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Hypnosis and cognitive neuroscience: Bridging the gap

Article  in  Cortex · December 2012

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Peter W Halligan David A Oakley

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Editorial

Hypnosis and cognitive neuroscience: Bridging

Peter W. Halligan a,* and David A. Oakley b

Controversy and disagreement lie at the heart of scientific suggested phenomena previously dependent on the subjects’
advance and hypnosis has had its fair share of detractors, largely unverifiable report and behaviour (Raz and Campbell,
given its chequered history in some areas of medicine and 2011; Terhune and Kadosh, 2012).
long standing association with mysticism and stage hypno- As one indication of the progress made, the cover of this
tism (Raz and Shapiro, 2002). Nevertheless, despite some special issue brings together one of the very first and one of
understandable scepticism, hypnosis’s compelling behav- the most recent ways of demonstrating objectively the power
ioural and experiential phenomena continued to provide of suggestion. The foreground contains Chevreul’s pendulum
a small number of neuroscientists with a rich paradigm for while the background provides a representation of brain
understanding the nature of hypnosis and using it to manip- activations seen following hypnotic suggestion during func-
ulate aspects of phenomenological consciousness (Spiegel tional magnetic resonance imaging (fMRI). The pendulum
et al.,1982; Kihlstrom, 1987; Crawford and Gruzelier, 1992; effect was described in 1833 by the French chemist Michel-
Kirsch and Lynn, 1995; Oakley, 1999; Kosslyn et al., 2000; Raz Eugene Chevreul in an open letter to the physicist André
et al., 2002; Barnier and McConkey, 2003). Ampère (Chevreul, 1833; Spitz, 1977). The effect involves
Recently, however, hypnosis has begun to attract renewed amplifying small, unconscious (ideomotor) movements of the
interest from cognitive and social neuroscientists interested hand, arm and body of the individual holding the pendulum.
in using hypnosis and hypnotic suggestion to test predictions The origin and direction of the movement is determined by
about normal cognitive functioning (Jamieson, 2007; Oakley the content of the concurrent suggestions provided by another
and Halligan, 2009; Terhune and Kadosh, 2012; Del Casale person, by environmental cues and/or by implicit expectan-
et al., 2012; Priftis et al., 2011; Connors, 2012; Hoeft et al., 2012). cies (via autosuggestion) on the part of the person holding the
This renewed interest was partly facilitated by the growing pendulum, who experiences the movement as occurring ‘all
acceptance of consciousness as a legitimate field of enquiry by itself’. This ideomotor response captured by the Chevreul
for cognitive neuroscience (Marcel and Bisiach, 1988; pendulum effect is a classic hypnotic phenomenon respon-
Velmans, 1996) but also critically, by the findings from sible for the apparently spontaneous movements experienced
neurophysiological tools (Hinterberger et al., 2011) and in in the context of water divining, automatic writing, the use of
particular the widespread availability of functional-imaging ouija boards and table turning in séances. It is also a good
techniques (Raz and Shapiro, 2002; Oakley and Halligan, example of ‘cold control’ e described by Dienes and Hutton
2009). In tandem with improvements in experimental design (2013). The background image on the cover features approxi-
and subject screening, these studies are now making inroads mate surface projections of activated voxels revealed by fMRI
into the functional anatomy of hypnosis (Jamieson, 2007) as during hypnotically suggested heat pain (Derbyshire et al.,
well as paving the way for its use as an experimental tool for 2004), superimposed on a glass brain. These activations were
neuroscience research (Oakley, 2006). In particular these similar to those produced by an actual painful heat stimulus
studies have begun to address the sceptic’s concern regarding but different from those seen when the hypnotised subject
the subjective reality and comparability of hypnotically was instructed to imagine the same pain experience.

* Corresponding author.
E-mail addresses: [email protected] (P.W. Halligan), [email protected] (D.A. Oakley).
0010-9452/$ e see front matter ª 2012 Elsevier Ltd. All rights reserved.
http://dx.doi.org/10.1016/j.cortex.2012.12.002
360 c o r t e x 4 9 ( 2 0 1 3 ) 3 5 9 e3 6 4

In addition to demonstrating the future potential for this disorders with the intention of uncovering the underlying
growing field, the contributors to this special issue illustrate cognitive processes implicated in these clinical conditions
how methodological and theoretical advances can return (Oakley and Halligan, 2009; Connors, 2012).
novel and experimentally verifiable insights relevant to The next three studies in this special issue [Cardeña et al.
neuroscience in general and the neuroscience of conscious- (2013); Dienes and Hutton (2013); Kihlstrom (2013)] and the
ness in particular. Moreover, the special issue includes several review by Mazzoni et al. (in this issue) that follows are geared
new and provocative contributions from a range of estab- towards exploring hypnosis and hypnotic suggestibility. That
lished and up and coming researchers that cannot be gained is, they are primarily ‘intrinsic’ in intent. The final five papers
from any other source. all involve hypnotically suggested phenomena but are less
In the opening paper Kihlstrom (2013), a pioneer in the easy to categorise. The studies by Deeley et al. (2013); Cojan
neuroscience of hypnosis, provides the inexperienced reader et al. (2013) and Burgmer et al. (2013) all derive from an
with an excellent overview of the area. He reminds us how, ‘instrumental’ interest in parallels between hypnotic and
despite being a “late comer”, hypnosis played a significant role conversion disorder paralysis but focus on the nature of
in the “consciousness revolution” within psychology and hypnotic paralysis as part of that interest in the ‘intrinsic’
cognitive science (Hilgard, 1987), and in particular rekindling question. Similarly, the final two papers, Valentini et al. (2013)
interest in, and acceptance of, research in unconscious and Lifshitz et al. (2013) derive from more general interests in
mental processing (Kihlstrom, 1987, 2007). The paper then pain perception and ‘automatic’ cognitive processes respec-
reviews neuroscience research in hypnosis which can broadly tively but equally help elucidate the hypnotic phenomena
be divided into two main approaches depending on the they employ.
primary focus of interest. The first more ‘intrinsic’ approach is From a cognitive neuroscience perspective, relatively little
directed at providing a better understanding of the neuro- is known about the underlying processes involved in the
ecognitive nature of hypnosis itself and of hypnotic hypnotic trance state itself. To remedy this, the paper by
phenomena in general (see also Posner and Rothbart, 2010). Cardeña et al. (2013) is a good example of an intrinsic study
Central to the intrinsic approach is the focus on under- that considers the neurophysiological basis of hypnosis in the
standing the behavioural, experiential and neuro-cognitive absence of explicit suggestions (referred to as ‘neutral’
nature of hypnosis and hypnotically suggested subjective hypnosis). Drawing on a meticulous analysis of experiential
changes. Relevant research here includes studies exploring and physiological data, and paying close attention to temporal
the neural correlates of individual differences in hypnotis- state fluctuations, this study provides new and intriguing data
ability, alterations in neural activity accompanying the that throw light on the nature of the spontaneous but trait
induction of hypnosis and the neural correlates of response to dependent changes that occur in neutral hypnosis over time
individual hypnotic suggestions, including hemispheric and across hypnotisability levels.
differences. More recently, several studies have attempted to According to the “cold control” theory of hypnosis (Barnier
characterise the neural signature of hypnosis by exploring et al., 2008) hypnotic responses comprise an intention to
alterations observed in the normal resting default mode state perform a motor or cognitive action, while the subject is
of brain activity following hypnotic induction procedures in unaware of the intention. In other words, if one intends to lift
the absence of suggested changes in experience (McGeown one’s arm it will rise; but if one is unaware of the intention, the
et al., 2009; Deeley et al., 2012). arm will appear to lift by itself, producing the classic
The second approach reviewed by Kihlstrom (2013) under phenomenology of the hypnotic arm levitation response.
the heading ‘Hypnosis as an experimental medium’ looks at Using repetitive transcranial magnetic stimulation (rTMS),
‘instrumental’ studies that employ targeted hypnotic sugges- Dienes and Hutton (2013) selectively disrupt dorsolateral
tion as a research tool to investigate a range of normal prefrontal cortex (DLPFC) processing on the hypothesis that,
psychological processes, such as motor control, pain percep- as the DLPFC is a key region involved in higher order thoughts
tion, memory and automaticity in the Stroop task, as well as related to performing action, it should be easier to respond to
abnormal processes seen in schizophrenia, delusions and a hypnotic suggestion if it is made harder for subjects to be
conversion disorder. As Kihlstrom points out however, there is aware of the intention to perform an action. The results show
considerable overlap between the two approaches. Intrinsic that that the subjective rating of hypnotic suggestibility was
studies whose primary intent is to explore suggested hypnotic higher after stimulation of the DLPFC and lend support to
phenomena such as changes in colour perception or hypnotic theories postulating that diminished frontal cortex func-
analgesia, for example, can equally help to elucidate the tioning is related to hypnotic response.
general mechanisms underlying colour vision and pain Hypotheses regarding the differential role of hemispheric
perception. Conversely, despite the primary focus of instru- processing in hypnosis have typically tended to implicate the
mental studies, many also shed light on the cognitive and right-hemisphere (RH) on the basis of its association with
biological substrates underlying hypnosis and the suggested creative, intuitive, and holistic processing. Despite evidence
hypnotic phenomena they rely on. While still relatively small, of RH involvement in hypnosis from behavioural or psycho-
the instrumental approach has established historical prece- physiological paradigms, neuropsychological reports testing
dence. Charcot, Janet, and Freud all employed hypnosis for the this hypothesis have been largely neglected. No study has
study of hysteria and dissociative disorders (Bell et al., 2011). A addressed the RH hypothesis explicitly by testing patients
recent and promising extension of this approach involves using with lateralized brain injury. In the small case series,
hypnotic suggestion to create “clinically informed analogues” Kihlstrom et al. (2013) do this by assessing the hypnotisability
of established structural and functional neuropsychological of patients with either left- or right-hemisphere lesions. Their
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findings show that it is possible for brain-injured individuals The potential for exploring this similarity was shown by
to experience hypnosis, and that their responses can be Halligan et al. (2000) and others when successfully attempting
assessed without unduly compromising standardised proce- to model conversion disorders (Ward et al., 2003; de Lange
dures. Moreover, the results showed that unilateral RH et al., 2007; Cojan et al., 2009a,b). Collectively these studies
damage following stroke does not impair hypnotic respond- provide evidence of engagement of a range of prefrontal
ing. Although based on modest sample sizes, the current ‘executive’ inhibitory regions when attempting to move the
study is valuable not only for evaluating the right-hemisphere paralysed limb. However, while earlier PET studies implicated
hypothesis, but also showing that people with brain damage orbitofrontal cortex (OFC) and anterior cingulate cortex (ACC)
can be as hypnotically responsive as controls. in involuntary inhibition of movement (Halligan et al., 2000;
A key issue that remains unresolved and hence relevant Marshall et al., 1997; Ward et al., 2003), subsequent fMRI
when considering hypnosis from a neuro-cognitive perspec- studies attributed these activations to the main effects of
tive is what we mean by the term ‘hypnosis’. Typically this is hypnosis (Cojan et al., 2009b). Accordingly, it is not surprising
reserved for the putative trance state produced by an induc- that the special issue contains three different papers
tion procedure. While related, the targeted suggestion tends to attempting to elucidate different but related aspects of the
be seen as a distinct process. This distinction is based on the functional anatomy of suggested limb paralysis.
well-established observation that subjects responsive to The first paper by Deeley et al. (2013) describes an fMRI
suggestions used in hypnotisability tests respond whether or study involving eight subjects selected for high hypnotic
not they have been exposed to a hypnotic induction procedure suggestibility that examines the functional anatomy of upper
(e.g., Braffman and Kirsch, 1999). Several accounts of limb movement during hypnosis, where subjects attempt to
‘hypnosis’ consequently tend to make ‘suggestion’ the move following limb paralysis suggestions. Combining
defining feature such that hypnosis is defined by a subject’s objective and subjective measures of movement in conjunc-
responsiveness to specific sorts of suggestion irrespective of tion with measurements of brain activity the main finding
whether a formal hypnotic induction procedure is used (Green was greater supplementary motor cortex (SMA) and ACC
et al., 2005). The issue raised by these accounts is that if activation in the suggested paralysis condition relative to
‘hypnosis’ is defined primarily in terms of the effects of normal conditions. This is consistent with the role of SMA in
suggestion, it can question whether hypnosis necessarily motor intention and planning and the involvement of ACC, BA
involves a unique altered-state of consciousness (Kirsch and 24 in involuntary, as well as voluntary, inhibition of prepotent
Lynn, 1995). This has led some in the hypnosis community motor responses. The generalisability of these findings and
to dismiss the issue of pursuing a “special-state” or “trance” specific contributions of SMA, and ACC to involuntary inhi-
on theoretical grounds, or pragmatically given the absence of bition need to be assessed in future studies by measuring the
a widely recognised or agreed behavioural marker (Lynn et al., neural correlates of both voluntary and involuntary inhibition
2007). In their review paper Mazzoni et al. (2013) tackle this in highly hypnotisable subjects across a variety of tasks
controversy head on. Despite the upsurge in the number of requiring motor and non-motor inhibition.
neuroimaging studies, they argue that the stalemate over the Debate continues as to whether direct inhibition of motor
altered-state issue persists, mainly due the confounding of systems is responsible for hypnotically induced paralysis and
hypnotic trance induction and suggestion in many studies. by extension motor conversion. Cojan et al. (2009a) provided
Although their findings are tentative, they conclude that an alternative account using a go e no go task to examine
appropriately controlled neuroimaging studies do support the brain activation during movement preparation, execution,
existence of an identifiable hypnotic state. As neither the and inhibition in a group selected for high hypnotic suggest-
hypnotic induction procedure nor the cortical alterations it ibility employing separate suggested and feigned paralysis
produces are necessary for the experience of ‘hypnotic’ conditions. This study found that highly hypnotically
suggestions, the substantive issue remaining is whether suggestible participants exhibited normal motor cortex acti-
a trance state enhances the experience of those suggested vation during a movement preparation phase, but right ACC,
effects and the related brain activity. bilateral OFC and extrastriate visual area increases during the
Patients with “functional” or “psychogenic” conversion paralysis condition which were interpreted as being indicative
disorders present symptoms, such as paralyses, that resemble of state-related hypnosis changes rather than an inhibitory
those of neurological illnesses and for which no organic or mechanism.
neurological cause has been established (Fink et al., 2006). In this special issue Cojan et al. (2013) use a modified
Such disorders are clinically challenging, as they can comprise bimanual GoeNo go task performed either as a normal base-
between 30 and 40% of patients attending neurology outpa- line condition or during unilateral paralysis following
tient clinics. Related to this, is one of most fascinating char- a hypnotic suggestion to compare motor inhibition mecha-
acteristics of hypnosis e namely the ability to produce marked nisms during hypnosis. Given the high temporal resolution
alterations in volitional control. Highly hypnotically suggest- and proven effectiveness in GoeNo go trials, they employed
ible subjects report being unable to execute simple motor topographical electroencephalography (EEG) analysis rather
acts in response to specific suggestions. The similarities in than fMRI to investigate both the spatial organisation and
reported experiences between conversions disorder patients temporal sequence of the neural processes involved in these
and hypnotised subjects responding to suggestions of different conditions. Although motor preparatory activations
paralysis, raised the possibility that such symptoms were were similar in all conditions, their results unlike Deeley et al.
generated by the same kinds of cognitive and neural processes (2013) suggest paralysis is not caused by direct motor inhibi-
(Bell et al., 2011). tion, such as in voluntary suppression of actions, but rather
362 c o r t e x 4 9 ( 2 0 1 3 ) 3 5 9 e3 6 4

differential enhancement of executive control systems in highly hypnotically suggestible participants, but not in those
mediated by right prefrontal areas. classified as low in hypnotic suggestibility. However, the
The paper by Burgmer et al. (2013) provides yet another manipulation was more specific to subjective reports of pain
perspective on the neural substrates underlying voluntary and unpleasantness (affect) than it was for reports of pain inten-
involuntary motor activation in hypnotic paralysis. Unlike the sity. In addition modulatory suggestions were found to be
two previous papers, Burgmer et al. (2013) are concerned to more effective in increasing, compared to decreasing the tar-
differentiate movement observation (passive experimental geted subjective experience. The EEG data was interpreted as
condition) and imitation (active motor effort) following a left being consistent with topedown influences underlying the
limb paralysis induced by hypnosis in control subjects. The modulatory effects of the hypnotic suggestion conditions.
passive condition was employed as a control given that acti- The final intriguing paper by Lifshitz et al. (2013) builds on
vation of the motor network during movement observation is a series of reports that Raz and colleagues inspired over the
thought to be mediated by a mirror neuron system indepen- past decade. This involves the use of hypnotic suggestion to
dent of voluntary factors in movement generation (Burgmer control or manipulate automatic processes e using specific
et al., 2006). The results showed that hypnotic paralysis suggestions capable of producing effects difficult to fake, such
during movement imitation induced hypo-activation of the as elimination of the Stroop effect. Collectively, these studies
contralateral sensorimotor cortex and ipsilateral cerebellum. demonstrate the influence that suggestion can have over
Hyperactivation of ACC, middle frontal gyrus (MFG), and automatic processes. In this multifaceted study, the authors
insula during the attempt to move under hypnotic paralysis marshal an array of converging evidence that shows the
was unrelated to the executive motor impairment and was capacity of suggestion to “derail” deeply ingrained automatic
interpreted as reflecting alteration in specific aspects of processes such as reading. In addition, they report prelimi-
attention, conflict-detection and self-representation. Criti- nary data indicating that hypnotic suggestion can in highly
cally, hypnotic paralysis did not affect the function of the responsive individuals override several effortful automatic
mirror neuron system, suggesting that early motor processes, processes including the audiovisual integration of the McGurk
such as intention to move or initiate movement are not effect. In addition to reviewing published work, the authors
disturbed in hypnotically suggested paralysis. suggest two new directions by providing pilot studies for
It is well-established that hypnotically suggested analgesia natural extensions of the previous Stroop work. Collectively,
can offer significant reduction in awareness of both clinical these findings open up a promising future research vein that
and experimental pain (Montgomery et al., 2000). Over the could serve to clarify underlying cognitive mechanisms and
past 20 years an extensive functional imaging literature has inform therapeutic applications of topedown control implied
demonstrated that pain experience is mediated via activation in hypnosis.
of a network of cortical regions including the ACC, insula, Although selective, the papers in the special issue make
prefrontal regions, and primary (S1) and secondary (S2) a strong case that the effects of hypnosis and hypnotic
somatosensory cortices. In a landmark study, Derbyshire et al. suggestion are more than capable of being harnessed by
(2004) helped identify brain areas directly involved in the experimental methodologies and contributing to develop-
generation of pain, using hypnotic suggestion to create an ments in cognitive and developmental neuroscience (Oakley
experience of pain in the absence of any noxious stimulus. In and Halligan, 2009; Raz and Campbell, 2011). There is
contrast to imagined pain, fMRI revealed significant changes a wealth of experimental data on hypnosis that still awaits
during this hypnotically induced pain experience within the neuroscientific explanation.
thalamus and ACC, insula, prefrontal, and parietal cortices For example, little primary research exists on the role of
(represented in the cover image of this Special Issue). These developmental factors in hypnotisability despite the finding
findings compare well with the activation patterns during that children are more hypnotisable than adults (Raz, 2012).
pain from nociceptive sources and provide the first direct From a cognitive neuroscience perspective, the use of effec-
experimental evidence in humans linking specific neural tive hypnotic analogues for clinical conditions require better
activity with the immediate generation of a pain experience. articulation of the phenomenological experience so that
It is well known that the perception of pain can be influ- hypnotic suggestions can faithfully replicate the relevant
enced by a number of cognitive manipulations such as atten- clinical symptoms (Woody and Szechtman, 2011). The corre-
tional focussing (Bantick et al., 2002), meditation (Perlman spondences between hypnotically suggested phenomena and
et al., 2010), pain expectation and anticipation (Porro et al., their neurological counterparts also provide research chal-
2002), placebo/nocebo experience (Kong et al., 2008) and, lenges for further development of practical clinical interven-
hypnotic suggestion (Derbyshire et al., 2009). The interesting tions such as the recently reported reduction of sensory
study by Valentini et al. (2013) investigates evidence provided extinction effects after stroke (Maravita et al., 2012). Finally,
by previous reports (Rainville et al., 1997; Hofbauer et al., 2001) we simply do not know the reconstructive process whereby
that hypnotic suggestion for changes in perceived intensity or hypnotic suggestions (or suggestions per se) are cognitively
affective valence of a painful stimulus could selectively influ- processed and translated into subjective experiences. The
ence subjective report and be mediated by different brain production of consistent outcomes suggests the employment
areas. In contrast to previous work, pain was created using of a set of common, largely implicit, ‘expectations’ regarding
pulsed laser stimulation rather than directly applied heat and the appropriate experience, role or symptom presentation.
EEG employed rather than positron emission tomography The nature of such experiences cannot be simply addressed
(PET). Valentini et al. (2013) found the expected modulation of by brain activity studies. In clinical training settings, the
affect and intensity dimensions of pain by hypnotic suggestion opportunity for practitioners to observe the creation (and
 c o r t e x 4 9 ( 2 0 1 3 ) 3 5 9 e3 6 4 363

removal) of neurological or functional neurological symptoms de Lange FP, Roelofs K, and Toni I. Increased self-monitoring
of ‘virtual patients’ in normal volunteers also provides during imagined movements in conversion paralysis.
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Deeley Q, Oakley DA, Toone B, Giampietro V, Brammer MJ,
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