Download frontal functions, connectivity and neural efficiency underpinning

Contemporary Hypnosis
15
Contemp. Hypnosis 23(1): 15–32 (2006)
Published online in Wiley InterScience
(www.interscience.wiley.com) DOI: 10.1002/ch.35
FRONTAL FUNCTIONS, CONNECTIVITY AND NEURAL
EFFICIENCY UNDERPINNING HYPNOSIS AND
HYPNOTIC SUSCEPTIBILITY
John H. Gruzelier
Department of Psychology, Goldsmiths College, University of London, UK
Abstract
An update is provided of an earlier review (Gruzelier, 1998) of the range of evidence for
neurophysiological changes in frontal and lateralized functions with hypnosis, changes
which have differentiated high from low hypnotically susceptible subjects, and which
led to a working model and neuropsychological translation of the hypnotic induction
process. New evidence is outlined from an fMRI/EEG study. This study also disclosed
the importance of neural efficiency in left lateral frontal and anterior cingulate structures,
and their connectivity, for distinguishing high from low hypnotic susceptibility both in
hypnosis and in the everyday state. This amplifies earlier constructs such as cognitive
flexibility. Though the focus will be largely on the alteration of connections with the
anterior brain and its corresponding alterations of function, interhemispheric, posterior
and subcortical connectivity is also considered. The practical implications for the interaction between the hypnotherapist and subject are considered, including stage hypnosis.
Copyright © 2006 British Society of Experimental & Clinical Hypnosis. Published by
John Wiley & Sons, Ltd.
Key words: EEG, fMRI, hypnosis, hypnotic susceptibility, neurophysiology, stage
hypnosis
Neurocognitive changes with hypnosis
Selective inhibition, dissociation and disconnection
Since the time of Janet dissociation has been historically the dominating cognitive theory
of hypnosis (Hilgard, 1965; Bowers, 1992). Now a range of evidence is showing that
following instructions of hypnosis a different and unusual pattern of abilities and disabilities is brought into play in hypnotizable subjects compared with the pre-hypnosis
state. These involve dissociations between cognitive processes, and disconnections
between brain regions together with selective inhibition and enhancement of abilities and
processes (Gruzelier, 1998; 2004). The likening of hypnosis to an inhibitory process is
enshrined in the term hypnosis, itself derived from Hypnos the god of sleep, and initially
made popular by Pavlov’s inhibitory concepts. Early electrophysiological studies found
no evidence of sleep per se (Crawford and Gruzelier, 1992), nevertheless frontal inhibition may represent one dynamic of frontal involvement in hypnosis (e.g. Gruzelier, 1990;
1998; Woody and Bowers, 1994; Woody and Sadler, 1998), and one which may be an
alternative to disconnection, or be in parallel with it. The experimental evidence for
changes in anterior brain activity will be considered in turn.
Copyright © 2006 British Society of Experimental & Clinical Hypnosis
Published by John Wiley & Sons, Ltd
Contemp. Hypnosis 23: 15–32 (2006)
DOI: 10.1002/ch
16 John Gruzelier
Error detection and evaluation
Neurophysiological fractionation of processes, to include possible inhibition, has been
demonstrated between error detection processes and error evaluation processes and with
the apparent inhibition or uncoupling of the latter, both of which are processes emanating
from the anterior cingulate. These processes were measured with event-related potentials
(ERPs) in a Stroop-like conflict task (Kaiser, Barker, Haenschel, Baldeweg and Gruzelier,
1997). The ERPs disclosed a dissociation not evident behaviourally. In the highly hypnotizable participants error detection rates decreased and reaction times (RTs) were prolonged following instructions of hypnosis, as has been reported by others (Nordby
Hugdahl, Jasiukaitis and Spiegel, 1999; Jamieson and Sheehan, 2004). Coincidentally
with the behavioural impairment error detection waves were unaltered, implying that
mistakes in performance were being detected but went uncorrected. But an electrophysiological change did accompany the impaired performance, and this involved the ensuing
positive wave that follows error-related negativity. This ‘error-related positivity’, which is
associated with error evaluation processes, was abolished. In contrast to the apparent
neurocognitive dissociation in the hypnotizable participants, the low hypnotizable group,
acting as a control for the effect of hypnosis, showed no falloff in performance behaviourally following instructions of hypnosis, and no change in their event-related potentials,
which contained both error detection and error evaluation waves. Using ERP source
localization procedures, the processes of error detection and evaluation, as reflected in the
error-related negativity and positivity, have indeed localized to the anterior cingulate.
In sum a neurocognitive dissociation was demonstrated following hypnosis. For while
hypnosis did not interfere with the detection of errors in performance, hypnosis did
interfere with the deeper processing of the errors, theorized to give rise to a falloff in
behavioural performance shown by the slow RTs. This dissociation may reflect either
inhibition/deactivation or disconnection. The psychological dissociation with hypnosis
has features in common with the dissociation implicit in Hilgard’s demonstration of a
hidden observer. Here pain analgesia is experienced, yet simultaneously the subject can
rate the intensity of the administered pain.
As an incidental finding, in the same experiment during hypnosis an alteration specific
to the hypnotizable subjects was found in EEG alpha coherence in the left frontal lobe
(Gruzelier, 1998). This will be seen to have parallels in the recent fMRI/EEG study.
Pain and hypnotic analgesia
The anterior cingulate has also been implicated in the underpinning of hypnosis-induced
analgesia (Faymonville, Laureys, Degueldre, DelFiore, Luxen, Franck, Lamy and Maquet,
2000; Rainville, Duncan, Price, Carrie and Bushnell,, 1997; Rainville, Hofbauer and
Paus, 1999; Derbyshire, Whalley, Stenger and Oakley, 2004), as we have demonstrated
electrophysiologically (Croft, Williams, Haenschel and Gruzelier, 2002). Here ‘inhibition’ as an explanatory concept can be ruled out. In response to painful stimuli we
examined fast frequency 40 Hz gamma oscillations in view of their putative role in
underpinning conscious perception (e.g. Tallon-Baudrey and Bertrand, 1999). In keeping
with this evidence the magnitude of frontal gamma oscillations in the pre-hypnosis state
was found positively correlated with the intensity of the affective response to pain.
However, following instructions of hypnosis, while the relation was retained in those
with low hypnotizability, the relation no longer held in those with high hypnotizability.
In other words outside of hypnosis the greater the distress experienced by the pain
stimuli, the higher the amplitude of the gamma oscillations, whereas during hypnosis
distress was unrelated to the magnitude of the gamma oscillations.
Copyright © 2006 British Society of Experimental & Clinical Hypnosis
Published by John Wiley & Sons, Ltd
Contemp. Hypnosis 23: 15–32 (2006)
DOI: 10.1002/ch
Frontal connectivity and hypnosis 17
Application of low resolution source localization methodology (LORETA) confirmed
that the generation of the gamma oscillations arose from the midline anterior cingulate,
in keeping with the extensive literature on the subjective distress of pain and this frontal
structure. Of theoretical importance was the finding that the magnitude of the gamma
oscillations was unchanged, indicating no change in arousability/activation per se. The
results support a selective dissociation with hypnosis of frontal and anterior cingulate
processes from somatosensory cortices, without alteration in anterior activation levels;
in other words with no evidence of inhibition.
Voluntary auditory attention
In an auditory attention task, with recording of frontal and parietal ERPs, an accumulation of anterior inhibitory processes was disclosed with the course of hypnosis in hypnotizable subjects (Gruzelier, Gray and Horn, 2002). Specifically, from the prehypnosis
baseline to early and later stages, over 40 minutes of hypnotic induction, the hypnotizable
participants showed a progressive reduction of attention related negativity (N100) in
frontal electrodes. These dynamics were not paralleled by changes in subsequent cognitive memory-related components (P300), nor were they found in parietal recordings. This
provided further evidence of regional changes and/or dissociated changes in hypnotizable subjects. We note that bilateral attenuation of the N100 difference wave is characteristic of frontally lesioned patients, whether or not the lesion is lateralized.
Interestingly in subjects with low hypnotic susceptibility the N120 was negligible in
their pre-hypnosis baseline, and became progressively larger with hypnosis. This was
the opposite result to the one seen in hypnotizable subjects. The fact that both low and
high hypnotizable groups undergo changes with hypnosis, but often in opposite directions, was disclosed in a previous study, now considered.
Automatic auditory attention
The concept of inhibition was introduced in our first study of hypnosis published two
decades ago (Gruzelier and Brow, 1985). This involved electrophysiological recording
of orienting and habituation processes to novel tones interspersed with the induction of
hypnosis. Orienting responses were recorded with electrodermal activity, a pure measure
of sympathetic autonomic responsiveness. Highly susceptible subjects showed a reduction in responses with hypnosis when compared with several control conditions, whereas
subjects with low susceptibility showed increased responding, the opposite effect. At the
same time both groups shared evidence from other autonomic parameters of attentional
engagement. In the subjects with low hypnotizability reverse effects were found with
more orienting responses and slower habituation, a pattern which is in keeping with
enhanced sustained attention as may occur with apprehension. The facilitation of habituation with hypnosis in hypnotizable subjects was then replicated in an experiment
designed to compare hypnosis with simulating hypnosis in subjects with medium/high
hypnotizability (Gruzelier, Allison and Conway, 1988).
Critical central influences on autonomic orienting responses include frontal modulatory connections of the orbitofrontal and dorsolateral cortices with the limbic system,
particularly the amygdala and hippocampus. The amygdala has been shown to exert
mainly excitatory influences on orienting activity whereas the inhibitory action of the
hippocampus facilitates the habituation (inhibition) of the orienting response with stimulus repetition (e.g. Gruzelier and Venables, 1972; Pribram and McGuinness, 1975; Gray,
1982). Accordingly the highly hypnotizable group showed evidence in line with reduced
orbitofrontal-amygdaloid excitatory influences on responding and increased dorsolateralCopyright © 2006 British Society of Experimental & Clinical Hypnosis
Published by John Wiley & Sons, Ltd
Contemp. Hypnosis 23: 15–32 (2006)
DOI: 10.1002/ch
18 John Gruzelier
hippocampal inhibitory influences. The influence of hypnosis on electrodermal orienting
and habituation was compatible with the neuroanatomical evidence of De Benedittis and
Sironi (1988) arising from recordings of intracranial electrical activity obtained during
hypnosis. They found that hypnosis involved functional inhibition of the amygdala and
activation of the hippocampus.
We also found evidence of shifts in hemispheric influences as a result of hypnosis in
the hypnotizable subjects now considered.
Hemispheric asymmetry as a dynamic in dissociation and disconnection
Electrodermal orienting response asymmetries
In the orienting response study above, electrodermal activity was recorded bilaterally to
investigate hemispheric influences (Gruzelier, Brow, Perry, Rhonder and Thomas, 1984).
Despite the attenuation in responding occurring with hypnosis, a reversal in asymmetry
in orienting response amplitudes could be detected when compared with the neutral
condition. With hypnosis right hemispheric frontolimbic influences predominated in
highly susceptible subjects.
Outside of hypnosis hypnotizable subjects were also asymmetric, in fact in the course
of stimulus repetition they showed a shift from an initial right-sided preference, in line
with the right hemisphere’s role in global orienting, to a left hemispheric preference, in
line with left-sided involvement in the local orienting process. This dynamic was compatible with the putative flexibility of hypnotizable subjects in their neurocognitive processing abilities, as outlined below. In those with low susceptibility there was no reliable
asymmetry in either condition. In other words hypnosis produced a shift in the activational balance of fronto-limbic influences to favour the right hemisphere.
Ideational fluency
The first clear neuropsychological finding of left frontal involvement in hypnosis involved
delineation of dissociations between three neuropsychological tests of ideational fluency.
These were selected to differentiate between anterior left and right hemispheric functions
and also within the left hemisphere to delineate between anterior dorsolateral and temporal functions (Gruzelier and Warren, 1993). The results disclosed an imbalance in
dorsolateral prefrontal functions, an imbalance that disadvantaged prefrontal left hemisphere processes (indexed by word fluency to letter designated categories), and favoured
anterior right hemisphere processes (indexed by fluency for designs). At the same time
left temporal functions (indexed by fluency for words belonging to semantic categories)
remained activated. The latter result would follow the necessary left temporal word
comprehension abilities required in listening to the verbal induction; though with practice these might be given over to rudimentary right hemispheric comprehension abilities
(Gruzelier, 1998).
This differential pattern between the two types of verbal fluency generation was
replicated by Kallio et al. (2001). They also found that the reduction in fluency correlated
positively with hypnotic susceptibility, and also with interference on the Stroop conflict
task, a task also shown to involve anterior functions to include the anterior cingulate
(Botvinik, Nystrom, Fissell, Carter and Cohen, 1999).
These unique patterns of neuropsychological abilities and disabilities between cognitive abilities could not be anticipated by social factors including expectation or task
demands, explanations favoured by some theorists, nor were they part and parcel
of normal functioning, all of which rules out an explanation based on expectancy.
Expectancy theory could not have predicted the dissociation between the three tests
Copyright © 2006 British Society of Experimental & Clinical Hypnosis
Published by John Wiley & Sons, Ltd
Contemp. Hypnosis 23: 15–32 (2006)
DOI: 10.1002/ch
Frontal connectivity and hypnosis 19
(Gruzelier, 2000a) and the focal inhibition/deactivation of the left prefrontal ideational
process.
Haptic discriminations
Lateral functional shifts with hypnosis have been demonstrated in somatosensory processing in a total of three investigations. Here reductions in left hemispheric haptic processing times coincided with enhancements in right hemispheric processing (Gruzelier
et al., 1984; Cikurel and Gruzelier, 1990), and in the first experiment the degree of reduction in the left hemispheric processing time correlated with the depth of hypnosis. It was
also the case that the hypnotizable subjects had superior left than right hemispheric discriminations in the prehypnosis state.
One of the follow-up experiments (Cikurel and Gruzelier, 1990) contained the activealert hypnosis procedure of Banyai and Hilgard (1976) with participants pedalling a stationary bicycle with instructions of mental invigoration. The demonstration of the
hemispheric shift in activation while pedalling precluded an explanation of the lateral
shift based on a nonspecific factor such as relaxation. Deep relaxation measured by
sensory reduction in a floatation tank while producing right hemispheric haptic enhancement, was without the simultaneous reductions (inhibition) in left hemispheric haptic
abilities (Raab and Gruzelier, 1994), found with hypnosis. Thus relaxation is an important component but cannot account for the left anterior inhibitory effects of hypnosis.
Brightness discrimination
Hemispheric asymmetry of function in visual processing in hypnosis was examined
using a standard divided visual-field apparatus in which flashes of light of varying brightness were presented in the peripheral visual fields (McCormack and Gruzelier, 1993).
Following instructions of hypnosis an enhancement of right hemispheric perceptual
sensitivity for brightness discriminations (the d prime psychophysical metric derived
from signal detection theory) was found in highly susceptible subjects. On the other hand
left hemisphere sensitivity remained unchanged, and therefore was seen to be independent/dissociated from the right hemisphere. Cognitive confounds were excluded because
there was no corresponding hemispheric dissociation in the psychophysical index of
cognitive influences on perception (beta).
Interestingly comparisons of the highly hypnotizable subjects with those with medium
levels of susceptibility indicated in the latter an increase in perceptual sensitivity which
was bilateral. Bilateral enhancement would be consistent with a less focal enhancement
of posterior processes with hypnosis. This result was also found in the previous haptic
sorting study in participants with moderate levels of hypnotic susceptibility (Cikurel and
Gruzelier, 1990).
Tone probe ERPs
Cortical evoked potentials (ERPs) were recorded to tone probes from electrodes placed
over the anterior temporal lobes bilaterally at T3 (left) and T4 (right). This probe strategy
enables cortical activation patterns to be assessed during concurrent tasks. The tone
probes were presented simultaneously either with a hypnotic induction or a story read
by the hypnotist, or were presented in a neutral baseline condition. The temporal electrode placements were compared with central electrode derivations (C3,4), and the two
tasks were referred to the baseline where there was no cognitive task (Jutai, Gruzelier,
Golds and Thomas, 1993). In participants with medium/high susceptibility the N100
attentional wave to the tones disclosed greater right temporal responsivity (T4) following
Copyright © 2006 British Society of Experimental & Clinical Hypnosis
Published by John Wiley & Sons, Ltd
Contemp. Hypnosis 23: 15–32 (2006)
DOI: 10.1002/ch
20 John Gruzelier
the induction of hypnosis, whereas the expected left temporal advantage (T3) was shown
when listening to the control story. In contrast participants with low hypnotizability
showed the left-sided preference to both the story and hypnosis.
The results demonstrated a lateral advantage in favour of right anterior temporal lobe
activity specific to the more hypnotizable participants with hypnosis, suggestive of a
right hemispheric processing of the hypnotist’s message, relying on the more rudimentary right hemispheric comprehension abilities. The group with low hypnotizability
exhibited left anterior temporal activation, which did not distinguish between the hypnosis and story conditions, and was congruent with left hemispheric preference for verbal
comprehension.
Neural efficiency and individual differences in hypnotic susceptibility
The thesis is developed elsewhere (Gruzelier, 2002a) that hypnotizability has many
advantages, aside from susceptibility to hypnosis, and these stem from the putative
underpinnings of neurophysiological and cognitive flexibility/efficiency. Evans (1991)
has reviewed two decades of his research on the theme of flexibility. He has related
hypnotizability, inter alia, with the facility for random number generation, and the flexible control of sleep (Evans and Graham, 1980). He reported that the ability to respond
to suggestion in sleep in the REM phase correlated positively both with hypnotizability
and with the facility for falling asleep in the laboratory; a phenomenon which signifies
the ability for dissociative control outside of awareness and volition.
Crawford (1989) and Crawford and Gruzelier (1992) used cognitive flexibility as an
explanatory construct when reviewing cognitive and neurophysiological findings that
have differentiated high from low hypnotic susceptibility. These included task-related
hemispheric specificity found only in highly susceptible subjects independent of hypnosis, along with functional neuropsychophysiological changes as a result of hypnotic
instructions. Similarly the ability to prime wider networks of association between cortical representational networks has been theorized to be associated with both hypnotizability and hypnosis (Shames and Bowers, 1992). The cognitive, affective and
neurophysiological flexibility of the hypnotizable participant includes superior abilities
in absorption, creativity, dissociation, attention and vividness of imagery; these are all
well known correlates of hypnotizability (Gruzelier, 2002a, 2006). Recent evidence
includes adaptive advantages for protection against cardiac hazard (Santarcangelo and
Sebastiani, 2004).
The experiments that have been outlined in the previous sections disclosed several
examples of differences between hypnotizability groups in control conditions without
hypnosis. Highly hypnotizable participants had superior left hemispheric haptic sorting
ability (Gruzelier et al., 1984) and word fluency (Gruzelier and Warren, 1993), and
exhibited hemispheric cognitive congruency in an apparent shift from global (right
hemisphere) to local (left hemisphere) orienting processes (Gruzelier et al., 1984).
Perhaps most striking of all was the difference in the ERP N100 attentional component
across the frontal chain in the auditory detection task (Gruzelier et al., 2002). This component was augmented in highly hypnotizable subjects, reflecting the engagement of
focussed attention processes, whereas it was virtually absent in those with low hypnotizability, as would occur with the failure to engage frontal attentional circuits which may
follow distraction. In line with the frontal model of hypnosis the N100 attention wave was
progressively attenuated in hypnotizable subjects with the course of hypnosis, and as
would occur with disengagement of frontal processes. In those with low hypnotizability
Copyright © 2006 British Society of Experimental & Clinical Hypnosis
Published by John Wiley & Sons, Ltd
Contemp. Hypnosis 23: 15–32 (2006)
DOI: 10.1002/ch
Frontal connectivity and hypnosis 21
the N100 attention wave progressively increased, as would occur with progressive engagement of attention. A similar increase in responsiveness was also shown in the electrodermal orienting responses of those with low hypnotizability (Gruzelier and Brow, 1985),
whereas responses were attenuated with hypnosis in hypnotizable subjects. These group
characteristics led to predictions about BOLD measurements in fMRI now described.
Conflict monitoring with fMRI and EEG
But first to consider the dynamics of blood flow oxygenation and cognitive processing and
their implications for individual differences. As will be seen this largely overlooked issue
has somewhat discomforting implications for the field of brain localization with fMRI and
PET. For essentially the more efficient the cognitive processing is, the less the oxygenation
requirement. With learning activation decreases, so that the greater the learning and the
higher the intelligence the greater the decrease in activation, especially in frontal brain
regions associated with reasoning (Haier, Siegel, Maclachlan, Soderling, Lottenberg and
Buchsbaum, 1992a; Haier, Siegel, Tang, Abel and Buchsbaum 1992b; Duncan, Seitz,
Kolodny, Bor, Herzog, Ahmed, Newell and Emslie, 2000; Gray and Thompson, 2004;
Neubauer, Grabner, Freudenthaler, Beckman, Guthke, 2004). In other words the more
intelligent brain requires less metabolism and consequently is less likely to show fMRI
activation. One implication for fMRI studies in general is that one cannot be certain that
less intelligent/efficient brains will process in the same way as less intelligent/efficient
brains so that regions utilized for processing in the former may go undetected.
Notwithstanding, the clear implication here is that when considering the flexibility
hypothesis, less activation will be predicted at baseline in participants with high hypnotizability than in those with low hypnotizability.
We investigated conflict monitoring with a Stroop-like interference task while subjects were scanned with fMRI and while their EEG was recorded in a separate session
(Egner, Jamieson and Gruzelier, 2005). In both sessions we successfully demonstrated
the Stroop conflict effect on behavioural performance and found that in line with other
evidence (Carter, MacDonald, Botvinick, Ross, Stenger, Noll and Cohen, 2000; MacDonald, Cohen, Stenger and Carter, 2000; Botvinik, Cohen and Carter, 2004) the conflict
task involved the anterior cingulate (ACC), which increased in activation with increasing
levels of conflict monitoring. At the same time (with high levels of conflict), a cognitive
control centre in the left lateral frontal cortex (LPC) was engaged (MacDonald et al.,
2000). There were two main fMRI hypnosis findings disclosed by a significant Group
x Session interaction in the blood oxygenation ACC response. In hypnotizable subjects
there was an increase in ACC activation from baseline to hypnosis, and this was to a
higher level than found in subjects with low hypnotizability in whom there was a nonsignificant decrease in activation. There was also a weak tendency for those with low
hypnotizability to have higher activation at baseline (p < 0.13). In other words the highly
susceptible subjects were compromised by hypnosis, whereas those with low hypnotizability tended to improve, perhaps due to practice. These differential changes have a
counterpart with our auditory discrimination ERP study (Gruzelier et al., 2002).
It was also the case that the ACC compromise with hypnosis was not paralleled by
compromise in the LFC (left inferior frontal gyrus) region that is associated with cognitive control and is activated significantly more in the higher difficulty level conditions.
In other words there was no commensurate increase in blood oxygenation in the hypnotizable subjects in the LFC as had occurred in the ACC, a result representing an uncoupling or dissociation between the ACC and LFC with hypnosis. This interpretation was
Copyright © 2006 British Society of Experimental & Clinical Hypnosis
Published by John Wiley & Sons, Ltd
Contemp. Hypnosis 23: 15–32 (2006)
DOI: 10.1002/ch
22 John Gruzelier
borne out by EEG recordings during the same task in a separate session. EEG coherence
measures indicated that following instructions of hypnosis, what characterized the highly
susceptible subjects was a reduction in connectivity between the anterior cingulate and
the left dorsolateral prefrontal cortex (F3), as reflected in the gamma rhythm coherence,
with the converse effect in those with low susceptibility. There was no such interaction
between group and session in the corresponding right homolateral site (F4). This evidence assists in clarifying the nature of the alteration in frontal functions with hypnosis.
The left inferior frontal locus that was activated in this investigation has been implicated
in contention scheduling, and contextual control processes including associating external
cues with appropriate actions (Passingham, Toni and Rushworth, 2000; Shallice, 2002;
Koechlin, Ody and Kouneiher, 2003). This underscores the disruption of executive functions with hypnosis through disconnectivity.
In a separate analysis, as presented at the British Association meeting, baseline differences between the groups emerged clearly, as shown in Figure 1. Blood oxygenation
level-dependent (BOLD) responses to different levels of response conflict were assessed
by random effect analyses comparing event-related activation in moderate versus low
conflict trials (moderate conflict contrast), and in high versus low conflict trials (high
conflict contrast), excluding error trials. Based on previous studies, the analyses were
carried out for a priori regions of interest covering the ACC (Brodmann areas 24 and
32) and the left dorsolateral prefrontal cortex (Brodmann area 9). Following the report
of Macdonald et al. (2000) moderate response conflict conditions activated cingulate and
medial frontal gyri while the high response conflict contrast resulted in cingulate activation, and additionally activation in left superior, middle and inferior frontal gyri. These
contrasts were analysed in the hypnotic groups separately. Clear differences in conflictrelated attentional processing emerged. At baseline, in the low susceptibility group both
moderate and high conflict elicited substantial activation in both regions, whereas in
highly susceptible participants the moderate conflict contrast did not result in any significant activation, and the high conflict contrast only produced limited cingulate activation. As above with hypnosis these patterns of conflict-related processing were reversed.
Thus, without group differences in behavioural performance levels, highly susceptible
participants were characterized by a higher efficiency of executive attention than participants with low susceptibility at baseline, and by relatively impaired executive function
in the hypnotic state.
Neuropsychological translation of the classical induction of hypnosis
The earlier findings with hypnotic relaxation led to a neuropsychological translation of
the nature of hypnosis as induced by the conventional procedure aimed at producing a
state of relaxation (Gruzelier, 1988, 1990, 1998). It is important to note that for the main
part in our studies we have deliberately avoided active challenges, which must provide
an added level of complexity in elucidating fundamental processes in hypnosis, let alone
the stunts involved in hypnosis for entertainment. Accordingly our hypnotic relaxation
may be thought of as akin to what has been termed ‘neutral hypnosis’. As will be seen,
anterior brain functions represent a cardinal region in the induction of the hypnotic
process, and in accounting for the character of the hypnotic susceptibility trait.
A three-stage working model of the induction process was evolved:
The first stage involves the traditional instructions to fixate on a small object and to
listen to the hypnotist’s voice. Here was posited an attentional network including thalamocortical systems and parietofrontal connections to engage a left anterior focussed
Copyright © 2006 British Society of Experimental & Clinical Hypnosis
Published by John Wiley & Sons, Ltd
Contemp. Hypnosis 23: 15–32 (2006)
DOI: 10.1002/ch
Frontal connectivity and hypnosis 23
Figure 1. High conflict BOLD responses in low and high hypnotically susceptible subjects, at
baseline and in hypnosis. (A) Brain activation (Talairach x = 6, z = 35) in ROIs in high conflict
trials at baseline for low (left panel) and high (right panel) hypnotizability participants. (B) Brain
activation (Talairach x = 6, z = 35) in ROIs in high conflict trials in hypnosis for low (left panel)
and high (right panel) hypnotizability participants. Activity is displayed at FDR = 0.05 with an
extent threshold of at least eight contiguous voxels, superimposed on a single subject MNI T*1
scan supplied with SPM99.
attention control system. This underpins the focussed, selective attention that is inherent
in visual fixation and listening to the hypnotist’s voice. Together these processes require
left hemispheric frontotemporal processing.
The second stage replaces eye fixation with eye closure, suggestions of fatigue at
continued fixation, and tiredness together with deep relaxation. It is posited that this sets
in motion frontolimbic inhibitory processes with dissociative or uncoupling consequences, left-sided in particular, encompassing orbitofrontal and dorsolateral frontal
regions and limbic structures such as the amygdala, hippocampus and cingulate. These
underpin the suspension of reality testing and critical evaluation, and the handing over
of executive and planning functions to the hypnotist; in other words the ‘letting go’
component of the hypnotic induction. This letting go is accompanied by a lateral shift
towards a right hemispheric preference.
The third stage involves instructions of relaxed, passive imagery leading to a redistribution of functional activity and an augmentation of posterior cortical activity, particularly of the right hemisphere in the highly susceptible subjects. Simplifying the verbal
Copyright © 2006 British Society of Experimental & Clinical Hypnosis
Published by John Wiley & Sons, Ltd
Contemp. Hypnosis 23: 15–32 (2006)
DOI: 10.1002/ch
24 John Gruzelier
content of the induction message may also facilitate right hemispheric processing as does
emphasizing past experience and emotion.
The participants with low susceptibility in contrast fail to show engagement of left
frontal attentional control mechanisms, or if there is focal attentional engagement, the
subject with low susceptibility fails to undergo the ‘inhibitory’, letting go process.
Accordingly this provides two reasons for ostensibly willing subjects not to undergo
hypnosis. The retarded habituation of orienting responses to stimuli irrelevant to hypnosis is consistent with vigilant, broad attention or distractibility, and slow habituation
occurs with anxiety (Gruzelier and Phelan, 1991). Letting go requires reassurance about
the lack of unwanted consequences of hypnosis, such as a loss of control or failure to
come out of hypnosis, which may preoccupy naïve subjects. We have theorized that the
alleviation of these worries may account with practice for evidence of focusing of attention, and through practice with self-hypnosis allow benefits such as natural killer cell
enhancement (Gruzelier, 2002b).
In sum the ‘letting go’ stage, which is cardinal to hypnosis, is underpinned by the
selective inhibition or disconnection of frontal functions from posterior and subcortical
functions, leading to the giving over and the placing of the executive and planning functions under the hypnotist’s influence, to suspension of critical evaluation and reality
testing, as well as to alterations in the control of the supervisory attentional system
(Gruzelier, 1990, 1998; Crawford and Gruzelier, 1992; Woody and Bowers, 1994; Woody
and Sadler, 1998). Oakley et al. (personal communication) investigating this three-stage
temporal process for depth of hypnosis in an fMRI scanner confirm the impact of the
‘letting go’ stage for increasing the depth of hypnosis.
A neurophysiological theory of altered top-down influences in stage
hypnosis
The author has proposed that frontal functions are fundamental to the stage hypnotist’s
persuasion (Gruzelier, 2000b, 2004). The thesis began with a landmark neuropsychological case of an alteration in personality through a brain lesion. In 1848 Phineas
Gage, a railway artisan working on the trans-Canadian railway, suffered a devastating
insult to the head following a dynamite explosion which drove an iron bar through his
cheek on a trajectory through the frontal cortex. After the accident the socially abiding
and popular worker displayed extraverted, nefarious, impulsive and profane behaviour,
making decisions against social convention and contrary to his best interest. Having
undergone a change of personality and character he ended his life as a fairground
sideshow (shades of the appeal of stage-hypnosis). Reconstruction with MRI from
photographic images of the skull has confirmed that it was the ventromedial or orbital
aspects of the frontal cortex that were damaged (Damasio, 1994). It should be emphasized that the damage was definitely not on a par with anything as pronounced as frontal
lobotomy
The Damasios undertook a programme of research on patients with damage to the
ventromedial prefrontal cortex. They contrived a task that simulated real-life decision
making while leaving intellectual functions unaffected. Patients were guided only by
immediate prospects, and were oblivious to the consequences and positive or negative
affective value of their future actions (Damasio, 1994; Bechara, Damasio, Damasio and
Anderson, 1994; Bechara, Tranel, Damasio and Damasio 1996; Bechara, Damasio,
Tranel and Damasio, 1997; Bechara, Damasio, Damasio and Lee, 1999; Bechara, Damasio
and Damasio, 2000). Furthermore the patients continued to behave disadvantageously
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Frontal connectivity and hypnosis 25
after being made aware of the consequences of their actions (Bechara et al. 1997; Bechara
et al. 1999). From simultaneous recordings of autonomic electrodermal activity an
absence of anticipatory responses was disclosed, and was interpreted as an unavailability
of emotionally related knowledge with which to inform decision making in social situations. This led to a ‘somatic marker’ hypothesis, which, inter alia, proposed that a deficiency in affect and feeling in anticipation of action played a critical role in impaired
decision making about the future actions of frontal patients (Damasio, 1994). It is the
ventromedial prefrontal cortex which processes the association between behavioural
outcome and the corresponding emotional outcome, an association contained in a dispositional rather than an explicit form. The emotional somatosensory image, via reactivation of a somatic memory, marks the potential outcome of actions as either positive or
negative. In other words, it is not that the patient with medial frontal damage cannot
experience and express emotion, as hypothesized to be the case in psychopathy or in the
syndrome belle indifference: the patient does feel emotion, but there is a failure to adjust
behaviour according to past experience, because the feelings based on past experience
are no longer engaged. Accordingly there is a reliance on the immediate advantage as
opposed to the future advantage, which can no longer be predicted accurately (Schoenbaum et al. 1998), and this appraisal is particularly faulty in unpredictable circumstances.
Social behaviour is disrupted, and ‘previously well adapted individuals become unable
to observe social conventions, and unable to decide advantageously on matters pertaining
to their own lives’ (Bechara et al., 2000:295).
This may be extrapolated to hypnosis, with its inherent selective suppression or disconnection of selected frontal functions, including orbito-frontal-amygdaloid connections, as shown in our electrodermal orienting response studies (Gruzelier and Brow,
1985; Gruzelier et al., 1988), and extending to the orbital frontal cortex (OFC) and its
connections with the conflict monitoring capabilities of the anterior cingulate. Relevance
to an understanding of stage hypnosis becomes apparent. On stage the hypnotically susceptible subject responds without embarrassment to the immediate contingencies, i.e. the
instructions of the hypnotist to enact behaviour typically making the subject appear a
fool, in order to provide entertainment for the audience. Furthermore the participant
persists in doing so even though cognitively aware, just as is found in the OFC lesioned
patient. Accordingly, what is missing in the stage hypnosis participant is the association,
based on past experience, of the emotional consequences of the actions instructed by the
hypnotist, such as emotional appraisal of likely humiliation. Behaviour is governed by
the immediate context, i.e. the instructions of the hypnotist. Negative consequences can
no longer be predicted.
Thus neuropsychology of altered frontal functions, including selective disconnection,
may offer an explanation for the attraction of hypnosis for entertainment. An explanation
for why subjects allow themselves to be made a fool of, to suffer humiliation without
embarrassment, often appearing to have undergone a personality change, and so to
provide the necessary theatrical display to maintain the popularity of stage hypnosis with
the general public, now chiming with the cultural appetite for ‘reality’ entertainment.
Orbitofrontal cortex, right hemisphere and the therapeutic relationship
Lateralized functional alterations leading to right hemispheric preferential activation
were found to be an important dynamic of hypnosis, as outlined here, while for a review
of earlier evidence see Crawford and Gruzelier (1992). The orbital and medial frontal
cortex, theorised to play a role in stage hypnosis, has a special relationship with the right
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26 John Gruzelier
hemisphere. As Cavada and Schultz (2000:205) concluded in the foreword to an issue
devoted to the orbital frontal cortex in the journal Cerebral Cortex, ‘The orbitofrontal
cortex is involved in the critical human functions, such as social adjustment and the
control of mood, drive and responsibility, traits that are crucial in defining the ‘personality’ of an individual.’ This region exerts the highest level of control over emotional behaviour, by virtue of having the only direct cortical connections with the amygdala,
hypothalamus, and brain stem reticular activating system. This region, which is anatomically larger in the right hemisphere, takes executive control over the right hemisphere per
se, and bilateral executive control of the limbic system and autonomic nervous system.
The right hemisphere matures earlier than the left, and is dominant for the attachment
process between mother and infant (Schore, 1994). Attachment involves the regulation
of biological synchrony between people and transactions, which mediate the social
construction of the brain for which the right hemisphere is dominant. The right hemisphere also has functional advantages for the control of attention and emotion, prosody
and facial recognition, unconscious processes such as implicit memory and preattentive
facial emotions, as well as the representation of somatic and visceral states and selfrelated material through its control over the limbic and autonomic nervous systems (e.g.
Hugdahl, 1995; Pizzagali, Regard and Lehmann, 1999; Keenan, Wheeler, Gallup and
Pasual-Leone, 2000).
In therapy, just as in studies of the empathetic processes between the intuitively
attuned mother and her infant, the affective synchrony is often nonverbal. Resonance is
with affective bodily states, rather than being cognitive in nature (Schore, 1997). This
spontaneous communication is mediated by the right-sided limbic system (Buck, 1994),
which as shown in our limbic-mediated electrodermal recording becomes dominant in
hypnosis (Gruzelier et al., 1984). The empirical results showing the shift of functional
activity to advantage the right hemisphere with conventional hypnotic relaxation, support
the well known clinical experiences and metaphors of access to right hemispheric processes with hypnosis (Pedersen, 1984)).
Thalamo-cortical functions
More than 70% of thalamocortical connections are with anterior cortex. This facilitates
the frontal lobe’s executive functions in playing a moderating role throughout the cortical
mantle as well as subcortically through the limbic structures and the brainstem. This
gives rise to wider implications for frontal influences on behaviour in hypnosis. The
release of functions from frontal inhibitory control may not only enhance posterior brain
activity but also release subcortical activity. Thalamo-cortical connections, and especially prefrontal connections, are central to consciousness circuits (Zeman, 2002). These
are directly involved in the alterations of consciousness experienced in hypnosis
(Rainville et al. 2000) including alterations in arousal at either extreme, such as seizure
and stupor (Kleinhauz and Behan, 1981).
Thalamocortical loops that involve orbitofrontal-limbic circuits such as orbitofrontalhypothalamus-amygdala-brainstem reticular formation not only regulate internal arousal
processes, but also appraise changes in the external environment by processing sensory
information including the face and voice. This allows an integration of adaptive bodily
responses with ongoing emotional and attentional states, and the regulation of interpersonal and social behaviour (Dolan, 1999; Critchley, Elliott, Mathias and Dolan, 2000).
These circuits provide a mnemonic repository of visceral and somatic states and material
related to self (Damasio, 1994). By a selective shutting down of customary everyday
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Frontal connectivity and hypnosis 27
frontal executive and inhibitory functions, hypnosis provides access to past memories of
cognitive, affective and somatic events (Damasio’s ‘somatic marker’). This may explain
how somatic memory, including surgical operations in childhood that involve the alteration and reduction of consciousness with anaesthetic (Hilgard, Hilgard and Newman,
1961), and the reinstatement of epilepsy (Page and Handley, 1993), may arise with
hypnosis.
Such a shutting down mechanism therefore facilitates age regression. The association
between hypnosis with an unpleasant childhood event has been a potent source of negative reactions involving revivification of emotionally laden and somatic events (or taking
the form of retrograde amnesia), and alterations of arousal with autonomic signs. Sequelae
have included chronic depression and PTSD symptoms (Gruzelier, 2000b, 2004); dissociative episodes following age regression to the time of WWII trauma (Kleinhauz,
Dreyfuss, Behan, Goldberg and Azikri, 1979); surgical operations in childhood involving
the alteration and reduction of consciousness with anaesthetic (Hilgard et al., 1961); the
production of stupor (Kleinhauz and Behan, 1981); and the reinstatement of epilepsy
(Page and Handley, 1993). Where there were multiple memory cues in this associative
network of negative episodes, adverse effects may be compounded (Page and Handley,
1993). A cumulative memory effect was observed when an unpleasant experience in
childhood with chemical anaesthesia, and the countdown while that anaesthetic took
effect, were associated respectively with a change in arousal with hypnosis and the
dehypnosis countdown (Hilgard et al., 1961). The reduction in frontal influences will
also lead to cognitive confusion and distortions of body schema.
Conclusion
Our programme of research has repeatedly provided support for alterations of anterior
brain functions as a significant factor in the influence of hypnosis in hypnotizable subjects, and one that is not seen in subjects of low hypnotizability who are in receipt of the
same instructions. In order to avoid misunderstanding, it has been emphasized throughout that the results in no way imply a global inhibition, disconnection or deactivation of
the frontal lobes. The ERP study which sampled both earlier and later stages of hypnosis
indicated that alterations may change with the temporal course of hypnosis. Left frontal
functions appear to be selectively more prone to alteration than right-sided functions,
but given the cognitive flexibility/neural efficiency of the hypnotizable subject some
frontal functions bilaterally may conceivably be enhanced depending on the instructions
of hypnosis given.
Consideration of the literature on hypnotizability (Heap et al., 2004) discloses that
this is the first time that neural efficiency as defined by the fMRI BOLD index has been
introduced as a construct to distinguish high from low hypnotizability. Neural efficiency
can be seen to amplify the construct of cognitive flexibility. As has been developed
elsewhere (Gruzelier, 2002a) a highly flexible nervous system may under some circumstances be a vulnerable one and reflect vulnerabilities for pathology through both imbalances in the internal milieu and susceptibilities to psychological stressors. The evidence
of associations with the schizotypal personality provides one such example (Jamieson
and Gruzelier, 2001; Gruzelier, De Pascalis, Jamieson, Laidlaw, Naito, Bennett and
Dwivedi, 2004). Recent evidence shows strong relations in medical students between
hypnotizability and a range of personality variables, including low self-directedness,
schizotypy, affective distress, anxiety and depression, as well as with altered states of
consciousness, imaginative involvement, and self-transcendence (Laidlaw, Dwivedi,
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28 John Gruzelier
Naito and Gruzelier, 2004). This is not the first time that an apparent predisposition to
psychopathology has been theorized to construe evolutionary benefits such as provocative theories of the evolution of man and culture through schizotypal characteristics
(Jaynes, 1976; Horrobin, 2001).
Finally another dynamic reviewed here concerns the enhancement of some right
hemispheric processes in hypnosis. Right hemispheric involvement in hypnosis has
been a popular though controversial view amongst hypnotherapists and scientists
(Crawford and Gruzelier, 1992), and has provided a highly appropriate metaphor in the
clinic (Pedersen, 1984). Right hemisphericity as a trait of hypnosis was also popular,
but for this we found no support (Gruzelier, 1998). In some groves of academe lateralization is anathema following journalistic popularization of theories of hemispheric
specialization. Our results (Gruzelier et al., 1984; Jutai et al., 1993; McCormack and
Gruzelier, 1993; Egner et al., 2005) should not be trivialized as evidence for simplistic
binary left-right dynamics. The brain consists of functional networks extending
bilaterally, and with excitatory as well as inhibitory dynamics, both of which require
neuronal activation and metabolism. And while on this theme, be mindful too, that
altered states of consciousness have only very recently been considered by some a
respectable subject of scientific investigation in cognitive neuroscience (see Dietrich,
2003; Vaitl, Birbaumer, Gruzelier, Jamieson, Kotchoubey, Kübler, Lehmann, Miltner,
Ott, Pütz, Sammer, Strauch, Strehl, Wackermann and Weiss, 2005, for some restoration
to favour). Currently then our evidence of disconnectivities of the left lateral prefrontal
cortex in our fMRI/EEG study contribute to growing evidence of a neurophysiological
basis to hypnosis and other altered states of consciousness (see also Rainville et al., 1999;
Halligan, Athwal and Oakley, 2000; Kosslyn, Thompson and Constantini-Ferrando,
2000; Spiegel, 2003). Much further research is required to elucidate the exact nature of
the processes involved.
Acknowledgement
Written while in receipt of EU New Information Technologies grant: Presenccia; Application, Creative Presence States.
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Address for correspondence:
John Gruzelier
Department of Psychology
Goldsmiths College
New Cross
London
SE14 6NW
UK
Email: [email protected]
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