learning eective-ness of 96%. The same subjects reached an average learningeectiveness of 90% in the waking state. For low-hypnotis-ables, on the other hand, no signicant dierence in theirretrieval rate could be shown (see Fig. 5a).

    In the condition with high-imagery/easy to associateword-pairs, there was no signicant dierence betweenhighly and low-hypnotisable subjects. This could have beencaused by a ceiling eect due to the fact that both experi-mental groups surpassed the 90% retrieval rate with greatease in this least dicult experimental condition. Interest-ingly, in the waking state high-hypnotisables showed a bet-ter performance in learning high-imagery paired words asdid low-hypnotisables (p < 0.01). In the condition high-imagery/dicult to associate (waking state), there was asignicant dierence (p < 0.05) between the high- andlow-hypnotisables, although this dierence was less pro-nounced as compared to the condition with high-imageryand easy to associate word-pairs.

    The results are in agreement with a verbal questioning ofthe volunteers, which indicates that subjects with high-hyp-notic susceptibility tended to use an optimal learning strat-egy, for example transferring each of the paired words intoa single mental image (example: a bear eating honey). This

  • ioloU. Halsband / Journal of Physstrategy was particularly eective in the condition with eas-ily associated word-pairs.

    3.4.1.2. Abstract word-pair associations. In all experimen-tal conditions, the recall of the easy to associate abstractword-pair associations was signicantly better thanthe dicult to associate abstract word-pair associations(p < 0.01).

    Striking was the nding that under hypnosis the learn-ing performance of the dicult abstract word-pairs wassignicantly poorer than in the waking state. The poorestlearning performance was shown by the high-hypnotis-ables in the experimental condition dicult abstract/learn-ing under hypnosis. Under this condition the subjects wereonly able to reproduce 9% of the word-pairs, whereas the

    Fig. 5. (a) Immediate retrieval of orally presented word-pair associations (highthe waking state and under hypnosis. The upper row shows the retrieval of hword-pairs. (b) Delayed retrieval of high-imagery word-pair associations aftergy - Paris 99 (2006) 470482 477same subjects were able to reproduce 35% of the dicultabstract word-pairs learned in the waking state. Thus,when high-hypnotisables learned abstract word-pairsunder hypnosis, their performance deteriorated signi-cantly as compared to the waking state. However, therewas no signicant dierence between high- and low-hyp-notisables in respect to their learning performance ofabstract paired words if these were acquired in the wakingstate.

    3.4.2. Delayed reproduction

    As shown in Fig. 5b, a 10 min interference had no signif-icant impact on the retrieval rate in any of the experimentalconditions (high-imagery easy/dicult or abstract easy/dicult).

    -imagery: easy/dicult to associate; abstract: easy/dicult to associate), inigh-imagery word-pairs, the lower row shows the retrieval of the abstract10 min.

  • iolo3.5. Conclusion

    Highly hypnotisable subjects show a better learning per-formance of high-imagery word-pair associations than dolow-hypnotisable subjects. Their greatest learning advan-tage was reached in trance, in the visual as well as in theauditory modality. But also in the waking state, high-hyp-notisables demonstrated better learning rates of high-imag-ery word-pairs than low-hypnotisables.

    4. Discussion

    4.1. PET study

    One interesting result of the PET study is that underhypnosis there is a signicant increase in the activation ofthe occipital area, not only during encoding but also duringretrieval. These ndings are in agreement with the results ofthe study by Kosslyn et al. (2000), who reported anincreased activity in the left fusiform of the occipital areawhen subjects were either presented a coloured stimulusor when they were presented a grey stimulus which theywere to imagine seeing in colour. The neural activity in thisregion of the occipital area only occurred under hypnosisand not in the waking state. Our experiment showed anincreased activation in various regions of the occipital areaunder hypnosis as well as a less pronounced activation inthe occipital area in the waking state. The ndings are sup-ported by the recent study by Tambiev and Medvedev(2005) using electroencephalography. The authors founda signicant increase in the special synchronisation of brainpotentials in both occipital areas.

    Rainville et al. (1999) examined highly hypnotisableright-handed volunteers using PET. In order to determinethe neurobiological activity in trance, the subtractionmethod was applied. Using this method, the cerebral bloodow under hypnosis was contrasted to the cerebral bloodow in the waking state. Signicantly higher activation lev-els were found on both sides of the occipital lobe. Theseresults support the assumption that a higher level of activa-tion in the occipital area under hypnosis is correlated withan increased use of visual imagination. Spiegel and Kosslyn(2004) postulated the idea, that the order in which the judg-emental characteristics of the frontal lobe aect the occip-ital lobe could be reversed under hypnosis: In hypnotictrance it is easier to transfer verbal messages into innerimages, which causes a change in the perception of reality.These ndings are relevant for a better understanding ofthe construction of reality under hypnosis (Peter, 2001).Perception as well as imagination of visual material haveboth been proven to increase the local neural blood circu-lation in those areas involved with visual processing (forexample Roland and Friberg, 1985). Peter (2001) pointsout a crucial interaction between the plasticity of functionwhich enables our construction of reality and the neural

    478 U. Halsband / Journal of Physequivalent of what is actually perceived, or a construct ofhallucinative imaginary reality. This explains the successof hypnotherapeutic interventions. A therapist can ensurethat hypnotic-suggested sensations are constructed asreal as possible by emphasising the primary sensorymodalities (visual, acoustic, kinaesthetic, olfactory, andgustatory) and by choosing an access which integrates sev-eral sensory modalities.

    In a newer study by Rainville et al. (2002), subjects wereto judge their own level of mental relaxation and absorp-tion immediately after the PET scanning. These judge-ments were then used as an index for the success of thehypnotic trance. All subjects reported a higher level ofrelaxation and absorption under hypnosis. The next stepwas to establish a correlation between the activation ofthe brain and the subjectively perceived relaxation andabsorption. The results can be summarised as follows: (1)relaxation-related activation eects: positive correlationswere shown bilaterally frontal and right occipital in theupper occipital gyrus. Contrary to this, there were negativecorrelations in the right posterior parietal lobe, bilateral inthe mid and inferior temporal as well as in the rightsomato-sensory cortex and the insula; (2) absorption-related activation eects: positive correlation eects werefound in the inferior parietal cortex, in the thalamus andanterior cingulate cortex, bilateral prefrontal and in the leftnucleus lentiformis. Negative correlations were shown inthe left inferior parietal cortex and precuneus as well ason both sides of the occipital cortex. The interesting dichot-omy of a bilateral occipital activation in relaxation-relatedexperimental conditions and a bilateral deactivation inabsorption-related conditions suggest that we are dealingwith two distinct neural mechanisms. It appears that thelevel of subjectively observed relaxation correlates withthe intensity of occipital activation.

    In this PET study, only volunteers with a prior positivetrance experience participated. When questioned, all sub-jects reported that they had perceived the hypnotic tranceas very relaxing, indicating a distinct level of mentalrelaxation.

    A further interesting result of the present PET study wasthe increased prefrontal activation under hypnosis whichwas present during encoding and retrieval. In the pastfew years we have been using methods of brain imagingsuch as PET and fMRI in order to dierentiate the neuralmechanisms involved in encoding and retrieving word-pairassociations in the waking state. We were able to show aninvolvement of the bilateral prefrontal cortex and the ante-rior cingulate cortex during encoding and retrieval of epi-sodic material. In addition, during retrieval a consistentactivation in the medial parietal cortex was shown (Hals-band et al., 1998, 2002; Krause et al., 1999a,b; Mottaghyet al., 1999a,b; Schmidt et al., 2002). The nding of an evenmore pronounced bilateral prefrontal activity duringencoding and retrieval under hypnosis is consistent withthe study of Rainville et al. (1999). The authors reportedan increased activity in the frontal cortex, in the inferior

    gy - Paris 99 (2006) 470482frontal gyri, and in the right anterior cingulate cortex.Additional activations were found in the right anterior

  • iolosuperior temporal gyrus and in the left insula. Maquet et al.(1999) reported left hemispheric changes under hypnosis inthe central, premotor, ventrolateral prefrontal and parietalarea, and signicant increases in the right hemisphere ofthe anterior cingulum.

    Interestingly, from a neurobiological perspective there isa signicant overlap of the circuits which play a decisiverole in attention (Kemna, 2003; Raz, 2005; Raz andShapiro, 2002; Raz et al., 2004; Sturm, 2003) and in impli-cit processing of information (Halsband, 1999; Halsbandet al., 2003). The neural networks which are involved insustained attention (for example when solving classical vig-ilance problems), showed right-sided activity in the ventro-lateral and dorsal frontal cortex as well as in regions of theparietal cortex. Important structures for the alerting orient-ing system are the frontal eye elds, pulvinar, superior col-liculus, temporo-parietal junction, and the superior parietallobe. An important role for executive functions is attrib-uted to the anterior cingulate structures (Raz and Shapiro,2002; Raz et al., 2004). Severals studies have suggested thatconict monitoring involves the anterior cingulate cortex.A typical example of a conict task showing reliable activa-tions in the anterior cingulated cortex is the Stroop testwhere subjects are requested to name the colour of anincompatible coloured word. Using fMRI, Egner et al.(2005) reported that conict-related activity in the anteriorcingulate cortex interacted with hypnosis and hypnotic sug-gestibility. The authors found that highly susceptible sub-jects showed an increased conict-related neural activitypattern. Interestingly, under posthypnotic suggestion toperceive words as nonsense strings highly hypnotisablesubjects showed a pronounced modulation of a decreasedactivity in both the anterior cingulate cortex and the occip-ital cortex (Raz et al., 2005).

    The neural regions involved in implicit learning includethe premotor cortex, the supplementary motor area, cingu-late and parietal regions, basal ganglia, and the cerebellum(Halsband et al., 2003). It is well known that the use ofimplicit knowledge and implicit information processingplay a key role in hypnotherapeutic interventions. Whenusing implicitly learned abilities, some aspects of percep-tion may be separated from the subjects intended voluntaryactions and are subconsciously registered and performed.Thus, hypnosis can have a direct inuence upon dierentaspects of implicit memory. In addition to motor skills,implicit memory tasks include not only motor skills butalso priming tasks, simple associations based on the princi-ples of conditioning, and non-associative learning.

    Focussing and directing of attention are key characteris-tics of a hypnotic induction and are attributed to the fron-tal lobe. Through activation and inhibition the cortexmodulates neural networks on the subcortical level (Fuster,1997). Walter (1992) was able to show an increase of therCBF in the left hemisphere of the superior frontal cortexand in the bilateral inferior areas in individuals with

    U. Halsband / Journal of Physhigh-hypnotic susceptibility. This was accompanied by areduced blood ow in other non-frontal areas. In contrastto this, Gruzelier and colleagues reported an inhibitionin the left prefrontal cortex areas in hypnotic trance(Gruzelier et al., 1998; Gruzelier and Warren, 1993; Kallioet al., 2001).

    The changes in prefrontal activity under hypnosis arealso relevant for our understanding of the neural mecha-nisms of hypnotic dissociation. The advantage of learningunder hypnosis is that irrelevant or disturbing perceptionssuch as pain, emotional components, and interfering visualor acoustic stimuli can be dissociated (Erickson, 1939/1995;Revenstorf and Peter, 2001; Spiegel and Vermutten, 1994).As a neurobiological basis of dissociation, the role of thefrontal executive functions was emphasised (Woody andParvolden, 1998). In this context the function of the frontalcortex should be interpreted as part of a complex neuralnetwork (Kallio et al., 2001). Crawford et al. (1998) arguethat in hypnotic analgesia a supervising attentional systemis activated in the anterior frontal cortex which regulatesthe thalamo-cortical activation through the subcorticalneural network. Rainville et al. (1999) reported that specichypnotic suggestions result in an activation of frontalregions and in alterations of the meaning of perceived stim-uli through top-down processes.

    4.2. Behavioural studies

    First attempts to experimentally quantify learning per-formance in trance can be found among the studies ofGheorghiu (1963, 1973). Gheorghiu (1963) observed animproved recollection of detailed structures in the drawingof animals in several subjects under positive suggestion.Later, Gheorghiu (1973) examined the ability to retrieveobjects in the waking state, in trance, and in autogenictraining. All objects were copied and named before handin the waking state. Results show a better recollection intrance as compared to autogenic training. According toGheorghiu (1973), the increase in amnestic performancein hypnotic trance could be the result of an aectiveunblocking due to hypnotic relaxation (see also Dorcus,1960). Alternatively, the ndings could be interpreted asa more pronounced representation of high-imagery objectsunder hypnosis.

    On a behavioural level, this study was able to show thatthere was an improvement in the recollection of high-imag-ery and dicult to associate word-pairs in trance comparedwith the waking state. This nding occurred in the visualand in the auditory modalities. Thus, for the rst time itcould be shown that an improved transfer of imaginablerepresentations is not specic to one sensory modality.The same learning performance was also observed after a10-min interference. In contrast, the ability to retrieveabstract word-pair associations (easy and dicult experi-mental conditions) strongly decreased when encoding tookplace in trance.

    Our ndings are in agreement with the study by

    gy - Paris 99 (2006) 470482 479Bongartz (1985) in which the eect of hypnotic trance onlearning and recollection was investigated. By means of

  • Jamison, S., Pribram, K.H., 1998. Hypnotic analgesia: 1. Somatosen-sory event-related potential changes to noxious stimuli and 2. Transfer

    iolothe Harvard Group Scale of Hypnotic Susceptibility FormA, six high and six low susceptible subjects were selectedfrom a sample of 45. In each of three experimental sessions,60 tape-recorded high- or low-imagery nouns were pre-sented to the subjects under hypnotic age regression, hyp-notic age progression, and in the waking state. At theend of each session subjects received a recognition listwhich contained the original nouns paired with either anacoustically similar distractor (for example: gunsun,functionjunction) or a semantically similar distractor(for example: shovelspade, thoughtidea). A dierencebetween high- and low-hypnotisables was observed onlyfor the age regression condition in which high-hypnotis-ables made signicantly less errors when a high-imagerynoun was paired with a rhyming distractor during retrieval.It is concluded that highly hypnotisable subjects underhypnosis encode verbal material predominantly in an imag-inable form which leads to better discrimination betweenthe original noun describing the stored image and a similarsounding distractor.

    In our study, only highly hypnotisable subjects showed alearning advantage in trance in the condition with high-imagery and dicult to associate word-pairs in the visualas well as in the auditory experimental conditions. Thelow-hypnotisable subjects however, showed no dierencein their learning ability of high-imagery paired words underhypnosis or while waking. Sweeney et al. (1986) alsoreported a better retrieval of high-imagery word-pairsunder hypnosis. However, unlike our study, no dierencewas reported between learning abstract word-pairs underhypnosis or in the waking state. One of the key problemsin the study by Sweeney et al. (1986) is that the authorsfailed to dierentiate between subjects with high or lowhypnotisability. Thus, the authors reported about a heter-ogeneous subject sample with very dierent trance experi-ences. Crawford and Allen (1996) reported an improvedretrieval of associated word-pairs under hypnosis byhigh-hypnotisables. However, an improved learning eectunder hypnosis was only evident in the within-subjectdesign (examination of the same subjects under dierentexperimental conditions) and not in the between-subjectdesign (examination of dierent subjects under dierentexperimental conditions).

    Interesting in the current study was the nding thathigh-hypnotisables outperformed the low-hypnotisablesubjects also in the waking state. These results coincidewith the ndings of other studies which also reported a bet-ter retrieval of associated word-pairs in subjects with a highfactor of hypnotic susceptibility in comparison to subjectswith low-susceptibility (Crawford and Allen, 1996;Hoen, 1978). In the study by Hoen (1978) high- andlow-hypnotisables were to learn four lists of paired wordseach containing nine word-pairs with dierent levels ofimaginability while in the waking state. High-hypnotisablesshowed a better recollection of high-imagery word-pairs as

    480 U. Halsband / Journal of Physdid low-hypnotisables. This rises the question to whatextent the highly hypnotisable subjects had better learninglearning to reduce chronic low back pain. Int. J. Clin. Exp. Hyp. 46,92132.

    Dorcus, R.M., 1960. Recall under hypnosis of amnestic events. Int. J.Clin. Exp. Hyp. 7, 5761.

    Egner, T., Jamieson, G., Gruzelier, J., 2005. Hypnosis decouples cognitivecontrol from conict monitoring processes of the frontal lobe.Neuroimage 27, 969978.

    Erickson, M.H., 1939/1995. Eine hypnotische Technik fur Patienten mitWiderstand: Der Patient, die Technik, die Grundlagen und Feldex-perimente. In: Rossi, E.L. (Ed.), Gesammelte Schriften von Milton H.Erickson, vol. 1. Carl Auer, Heidelberg, pp. 416461 (Chap. 13).

    Faymonville, M.E., Laureys, S., Degueldre, C., Del Fiore, G.,Luxen, A., Franck, G., Lamy, M., Maquet, P., 2000. Neuralmechanisms of antinoceptive eects of hypnosis. Anesthesiology92, 12571267.

    Frackowiak, R.S., Lenzi, G.L., Jones, T., Heather, J.D., 1980. Quanti-tative measurement of regional cerebral blood ow and oxygenmetabolism in man using 15O and positron emission tomography:theory, procedure and normal values. J. Comput. Assist. Tomogr. 4,727736.

    Fletcher, P.C., Frith, C.D., Grasby, P.M., Shallice, T., Frackowiak,R.S.J., Dolan, R.J., 1995b. Brain systems for encoding and retrieval ofstrategies a priori as compared to the low-hypnotisables.Other authors reported a faster motor reaction time bythe highly hypnotisable subjects (Braman and Kirsch,2001) as well as a higher speed of information processing(Ingram et al., 1979). One distinctive aspect of our studywas the fact that the highly hypnotisable subjects oftenspontaneously transferred the information about thepaired words which were to be learned into a mental image,thus making these easier to learn. However, this strategyapplied only to the learning of high-imagery word-pairsand not to abstract constellations of word-pairs which werenot easily transferred into a mental image.

    In summary, it can be said that highly hypnotisable sub-jects showed an improved processing of high-imagery repre-sentations. The best learning performance was reached byhighly hypnotisable subjects under hypnosis. These resultshave therapeutic implications and are relevant for ourunderstanding of the perception of reality under hypnosis.

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    482 U. Halsband / Journal of Physiology - Paris 99 (2006) 470482

    Learning in trance: Functional brain imaging studies and neuropsychologyIntroductionExperiment 1: Visual word-pair association learningMethodsExperimental subjectsPositron emission tomography imagingExperimental set-up: word-pair association learningAnalysis of data

    ResultsEncoding of high-imagery word-pairsRetrieval of high-imagery word-pairs

    Conclusion

    Experiment 2: Auditory word-pair association learningIntroductionPreliminary test: methodsExperimental subjectsExperimental set-up

    Main study: methodsExperimental subjectsExperimental set-up

    ResultsImmediate reproductionHigh-imagery word-pair associationsAbstract word-pair associations

    Delayed reproduction

    Conclusion

    DiscussionPET studyBehavioural studies

    References