Unedited draft of the article that has been accepted for publication International Journal of Clinical and Experimental

Hypnosis (2001) 49, 95-108.

Anterior brain functions and hypnosis:

A test of the frontal h ypothesis
SAKARI KALLIO1,2, ANTTI REVONSUO 2, HEIKKI HMLINEN 2, AND JAANA MARKELA 2
1 University of Skvde, Sweden 2 University of Turku, Finland

JOHN GRUZELIER
Imperial College of Science Technology and Medicine, London, UK

Abstract Neuropsychological frontal lobe tests were used to compare individuals with high (n = 8) and low ( n = 9) hypnotizability during both baseline and hypnosis conditions. Subjects were assessed on two hypnotic susceptibility scales and a test battery that included the Stroop test, word fluency to letter- and semanticdesignated categories, tests of simple reaction time and choice reaction time, a vigilance task, and a questionnaire of 40 self-descriptive statements of focused attention. Effects for hypnotic susceptibility and hypnosis/control conditions were scant across the dependent variables. High hypnotizables scored higher on the questionnaire at baseline, and their performance on the word-fluency task during hypnosis was reduced to a greater extent than lows. Findings indicate that although the frontal area may play an important role regarding hypnotic response, the mechanisms seem to be much more complex than mere general inhibition.

The definition of hypnosis as a specific state of consciousness with neuropsychological and neurophysiological correlates is controversial. Both hemispheres of the brain have been suggested to be crucial for hypnosis but so far the results have been rather contradictory (Jasiukaitis et al., 1997). The hypothesis of attentional differences between high and low hypnotizable subjects has however been supported by several experiments (for a review see Crawford, 1994). Because neuropsychological studies suggest that the frontal lobe and attentional functions have a close relation (Stuss et al., 1994) it is very tempting to associate frontal lobe functions and hypnosis with one another. Pribram & McGuinness (1975) proposed a model of attention explaining that the prefrontal cortex controls the limbic system in the gating of sensory stimuli arri ving from periphery. The model was supported by Crawford's (Crawford et al., 1993) ERP studies which demonstrated the involvement of the prefrontal cortex in the conscious perception of pain. Crawford's (1993) studies have also revealed an increased cerebral blood flow in the orbitofrontal cortex during hypnotic analgesia, which is interpreted as a sign of increased attentional efforts (Crawford, 1994). On the other hand recent studies using positron emission tomography (PET) to measure regional cerebral blood flow have suggested changes in much wider areas of brain during hypnosis (Maquet et al., 1999; Rainville et al., 1999). Gruzelier (1988; 1990) and Crawford & Gruzelier (1992) have introduced a neuro psychophysiological model of hypnosis based on neuropsychological and

neurophysiological experiments. It is hypothesized that the differences in hypnotizability are partly due to the dissimilar attentional abilities of different individuals. These differences would be seen between lows and highs not only after an induction of hypnosis but also in the nonhypnotic, baseline condition (Crawford et al., 1993). Gruzelier & Warren (1993) have proposed that in highly hypnotizable individuals frontal lobe functions become engaged through instructions of focusing attention during the hypnotic induction procedure. This engagement is followed by inhibition of other typical frontal functions such as reflective consciousness, monitoring, and self-awareness. Norman & Shallice (1986) and Shallice & Burgess (1991) have characterized frontal functions in terms of different control systems. Basic cogni tive operations are carried out in modules controlled by programs called schemata. These schemata are, even when complex, standard and routine. When automatic routines do not produce an appropriate outcome, a general executive component labelled the Supervisory System, controls the function of schemata. It functions by top down activation or inhibition of schemata. The supervisory system can further be fractionated into component supervisory processes which in different ways control the appropriate function of schemata. Stuss et al. (1995) present a new model where this approach is applied to attentional functions and postulate that the control of attention is shown in seven types of tasks: sustaining, concentrating, sharing, suppressing, switching, preparing and the setting of attention. They also suggest anatomical correlates to these tasks fixing them even more closely to the frontal area (Table1). In the present experiment we focused on these attentional differences in the baseline situa tion and on the inhibition of the frontal regions during hypnosis. We chose to focus on three controlling processes of the attentional system: suppressing, concentrating, and sustaining, which were investigated using four different neuropsychological tests. A neuropsychological test where suppressing is required is the Stroop - colour naming task (Stroop, 1935). The subject is presented with stimuli including incongruous features and response to only one feature is required. The task requires the active suppressing of a salient feature which is inappropriate to task requirements. The Stroop effect has been previously studied in association with hypnosis but the results have been somewhat controversial. In some studies hypnosis has led to prolonged reaction times (increased Stroop-effects) in highly hypnotizable subjects e.g. (Sheehan et al., 1988) and in some studies no differences were found in the Stroop-effect in either waking or hypnosis conditions (Kaiser et al., 1997; Nordby et al., 1999) The concentrating of attention is needed when the task is demanding and responses are occurring too quickly rather than too slowly (Stuss et al., 1995). A simple reaction time (SRT) task was included in the battery as a basic test of concentration . A choice reaction time (10-CRT) task was also included since

adding more stimuli and reaction options the task requires also suppressing of the rapid response schema. A third computer task was a typical vigilance task. Sustaining attention is required when the relevant events occur at relatively slow rate over prolonged periods of time (Stuss et al., 1995). Table 1 The neuropsychological Tests (modified from Stuss et al. 1995) Neuropsychological Test Possible Anatomical Basis Dorsolateral Cingulate Cingulate Right frontal Left frontal Left frontotemporoparietal Attentional Task Suppressing Concentrating Concentrating, Suppressing Sustaining -

Stroop Simple reaction time (SRT) Choice reaction time (10CRT) The vigilance task (Vigilance) Fluency to letters (LetFlu) Fluency to categories (CatFlu)

We also added two fluency tasks on the test battery since impairment in generating words beginning with a specific letter has often been described after frontal lobe damage. (Gruzelier & Warren, 1993) reported a reduction in letter fluency task with highly hypnotizable subjects in hypnosis and the absence of the effect with a category fluency task. In this study these tasks were replicated. Table 1 presents the neuropsychological tests used according to which attentional task they engage and their possible anatomical basis according to Stuss et al., (1995). The subjects were also given the Finnish translation of the Different Attentional Processes Inventory (DAPI; Crawford, 1993) which consists of 40 self-descriptive statements about experiences of focused attention and ignoring of distractions, as well as experiences of carrying out two tasks simultaneously. Crawford et al. (1993) found an interaction between hypnotizability and self-reports of extreme, focused attentional skills in which one loses awareness of surrounding environments. This is particularly measured by a subscale of extreme, focused attention on the DAPI. The aim of this study was to test the frontal hypothesis of Gruzelier (1988; 1990) and Crawford & Gruzelier (1992) and to further build connections between theories of attention in cognitive neuroscience and hypnosis. The a priori hypotheses were: a) in the non-hypnotic condition, the highs will perform better than the lows in neuropsychological tests measuring anterior attentional functions; b) following hypnotic induction, the reduction in performance in attentional tests

will be greater for highs than for lows; c) in highs, a reduction following an hypnotic induction will be greater in the generation of letter designated categories than in the generation of semantically designated categories; and d) the highs will obtain higher scores than lows in the DAPI and especially in the subscale measuring extreme, focused attention.

METHOD Subjects Subjects were selected from a pool of 15 highs as defined of scoring 9 to 12 on the Harvard Group Scale of Hypnotic Susceptibility form A (Shor & Orne, 1962) Finnish translation (Kallio, 1996) and 10 lows scoring 0 - 5 on the HGSHS:A. All the subjects were right-handed students (mean age 22.4, SD 0.87 years). These subjects were further tested with the Barber Suggestibility Scale (Barber, 1969; Finnish translation Kallio, 1997). The criterion for inclusion in the study was a BSS score of 13 points or more for highs and 4 points or less for lows and an a appropriate response to an additional challenge test which was carried out together with the BSS 1. Due to the character of the tasks required during the experiment, it was important to assess the extent to which subjects continued to respond hypnotically. This test was used for this purpose during the experiment (see Procedure). A to tal of 19 (out of 25) passed the criteria and participated in the study: 9 highs (3 males, 6 females; HGSHS:A M = 11.2, SD 0.67; BSS M = 14.3, SD 1.3) and 10 lows (2 males, 8 females; HGSHS:A M = 3.0, SD 0.94; BSS M = 2.1, SD 1.2). All subjects gave their informed consent for participation in the study which was described to the subjects as an experiment where the effects of relaxation/hyp nosis will be tested with a battery of neurops ychological tests. Neuropsychological tests The Stroop task In the Stroop task the subjects were given a handout presenting the control stimuli on one side and an identical set of incongruent stimuli on the other side. The subjects were instructed to name aloud as fast as possible the colour of each
1

Because the experiment itself took about 45 minutes to perform, a simple motor inhibition test (not being able to stand up) was chosen for monitoring susceptibility. After finishing the suggestions in BSS, the subject was asked to open his eyes and a motor inhibition test was given: Now you will feel so heavy that you are not able to stand up from the chair no matter how hard you try. After this the suggestion of lightness and ease to move again was given and the subject was asked to try to stand up and sit again. This preliminary test was done twice thus simulating the experiments situation of performing neurops ychological tests between the monitoring of suggestibility.

letter string starting with nonsense xxxx-strings (control) and after that the other side with letter strings including the classical incongruity of the meaning and the colour of the letter strings. The responses of the subjects were tape -recorded and the time required to complete the task was measured. Fluency tasks (LetFlu and CatFlu) In the letter fluency task (LetFlu), the individual letter frequency at the s tart of the word was taken from unpublished computerized norms of Laine & Virtanen (1996) which include 22.7 million word tokens from a major Finnish newspaper. In the first session the subjects were given 90 s per letter category to produce aloud as many words as possible beginning with the letters S (frequency percentage = 8.58), V (freq. % = 7.69) and O (frequency percentage = 7.33) and in the next session the letters M (frequency percentage = 7.94), J (frequency percentage = 7.46) and P (frequency percentage = 7.23). The subjects were instructed not to use human proper names or repetitions of the same word with different suffixes. All responses were tape-recorded. If proper names or repetitions were used they were subtracted from the total score. In the category fluency task (CatFlu), the procedure was the same as in the LetFlu task. Both sets had two category groups: native wild animals and fruits in the first session and foreign wild animals and vegetables in the second session. Reaction time tasks (SRT and 10-CRT) A standard IBM-compatible computer with 486 processor and a colour screen was used to display the stimuli, record the subjects responses and measure the manual reaction times. The stimuli were presented in the centre of the screen with a character size of 5x5 mm. The responses to the target stimuli were recorded to the nearest millisecond. The RT and vigilance tasks were taken from the CogniSpeed software (Revonsuo & Portin, 1995; for earlier studies of these tasks, see Koivisto, et al., 2000). In the SRT test, the number character 0 (zero) appeared in the centre of the screen and the subject was instructed to press the big number key 0 (located in the right-hand side on a standard IBM compatible PC keyboard) with the right index finger as quickly as possible when the stimulus appeared. The stimulus reappeared with a random delay ranging from 1 to 4 seconds. The test contained 40 trials. In the 10-CRT task, the procedure was the same as above except that the number character varied randomly from 0 to 9. The subject was instructed to press the corresponding number key located in the right-hand side on a standard IBM compatible PC keyboard. The interval between the pressing of the button and the next target number was 1 second. The test co ntained 40 trials. The vigilance task (Vigilance) The visual vigilance task is designed to measure sustained attention for a 15minute period. Different letters (5 x 5 mm) were randomly presented on a

computer screen and the subject was instructed to react to a target stimulus by pressing the space bar as quickly as possible. The subjects were given two target letters (letters Y and L), which was 20% of the total amount of stimuli and instructed to keep the right hand on the spacebar and press it as soon the target stimulus appeared. The presentation time of the letters was 200 ms and the interval between the stimuli varied from 300 to 3000 ms. The subjects were also informed that the computer records all correct responses, omissions and false alarms. The number of false alarms, omissions and reaction times served as dependent variables. DAPI- questionnaire The subjects were also given the Different Attentional Processes Inventory DAPI, (Crawford, 1993; Grumbles & Crawford, 1981) which consists of 40 selfdescriptive statements about experiences of focused attention and ignoring of distractions, as well as experiences of carrying out two tasks simultaneously. Subjects are asked to rate themselves as to a degree which they typically carry out activities on a 7-point scale ranging from 1 (not at all) to 7 (always). Crawford (1993) reports test-retest reliability of .90 (a college sample) for 4 weeks; Cronbach's alpha for two testing periods equaled .91 and .94.

Procedure The subjects were pooled into two groups, Groups A (5 highs and 5 lows) and B (4 highs and 5 lows) according to the counterbalanced order of baseline and hypnosis. The test was delivered on two separate sessions with a time interval of one week between the sessions. Both sessions consisted of six different tests which followed each other in the same order. The tests were delivered by two different investigators, one of whom executed the testing in the hypnosis condition (S.K.) and the other in the baseline condition (J.M.). The instructions were the same for all subjects at both times and were read verbatim for each test during both sessions. The study was performed using a 2 X 2 within-subjects crossover experimental design. For Group A the first session began with a 10minute standard induction (S.K.) and after this the subject performed Tasks 1. (Stroop), 2. (LetFlu) and 3. (CatFlu). A sta ndard waking procedure followed and a break of ten minutes was held. After the break the other investigator took over and the subjects performed the computerised tasks 4. (RT), 5. (10 -CRT) and 6. (Vigilance) in a row. The second session was identical except that this time the tasks 1 - 3 were conducted by investigator J.M. After a pause of ten minutes the second half began with the same 10-minute induction by investigator S.K. and tasks 4 through 6 were conducted. For group B the procedure was identical but the sessions were done in the reverse order. The subjects' ability to sustain hypnotic response across tasks was monitored with the motor inhibition test which was performed after each individual test during the sessions where hypnosis was involved. The test was performed first after the

induction procedure and then after each task: 1. (Stroop), 2. (LetFlu), 3. (CatFlu). In the other session continued hypnotic responding was monitored first after the induction and then after tasks 4. (SRT), 5. (10-CRT) and 6. (Vigilance). All highs had to pass this test every time and all lows had to fail the same challenge every time during the experiment. Statistics The data was analyzed with a repeated measurements 2 x 2 x 2 (Condition x Group x Order) ANOVA, with hypnotizability (high vs. low) as a between-subject variable and condition (baseline vs. hypnosis) and test as within-subject variables. Further characterization of differences was done with two -tailed Student's t-tests as appropriate. RESULTS While performing the actual experiment, 1 high and 1 low subject failed the additional motor inhibition test and were excluded from the analysis. The following analyses are therefore based on the remaining 8 high hypnotizables and 9 low hypnotizables. Regarding the order effects, there was a significant main effect when comparing the first and second session with the LetFlu task F(1.15) = 14.3, p < 0.05). This indicated that either the given letter cues were more difficult the first time or that the subjects were more at ease with the test and could come up with more responses in the second session. However, this did not interact with any other factor in the analysis of variance. No other order effects were found. Stroop In baseline the highs and lows performed very similarly in both congruent and incongruent situation. The Stroop interference effect was highly significant in both baseline (F(1,15) = 84.2, p < 0 .001) and hypnosis conditions (F(1,15) = 50.1, p < 0.001.) There was some suggestion that the effect decreased with hypnosis for lows and increased for highs, but the interaction was not significant (F(1,15) = 2.5, p = 0.13). Both groups used more time for the task in hypnosis, both in congruent (F(1,15) = 4.8, p < 0.05) and incongruent trials (F(1,15) = 4.5, p = 0.05).

30 % 20 % 10 % 0% -10 % -20 % -30 % Stroop LetFlu CatFlu SRT 10-CRT Vigilance Vigilance Vigilance RT false alarms omissions 67 46 Highs Lows

Figure 1. The percentage change in relation to baseline condition (- indicates reduction and + indicates improvement) in performance in highs and lows after the induction of hypnosis. Word fluency The ANOVA for the letter task showed a significant main effect for cond ition (F(1, 15) = 7.27, p < 0.05) such that fluency was poorer with hypnosis. This effect was not found for the category task (F(1,15) = 2.79, p = 0.12). There was no main effect of hypnotizability in either letter (F(1,15) = .86, p = 0.36) or category (F(1,15) = 1.2, p = 0.28) tasks. The analysis between hypnotizability and condition revealed a significant difference between highs and lows in the LetFlu task (F(1, 15) = 8.47, p < 0.05) but not in the CatFlu task. Elucidating this further with t-tests disclosed that whereas at baseline highs and lows did not differ (M = 48.7, SD = 10.1 and M = 45.0, SD = 10.2, respectively), hypnosis led to a significant difference between the groups (t(16) = 2.4, p< 0.05) in the direction of poorer letter fluency in high susceptibles. RT tasks In the SRT task there was a main effect for condition (F(1.15) = 9.5, p <0.01) indicating that after instructions of hypnosis reaction times increased for both groups. There was no difference between highs and lows nor was there an interaction between hypnotizability and condition (F(1.15) = 1.5, p = 0.24). In the 10-CRT task there were no significant effects. Vigilance In the Vigilance task the RT:s also increased in hypnosis. The main effect for condition was similar to the SRT task and approached statistical significance (F(1.15) = 4.4, p = 0.054) and there was no interaction between hypnotizability and condition. High susceptibles showed an increase in the amount of omissions in hypnosis (F(1.15) = 3.8, p = 0.069 NS). Though the interaction on omissions did not reach statistical significance, we noted that at baseline highs seemed to make fewer omissions during the 15 minute period (t(16) = -2.4, p < 0.03). It must

be noted that the ANOVA does not allow for group comparison under these conditions. DAPI- questionnaire On the DAPI, the ans wers of highs and lows differed significantly on the whole scale (F(1.15) = 2.4, p < 0.03). DISCUSSION The baseline attentional abilities were measured with four different tasks conceptualized as associated with different attentional abilities: the Stroop test (suppressing ), SRT (concentrating), 10-CRT (concentrating, suppressing), Vigilance (sustaining), as well as with the DAPI questionnaire. With regard to planned analyses, the results indicate that hypnotizability was associated only with the DAPI self-report questionnaire measure. Further, support for a reduction in performance in high susceptibles with hypnosis was found for word fluency to letter designated categories. There was some suggestion in the data that low hypnotizables might be less vigilant, at least in regards to omission errors. In the Stroop task, contrary to hypotheses, the main effect of hypnotizability was not significant in either baseline nor hypnosis condition. Our null results lend no support to the findings of Dixon & Laurence (1992) who inferred that in baseline situation highs showed greater discrepancies between reaction times of congruent and incongruent trials than moderately or low susceptibles. There was however a non significant trend consistent with Sheehan, Donovan, & MacLeod (1988) who found that hypnosis increased the Stroop-effect. These results are also consistent with the results of Nordby et al. (1999), who similarly found a non significant trend indicating that high hypnotizables had shorter reaction times than lows and also significantly more errors in hypnosis. Kaiser et al. (1997) and found no increased Stroop effect in ether waking or hypnotic condition. These results are difficult to compare with one another since studies differ in the way they were performed and how the subjects were selected. Nevertheless it would seem difficult to interpret the effect of hypnosis per se as merely hampering the function of the supervisory system. The verbal fluency task results are consistent with a previous report (Gruzelier & Warren, 1993) regarding both the reduction in letter fluency with high hypnotizables and the absence of the effect with the category task. Generation of word lists with a letter cue has been reported to be maximally impaired after left dorsal lateral or medial fro ntal lobe damage, but not after orbital frontal damage (Benton, 1968). In contrast, word fluency to designated categories may not be as pure a frontal task as it is also impaired with lesions in the temporal and parietal regions, so that if frontal regions are inhibited, compensation may occur from these other regions (Newcombe, 1969). The within-group dissociation in the fluency tasks is also important from the perspective of psychosocial theories of hypnosis. If the result were to be explained by factors like expectancies of the

effects of hypnosis (Kirsch, 1991) it would have been expected to affect both fluency tasks. The results in different studies focusing on neuropsychology / neurophysiology and hypnosis are still quite variable. One of the reasons may be the lack of standardization in the way subjects are selected into these studies. Indeed, the definition of hypnotizability varies significantly with some investigators applying more stringent criteria for group assignment than do others. For example, Gruzelier & Warren (1993) divided a cohort of volunteers into two groups - highs and lows - using the Barber scale. Kaiser et al. (1997) used a scale where the subjects responded to traditional hypnotic challenges. In some studies (Dixon & Laurence, 1992; Weitzenhoffer & Hilgard, 1962), the threshold value for high hypnotizability has been a score of 8 or more on the SHSS:C (Weitzenhoffer & Hilgard 1962) whereas others have used a score of 9 or more on the same scale (Dixon, Brunet, & Laurence, 1990), or 10 or more (e.g. Sheehan, 1988) on the HGSHS:A (Shor & Orne, 1962). The main limitation of this study is its small sample size, and the resulting compromised statistical power. Thus, rigorously testing hypotheses with a minimum probability of type II error is at issue. Relatedly, this study examined only a few subjects over many variables. Thus, when statistical significance did obtain, we must entertain the notion of type I error due to multiple comparison across essentially 10 variables. Hence, Though this study provides some interesting leads, it is most properly understood as a preliminary pass at the notion of something broad and dramatic about fro ntal involvement with hypnosis. Also the understanding of cognitive processes carried out in brain and particularly by the prefrontal cortex is still rather limited. Regions of brain have extensive connections and there are many controversial hypotheses concerning the functions e.g. of the fro ntal lobe (Stuss, Eskes, & Foster, 1994). Thus it is obvious that the so-called frontal tests may be heavily loaded with other nonfrontal processes and there are also regional differences within the frontal lobes. Taken together, we found scant evidence for frontal differences between high and low hypnotizable subjects across 8 indices of functions posited to operate frontally. We did however, confirm that the hypothesized inhibition of frontal functions in high hypnotizable subjects (during hypnosis) was supported by a finding of less verbal fluency to letter designated categories, which is a task suggested to be associated with left dorsolateral area. Some aspects of attention and vigilance show some promise as well. Our results do not support the view that hypnosis and hypnotizability is associated with dramatic and generalized inhibition of frontal lobe functions. Indeed, the frontal lobe may have a more subtle and yet important role in explaining hypnotizability and hypnotic phenomena. But if it does, investigations using more powerful designs, and testing more specific hypotheses are needed.

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