FUNCTIONAL BRAIN IMAGING
AND THE INDUCTION
OF TRAUMATIC RECALL:
A Cross-Correlational Review Between
Neuroimaging and Hypnosis
ERIC VERMETTEN1,2
University Medical Center and Central Military Hospital, Utrecht, The Netherlands
J. DOUGLAS BREMNER
Emory University and Emory Hospital, Atlanta, Georgia, USA
Abstract: The behavioral and psychophysiological alterations during
recall in patients with trauma disorders often resemble phenomena
that are seen in hypnosis. In studies of emotional recall as well as in
neuroimaging studies of hypnotic processes similar brain structures
are involved: thalamus, hippocampus, amygdala, medical prefrontal
cortex, anterior cingulate cortex. This paper focuses on cross-correla-
tions in traumatic recall and hypnotic responses and reviews correla-
tions between the involvement of brain structures in traumatic recall
and processes that are involved in hypnotic responsiveness. To further
improve uniformity of results of brain imaging specifically for trau-
matic recall studies, attention is needed for standardization of hyp-
notic variables, isolation of the emotional process of interest (state),
and assessment of trait-related differences.
In the last 10 years, there has been a rapid increase in our under-
standing of the brain processes that are involved in processing of
traumatic events (see Stern & Silbersweig, 2001). Much of this research
is related to the processing of stress, memory, and emotion (see reviews
of Armony & LeDoux, 1997; Baddeley et al., 2000; Bremner, Krystal,
Southwick, & Charney, 1995; Bremner & Narayan, 1998; Cahill, 2000;
LeDoux, 1993; McGaugh, Cahill, & Roozendaal, 1996; Nijenhuis,
The International Journal of Clinical
and Experimental Hypnosis
2004, Vol. 52, No. 3, pp. 280–312
Manuscript submitted November 02, 2002; final revision received October 24, 2003.
1
This study was supported NIMH 1R01MH56120-01A1, and a Veterans Administra-
tion Career Development Award to Dr. Bremner.
2
Address correspondence to Eric Vermetten, MD, PhD, Department Psychiatry,
University Medical Center Utrecht, Utrecht University, Heidelberglaan 100, 3584 XC
Utrecht, The Netherlands. E-mail: e.vermetten@azu.nl
0020-7144/04/5203-280$16.00 # The International Journal of Clinical and Experimental Hypnosis
280
Van der Hart, & Steele, 2002; Packard & Cahill, 2001; Phillips, Drevets,
Rauch, & Lane, 2003a, 2003b; and the special issues of the International
Journal Clinical and Experimental Hypnosis, April and July 2003). Among
the factors that contributed to this increase are the availability of high-
quality functional brain imaging techniques, cross-fertilization of
different disciplines (e.g., cognitive and developmental psychology,
nuclear medicine, pharmacology, molecular biology, psychiatry), and
the increasing specificity of induction procedures for traumatic recall in
study protocols. (For a description of the characteristics of two of the
main neuroimaging methods, functional magnetic resonance imaging
(fMRI) and positron emission tomography (PET), see the Appendix).
Innovative experimental designs in the field of neuroimaging have
increased our understanding of basic processes of memory storage and
emotion processing, lesion studies have pointed to brain regions that
are critically involved, and clinical studies in a variety of patient
populations have revealed a neural circuitry that is involved in differ-
ent disorders. These developments have also further contributed to our
current understanding of brain processes involved in pain, the phe-
nomenology of consciousness, and emotional processing in general and
have led to an understanding of regional patterns of activation and
deactivation.
Still, little is known about this neural circuitry that underlies (altera-
tion of) perceptual processing in patients with psychopathology in
which emotive processing is challenged in relation to exposure to
traumatic events. This alteration of perceptual processing can be
challenged by using visual, acoustic, or other sensory stimuli, or with
personalized narratives that induce recall of traumatic events. The
pattern of metabolic changes in the brain can be measured and corre-
lated with the subjective emotional response. This emotive process may
be paralleled by a set of involuntary/automatic processes that occur:
effects in heart rate, perceptual and emotional alteration, time distor-
tion, and analgesia (Hull, 2002), upon which patients may be selected
for assessment of their regional blood flow patterns (Lanius et al., 2002).
These studies have started to appear in scientific journals in the last 8
years but are still scarce.
Despite promising study results, the field of hypnosis has not fully
used the momentum that arose from these developments. Several
imaging studies in healthy populations have demonstrated differences
in the neural circuitry that is involved in response patterns across
hypnotic states, e.g., alterations of pain affect and pain modulation
(Faymondville et al., 2003; Rainville, Duncan, Price, Carrier, & Bushnell,
1997), alteration of visual processing (Kosslyn, Thompson, Costantini-
Ferrando, Alpert, & Spiegel, 2000), or hypnotic alteration of acoustic
perception (Szechtman, Woody, Bowers, & Nahmias, 1998). Most of
these studies have used high and low hypnotizable subjects to gain
NEUROIMAGING AND HYPNOSIS 281
insight in the neural mechanisms of perceptual alteration by measur-
ing alteration in regional brain blood flow. From these studies, it
appears that high hypnotizables are capable of modifying their brain
metabolism in response to a specific set of instructions to alter affect,
pain, or other experiences and have pointed out that subjects can
differentially alter (block or stimulate) certain perceptual functions,
e.g., ‘‘taking the color out of a picture’’ that is presented in front of
them. To a considerable extent, high hypnotizables are capable of
modifying the circuitry with which their brains process stimuli. To
date, few of these studies have used the cumulative power of combin-
ing these knowledge-based resources in neuroimaging studies in
patient populations.
It has been a decade since studies by Stutmann and Bliss (1985),
Spiegel, Hunt, and Dondershine (1988), and Frischholz, Lipman, Braun,
and Sachs (1992) empirically confirmed Janet’s early notions (1889) that
there is an overlap between the phenomena that are typically related to
hypnosis and the phenomena occurring in emotional recall in post-
traumatic stress disorder (PTSD). These patients have demonstrated
enhanced susceptibility to ‘‘hypnotic’’ situations, which traumatic re-
call can be considered to be. Hypnotic induction can mobilize a wide
spectrum of responses, varying from increased anxiety to flashbacks
that can occur with or without feelings of detachment to other dis-
sociative experiences, such as numbing or freezing, feelings of in-
voluntariness, and loss of self-agency.’’ Moreover, classic hypnotic
responses such as time distortion, analgesia, and derealization can
occur along with these memories. The content of the emotion is also
widespread and can change rapidly depending on the focus of atten-
tion: e.g., anger, shame, guilt, or disgust. These responses can have
bimodal effects, such as enhanced attention versus lowering of atten-
tion or out of body experiences versus detailed focus on details, and can
also be reflected on the level of psychophysiological alteration, e.g.,
increased versus decreased heart rate. Although these may be related to
hypnotic virtuosity, this has not been studied yet.
Within a general framework of identification, production, and reg-
ulation of emotional recall (see Phillips et al., 2003), hypnotic response
patterns are related to the involvement of different brain correlates
(Lanius et al., 2002). We pose that insight in these hypnotic response
patterns needs to be taken into account when analyzing brain correlates
of traumatic recall in trauma disorders, e.g., in PTSD but also in
dissociative identity disorder (DID) and borderline personality disor-
der (BPD). Moreover, hypnotic paradigms can provide additional
information regarding the involvement of involuntary mechanisms
in traumatic recall. In addition, we feel that by cross-correlating the
phenomenology and neurophysiology of traumatic recall and hypnosis
similarities in parameters, results can be found that improve our
282 ERIC VERMETTEN AND J. DOUGLAS BREMNER
understanding of hypnosis and basic elements of consciousness and
emotion. To explore this relation, we will review the imaging results in
these studies.
TRAUMA AS A HYPNOTIZING AGENT
It is a known fact that traumatic stress can mobilize responses that
have hypnotic features. These can be seen in a variety of situations,
e.g., in the battered and abused child who creates an invisible identity
so as not feel the pain and humiliation (identity alteration, amnesia,
R. Loewenstein, personal communication, November 2000), in jour-
nalists when watching an execution as an eyewitness (dissociation;
Freinkel, Koopman, & Spiegel, 1995), in survivors of the Estonia ferry
disaster who attempted to rescue other survivors (numbing; Ericksson
& Lundin, 1996), in people who witnessed victims jumping from the
World Trade Center on September 11, 2001 (verbal inhibition, Spiegel,
personal communication, 2001), or the responses in orphaned
Rawandan children (stupor). Traumatic experiences can mobilize hyp-
notic responses that resemble the hypnotic state during which intense
absorption in the hypnotic focal experience (Tellegen & Atkinson,
1974) can be achieved by means of a dissociation of experience
(Hilgard, 1977; Spiegel et al., 1988, p. 301). It was Janet who described
the splitting of consciousness that occurrs in response to traumatic
stress and the consequences of trauma on memory and identity. Janet
described a constellation of symptoms that we now categorize as PTSD
or dissociative disorders, including dissociative amnesia and fugue,
with a central assumption that different aspects of the traumatic
experience are not actively available to consciousness, although they
may have an influence on behavior (Loewenstein, 1993; Spiegel &
Carden˜ a, 1991).
The psychological processes that were captured as core components
of the hypnotic experience as described by Spiegel (1997) are: (a)
absorption; (b) dissociation, and (c) automaticity. These three factors have
been postulated because they explain the phenomena best in a hypnotic
situation (Spiegel & Carden˜ a, 1991). Hypnosis has been best defined as
an altered state of consciousness. Recently, a new definition of hypnosis
has been coined in which the use of the word hypnosis as part of the
hypnotic situation is not necessary for the induction nor description of
the state of hypnosis (A. Barabasz, personal communication, September
2003).
Absorption is defined as a narrowing and intensification of attention,
a disposition for having episodes of single total attention that fully
engage one’s representational resources (Tellegen & Atkinson, 1974).
Physiological arousal can produce this narrowing of attention, which is
directed more to central aspects of the traumatic experience than to
NEUROIMAGING AND HYPNOSIS 283
peripheral aspects (Christianson, 1992). Narrowing of attention can be
functional in that all attention can be devoted to essential threat stimuli
and defensive concerns. Dissociation can be described as a kind of
divided or parallel access to awareness where several systems may
have some independence. It refers to a compartmentalization of ex-
perience, which can be considered complementary to absorption. The
term refers both to its origins, i.e., the splitting of consciousness that
may occur during trauma, and to the subsequent process of associating
or assigning experiences, as they occur over and over in time, to specific
states of consciousness, ego centers, or affective states (Crabtree, 1992).
Dissociation can also be part of an autohypnotic process (e.g., ‘‘I am
invisible; I have no feelings’’), which is applied to reduce the perception
of pain and the personal implications of trauma (Van der Kolk &
Van der Hart, 1989). Automaticity may be defined as the tendency to au-
tomatically develop a belief in a suggested reality or the nonvolitional
transformation of a suggested idea to a suggested effect (Van Der Hart
& Van Der Kolk, 1991). Hypnotic automaticity reflects an altered sense
of self-agency consistent with a modification of the property of mineness
of self-generated intentions and voluntary actions. The involuntariness
is captured in this description as well, representing the recognition of
one’s own volition and capacity to act (P. Rainville, personal commu-
nication, September 25, 2002; cf. Krystal, 1988). A diagram illustrating
the shared neurophysiology of hypnosis with the neurophysiology of
traumatic recall situations in highly hypnotizable subjects is illustrated
in Figure 1.
HYPNOTIC SUSCEPTIBILITY IN TRAUMA-RELATED
PSYCHOPATHOLOGY
A central theme in trauma-related psychopathology is that physical,
emotional, or sexual trauma can play a major role in the shift of this
control function manifesting psychological dysfunctions and/or bodily
or somatic problems (Van Der Kolk et al., 1996). This can be viewed as a
Figure 1. Hypothesized similarities between hypnosis and traumatic recall. This diagram
may be especially true for high hypnotizable subjects, which is usually the case in
patients with PTSD. (Adapted from P. Rainville, personal communication, 2002).
284 ERIC VERMETTEN AND J. DOUGLAS BREMNER
disembodied process with an emphasis on the information processing
analysis of attention mechanisms but also as a state of engagement of
the body-self in the interaction with an object of consciousness, with
emphasis on the biological substrate for the representation of self
(Damasio, 1999) and the property of selfhood (Metzinger, 2000). This
disembodiment can also be seen as a disengagement strategy that
serves a natural defensive function (Gilbert, 2000).
Hypnotizability has been described as the fundamental capacity to
experience dissociation in a structured setting. It underlies the ability to
enter trance; it involves the ability to segregate and idiosyncratically
encode experience into separate psychological or psychobiological
processes (Janet, 1898). Like dissociation, hypnotizability can be related
to a lack of agency or control versus loss of control over psychological
and sometimes also physical functions. It is a dispositional term that
points to its manifestation under certain circumstances, e.g., hypnotic
induction. The critical alteration in these processes occurs in what
Damasio called ‘‘feeling of knowing,’’ which is a fundamental aspect of
self-reflective consciousness that can be separated in hypnosis (p. 280,
1999). Self-representation is a derivative of this fundamental function
of consciousness. It is thought that in hypnosis, and also in traumatic
situations, these representations can be disrupted or processed in
separate streams of information. Self-representation is a hierarchically
organized function with activity in some first-order maps in the brain
that are necessary (but not sufficient) for higher-order representation of
self (e.g., autobiographical self), regulation of cognition and behavior,
and other more extended forms of consciousness.
From these notions, hypnotic capacity can be considered to be both
a liability and an asset; from the perspective of a defense strategy, it
serves a protective purpose (e.g., not remembering or not feeling),
however it can also become maladaptive and lead to dysfunctions
(e.g., time gaps, estrangement from inner feelings, flashbacks) and
(psycho)pathology, like PTSD and dissociative or other trauma spec-
trum disorders. The disposition itself does not change but can be
considered ‘‘sensitized.’’ The symptoms of the dissociative and post-
traumatic states have been hypothesized to fit in a diathesis-stress
model that views pathological dissociation as originating from an
interaction between innate hypnotizability and traumatic experience
(Butler, Duran, Jasiukaitis, Koopman, & Spiegel, 1996). If traumatic
experiences involve a hypnotic process or induce a hypnotic state,
then we should expect traumatized patients to show higher hypnotiz-
ability, in particular while still suffering from their trauma-induced
disorder. One would expect that they have higher scores on classical
hypnotizability scales than other psychiatric patient groups and
healthy or trauma controls. Indeed, several studies supported the
hypothesis that trauma-spectrum-disorder patients demonstrate
NEUROIMAGING AND HYPNOSIS 285
higher scores on classic hypnotic susceptibility scales than other psy-
chiatric patient groups and normal control subjects (Frischholz et al.,
1992; Spiegel et al., 1988; Stutman & Bliss, 1985). Their attention and
arousal systems are altered, rendering them prone to entering hyp-
notic states, with a relative decoupling between irrelevant external
events and mental (emotional) states during hypnotic states. It is not
the experience of trauma; it is the psychopathology that accounts for
the difference in hypnotic susceptibility. What happens with their
hypnotic susceptibility after successful treatment is largely unknown.
Although Janet observed that recovered patients became less hypno-
tizable (Janet, 1898), this finding still awaits testing in systematic
research.
RECALL OF TRAUMATIC MEMORIES
The field of trauma spectrum disorders (consisting of PTSD, dis-
sociative disorders, (DD)), and perhaps also borderline personality
disorder (BPD, see Schmahl, McGlashan, & Bremner, 2002) has re-
ceived a great deal of interest in brain imaging studies. The phenom-
enology of theses disorders is at the heart of the interface between
memory and emotion.
Reexperiencing, Traumatic Recall, Flashbacks, and Flashbulb Memories
One of the most intriguing aspects of trauma disorders is the
reexperiencing phenomena. Numerous labels and descriptions have
been applied to this phenomenon (vanOyen Witvliet, 1997). In earlier
days traumatic recall was also described as ‘flashback’, the reliving of
the traumatic event with strong emotional involvement (Frankel, 1994).
Flashback can lead to sleeping problems, irritability, feeling worse with
traumatic reminders, and secondary avoidance. For a long time flash-
backs were assumed to lack a recognizable neurophysiological corre-
late – therefore they were thought to be at least as likely to be the
product of imagination as it is of memory (Frankel, 1994). However, in a
recent study in 62 PTSD patients comparing flashbacks with ordinary
autobiographical memory performance on cognitive tasks demon-
strated that flashback periods were associated with a specific decre-
ment in visuospatial processing, not specific with decrements on a
verbal processing task. Flashback periods were found to be associated
with increases in a wide range of autonomic and motor behaviors
(Hellawell & Brewin, 2002).
Flashbacks share a phenomenology with what has been described
by Brown and Kulik in 1977 as flashbulb memory, to refer to the vivid
recollections that humans may have of events considered to be of
particular significance to the individual. These memories were de-
scribed as having a photographic quality and as being accompanied
286 ERIC VERMETTEN AND J. DOUGLAS BREMNER
by a strong apparel of contextual information (weather, background
music, clothes worn, etc.) pertaining to the time and place where the
event was first known. From a memory point of view we now know
that these memories are not perfectly accurate and are subject to
decay, but what does not necessarily decay is their capacity to evoke
emotions similar to the ones felt upon when first exposed (Conway
et al., 1994). We feel that flashbulb memories are formed by the
activity of evolutionary old brain mechanism evolved to capture
emotional and cognitive information relevant to the survival of the
individual. In the modern neuroimaging era some of the original
assumptions made by Brown and Kulik have since been challenged,
but the phenomenon in question has remained an important area of
research (Davidson & Glisky, 2002; Sierra & Berrios, 1999). The ex-
periences share clinical features such as involuntary paroxysmal
repetition, sensory vividness, and a capacity to trigger emotions like
anxiety, shame, or anger.
We prefer to use the term ‘traumatic recall’. This can be defined as
imaginary (or virtual) re-exposure to a traumatic event in which the
person experienced, witnessed, or was confronted by death or serious
injury to self or others, and responded with intense fear, helplessness,
or horror, in which a re-experience of similar emotional responses
occur. They usually differ from usual/normal (autobiographical) mem-
ories in their emotional involvement (Van Der Kolk & Van Der Hart,
1991). Their nature is that a recall of the helplessness and uncontrol-
lability of the situation at that time, co-occurs with narrowing of the
attention so that ‘it feels like being back there’ (i.e., when and where the
traumatic event occurred). There can be a sense of loss of control or of
self-agency (‘‘That’s not who I am’’ or ‘‘It is not me to whom that
happened’’). There can be an autonomic response (such as tachycardia,
tachypnea, and diaphoresis) that can induce a feeling of panic (‘‘I’m not
going to make it’’). The recall may be activated by a variety of trauma-
related stimuli, thoughts about the trauma, the context, information
about the trauma, and trauma-related images, sounds, or smells, all
factors of which the person does not have to be aware. Veterans can
reveal this effect potently when they are exposed to darkness and
demonstrate augmented startle reflexes (Grillon, Morgan, Southwick,
Davis, & Charney, 1996).
Storage and Retrieval of Traumatic Memories
With long-term storage, memories are shifted from hippocampus
to neocortical areas, where the sensory impressions take place (Kim &
Fanselow, 1992; Phillips & LeDoux, 1992). This shift in the process of
memory storage to the cortex may represent a shift from conscious
representational memory (explicit memory) to unconscious memory
processes (episodic and implicit memory) that indirectly affect
NEUROIMAGING AND HYPNOSIS 287
behavior (Wallenstein, Eichenbaum, & Hasselmo, 1998). The cogni-
tive neuroscience perspective (see Brewin, 2001) favors a dual re-
presentational model of traumatic memories that proposes separate
memory systems underlying vivid reexperiencing versus ordinary
autobiographical memories of trauma. These two can be separated in
hippocampally-dependent and non-hippocampally-dependent forms
of memory, and are differentially affected by extreme stress. Within
this system, the strength of traumatic memories relates, in part, to
the degree to which certain neuromodulatory systems, particularly
catecholamines and glucocorticoids, are activated by the traumatic
experience (Cahill, 1997; Hasselmo, 1995). Both the quantity of re-
lease of these stress hormones, and the functional availability of the
target brain areas (e.g. hippocampus) modulate the encoding of
memories of the stressful event; ineffectiveness of the system may be
responsible for breakdown in the stream of events and changes in
the central and peripheral processing of the events. This can lead to
the wide spectrum of memory symptoms, ranging from hypermne-
sia, amnesia, deficits in declarative memory, delayed recall of abuse,
and other memory alterations or distortions in trauma disorder
patients.
It should be kept in mind that traumatic memories are not fixed or
indelible, but can change over time. Enhanced memory for the gist of
emotional events seems to be a dominant theme. What is encoded
depends on what was perceived, and what is encoded determines
what will be retrieved (Tulving & Thomson, 1973). Neuroimaging
may shed a light on the retrieval aspect of memory and its emotional
involvement by investigating brain processes that are occurring dur-
ing traumatic recall (Baddeley et al., 2000; Bremner, Krystal, Charney,
& Southwick, 1996; Sara, 2000; Zola, 1998). In PTSD patients ‘traumatic
cues’, such as a particular sight or sound reminiscent of the original
traumatic event, typically can induce a cascade of anxiety and fear-
related symptoms, sometimes without conscious recall of the original
traumatic event. This traumatic stimulus may not always be easy to
identify; it may be that through exposure to a movie, a smell, or more
subtle, a gesture or voice, a memory is metaphorically ‘reawakened’ –
traumatic memories can remain indelible for years or decades and
can be recalled by a variety of stimuli and stressors. A model of
extinction to explain this does not seem to qualify in these cases; a
better model seems to be the failure of successful inhibition of
traumatic memories.
Traumatic recall may not always be processed in an integrated mode
of consciousness. This may be a discontinuous experience with amnesic
gaps. Zimbardo, LaBerge, and Butler (1993) compared the emotional,
cognitive, and physiological responses of subjects experiencing induced
physiological arousal with and without awareness of the source of their
288 ERIC VERMETTEN AND J. DOUGLAS BREMNER
arousal. When subjects received posthypnotic suggestions for arousal
(increases in heart and respiration rate) with and without amnesia for
its source only hypnotizable subjects were expected to differ between
conditions. Indeed, for the hypnotizable subjects, unexplained arousal
produced significant and dramatic effects when compared with
explained arousal, including misattributions (Zimbardo et al., 1993).
These experiments demonstrated that ‘discontinuous experiences’ can
contribute to the development of psychopathological symptoms in
normal persons. But recall can also be hypnotically blocked, e.g. by
posthypnotic suggestion. Here a disruption of retrieval like in post-
hypnotic amnesia or posthypnotic suggestion refers to a subjects diffi-
culty in remembering, after hypnosis. This is not a state-dependent
memory, but it does involve a disruption of retrieval processes similar
to the functional amnesias observed in clinical dissociative disorders. In
a situation like this implicit memory, however, is largely spared, and
may underlie subjects’ ability to recognize events that they cannot
recall (Kihlstrom, 1997).
INDUCTION PROCEDURES OF TRAUMATIC RECALL
Recall of traumatic events in imaging studies is usually embedded
in a so-called ‘‘activation paradigm’’ of re-experiencing traumatic
events. In this paradigm, the patient is asked to briefly (for 1 to 2
minutes) recall a memory that is induced by a personal narrative,
smell, picture, or sound with different traumatic load (traumatic vs.
neutral). For the purpose of this paper, we focus on the recall induced
through emotional or cognitive induction. For the purpose of this
paper, we focus on the recall induced through emotional or cognitive
induction.
Traumatic Recall Through Emotional and Cognitive Induction
Typically in a traumatic-script procedure, the patient writes a
narrative of his or her two most traumatic personal events some days
before the scanning. Usually two neutral texts are made at that time for
the no-activation scan. This text is edited for length (30–40 seconds) and
content. The script is audio taped or can be read during the scan
procedure. The script can then be presented in first or second person,
usually present tense. Immediately before each scan the participant is
instructed to ‘‘close your eyes, listen carefully to the audiotape or voice
and imagine the described events as vividly as possible, as if you were
actually participating in the event again’’ (cf. Lanius et al., 2001; Osuch
et al., 2001; Shin et al., 2000). The participant is then usually scanned 6
to 12 times with a 10-minute interval between scans. When the patient
is lying in the scanner, and the radioactive ligand is administered
intravenously, a trauma script (prepared by a participating patient)
NEUROIMAGING AND HYPNOSIS 289
similar to the one below (B. Elzinga, personal communication, July
2000) can be read:
Listen carefully to the script, and try to imagine as vividly as possible
the experience:
My mom is taking a shower. Dave comes up to me in the living room, where I
am standing. He is whispering in my ear, ‘‘I would prefer to kiss your private
part.’’ I think he is saying that as he presses my breast. Soon his hands sweep
down to my private area and he begins to massage it. His touch is not
welcoming; his pressing my breast hurt me and so does his touching my private
area. I am confused and afraid. Mom can come out of the bathroom any minute.
I want to tell him ‘‘stop,’’ but I don’t. It seems as if I can’t find my voice.
Eventually, I make gestures that imply I don’t want any more touching. He
eventually stops, after calling my name a couple of times. I am relieved, and I
seek some quiet corner of the apartment, just as my mom comes out of the
shower.
Now, continue to imagine the experience from the beginning to the end,
until I ask you to stop.
When applying the model of induction of emotional memories in a
trauma population, some points need to be considered:
(1) A prerequisite for successful implementation of a recall paradigm and
completion of the task in neuroimaging research is the ability of
the participating subjects to have reasonable control over their emo-
tional response in recalling traumatic events. In a PET paradigm, they
need to be able to return to a normal state within approximately 10
minutes. Subjects may – even though they are informed and have given
informed consent – become tearful, panicked, and emotionally over-
whelmed during the recall and feel an urge to suppress these responses.
Sometimes this fails and leads to termination of the scan (Osuch et al.,
2001).
(2) Extreme stress, high or low arousal, and fatigue are distinct psycholog-
ical factors that can separately and interactively affect how information
is processed – rendering it especially influential because it is not sub-
mitted to critical reality testing in a calm, relaxed, and rested state. This is
what Bowers described as a situation in which type II unconscious
influences occur. These describe how information is processed outside
normal awareness, initiative, and volition, speaking of dissociated experi-
ence and dissociated control as two complementary aspects of hypnotic
responsiveness (Bowers, 1973). Low-level monitoring of the process
when exposed to traumatic slides and sounds and calling this to a halt
will typically occur in the trauma-control subject; the situation is dif-
ferent in patients with PTSD. Their dissociated experience refers to the
fact that the (induced) state of affairs seems to occur nonvolitionally, –
which means here that the effort involved is not well presented in
conscious experience. These observations contribute to a framework
in which brain correlates of traumatic recall can be understood as
dissociated control. Upon asking subjects to voluntarily start recalling
290 ERIC VERMETTEN AND J. DOUGLAS BREMNER
a situation (‘‘Now continue to imagine the experience from the begin-
ning’’), some will anticipate becoming stressed and voluntarily control
the situation, and some will become upset and may not be able to stop
recalling (involuntary response).
(3) An important aspect in recall inductions is the content of intrusions.
Research studies suggest that they are not random fragments of the
experience. Typically, they represent stimuli that were present shortly
before the moments with the largest emotional impact (Ehlers et al.,
2002). They need not be sensory per se. Reynolds and Brewin de-
scribed elaborations of the original experience as the most intrusive,
linked to preoccupations with appraisals of the trauma and its se-
quelae, rather than presenting trauma memories (Reynolds & Brewin,
1998). This needs to be taken into account when preparing a narrative
script.
(4) Of importance in the induction of traumatic recall for brain imaging
studies is the theme of general versus specific induction of trauma-
related memories. Typically, in a general paradigm a standardized set
of images or words is presented, and the response pattern in the target
population can be calculated by averaging the responses. In a trauma-
specific paradigm, an individual induction is prepared before the brain
imaging procedure. In this paradigm, the surprise effect of the induc-
tions is somewhat diminished since the subject will recognize his or
her specific elements. Ehlers provides examples of the specific (sen-
sory) nature of the traumatic events from which it appears that
traumatic triggers are specific for both nature and content of the
trauma-related stimulus. In designing an experiment using olfaction
as a trauma-related cue in combat-related PTSD, we were to choose a
traumatic smell that could either be specific for each person or a smell
that all veterans reported as a trigger for traumatic memories. All
veterans had been exposed to diesel during their combat experience,
and diesel was present throughout the war. This smell therefore
seemed to qualify as both a generic and specific trauma-related smell
in the population (Vermetten, Schmahl, Southwick, & Bremner, 2003).
The same can be applied to trauma-related words and other types of
sensory stimulation.
(5) Laboratory studies have demonstrated that central cues of a traumatic
event are usually well remembered, whereas memory for peripheral
details is poor (Christianson, 1992). The narrowing of attention is often
used as an explanation for this finding. High anxiety and arousal are
thought to focus the attention on central aspects, such as the weapon
used, and hinder a full processing of the situation. It is thought that
changes in the perfusion of limbic brain structures that coincide with the
high arousal and/or anxiety, such as the amygdala and the hippocam-
pus, can lead to fragmented memories and personality fragmentation
(Spiegel, 1989; Van Der Kolk, Burbridge, & Suzuki, 1997). Narratives
should be written according to these notions.
(6) In all imaging studies in traumatic recall, the patient anticipates the
presentation of trauma (-related) material, and some researchers have
performed a dry run with the patient. Then the subject is not ‘‘cold’’ to
NEUROIMAGING AND HYPNOSIS 291
the trauma cue. It needs to be taken into account that this may dampen
the activation of the brain when exposed to the challenge.
(7) Last, in addition to the first observation of this section, many clinicians
have described a ‘‘dissociative’’ or ‘‘hypnotic’’ blocking of perceptual
aspects as an adaptive response to trauma. Pain in recall can be blocked,
time processing can be distorted, or processing of the perception of
emotions like threat cannot be adequately processed. Patients may
dissociate during the experience and unless this is assessed at each
between-scan interval (to assess whether this is a positive or negative
phenomenon, see Lanius et al., 2002; Nijenhuis et al., 2002) it may
explain a difference in participant responding. In case patients do
dissociate, a systematic procedure needs to be administered to help
reorient them to the common environment and enable them to continue
with the scanning procedure reliably. In PET protocols, this is especially
important since the production of radioactive material is delivered in a
time-wise manner, and typically each interscan interval is set to 10
minutes.
FUNCTIONAL BRAIN IMAGING RESULTS IN TRAUMATIC
RECALL IN TRAUMA DISORDERS
To date, 12 imaging studies that used a symptom provocation
paradigm in PTSD have been published. Seven studies used PET
(Bremner, Narayan, et al., 1999; Bremner, Staib, et al., 1999; Osuch
et al., 2001; Pissiota et al., 2002; Rauch et al., 1996; Shin et al., 1997, 1999),
three used fMRI (Lanius et al., 2001, 2002; Rauch et al., 2000), and two
used SPECT as imaging technique (Liberzon et al., 1999; Zubieta et al.,
1999). The design, patient population, induction method, measure of
recall, psychophysiological coregistration, and changes in brain me-
tabolism are tabulated in Table 1. These studies have used various chal-
lenge models, exposing the subject – at varying levels of complexity –
to perceptual stimulations that range from exposing patients to slides
and sounds, smells of trauma-related experiences, to reading narrative
scripts, to the administration of pharmacologic agents like yohimbine
(see reviews by Bremner, 2002; Hull, 2002). Reexperiencing of traumatic
events typically coincides with heightened attention, lack of awareness
for the surroundings, and loss of perception of time. At the same time,
emotions of fear, shame, disgust, anger, and sadness, may occur and
sometimes coincide with dissociation, freezing, and other psychophy-
siological arousal phenomena (Nijenhuis et al., 1998).
The first PET studies in traumatic recall used combat slides and
sounds and script-driven imagery in PTSD patients. The results sug-
gested that symptoms associated with traumatic recall were mediated
by the limbic and paralimbic systems within the right hemisphere.
Activation of visual cortex corresponded to the visual component of
PTSD reexperiencing phenomena (Rauch et al., 1996). When generating
Note. TC ¼ trauma controls, HC ¼ healthy controls, HR ¼ heart rate, GSR ¼ Galvanic Skin Response, SUDS ¼ Subjective Units of Distress,
PAG ¼ periaquaductal gray, ri ¼ right, le ¼ left, act ¼ n accumbens, VAS ¼ visual analog scale, CADSS ¼ Clinician Administrated Dissociative Symptom
Scale, STAIS ¼ State-Trait Anxiety Inventory Trait Test, MVA ¼ Motor Vehicle Accident, VVIQ ¼ vividness visual imagery questionnaire.
mental images of combat-related pictures, increased regional cerebral
blood flow (rCBF) in the ventral anterior cingulate cortex (ACC) and
right amygdala was seen; when viewing combat pictures, subjects with
PTSD showed decreased rCBF in Broca’s area (Shin et al., 1997). These
first PET studies of traumatic recall in PTSD have since led to a rapid
increase in similar studies modifying the experimental condition and/
or study population.
There is overlap but also considerable diversity in various traumatic
recall studies. The ACC, middle and superior temporal, middle frontal,
right orbitofrontal, occipital, hippocampal, parahippocampal, anterior
temporal, and inferior frontal cortices have all been implicated in
different studies, demonstrating either increases or decreases in perfu-
sion depending on the study conditions and sample population
(Phillips et al., 2003a, 2003b). In general, in comparison to trauma-
control subjects, these studies reveal an exaggerated response activa-
tion in the right (Rauch et al., 1996; Shin et al., 1997) or left (Liberzon
et al., 1999) amygdala, and in the sensorimotor cortex (Bremner,
Narayan, et al., 1999; Shin et al., 1997) and attenuated responses within
the medial prefrontal cortex (mPFC) (Bremner, Narayan, et al., 1999;
Shin et al., 1999) in patients with PTSD. In line with this, imaging
studies of normal autobiographical memory (i.e., no emotional activa-
tion) in healthy subjects compared to memory-control tasks have
pointed to mPFC and (left) hippocampus that are just particularly
responsive to such memories (Conway et al., 1999); other studies point
to right frontal cortices, medial parietal cortex, and cerebellum (Nyberg,
Forkstam, Petersson, Cabeza, & Ingvar, 2002).
Current studies support a model of PTSD in which (a) the amygdala
is hyperresponsive to threat-related stimuli, and (b) interconnected
areas may provide insufficient ‘‘top-down’’ inhibition by mPFC and
ACC of amygdala response. This relative dysfunction of mPFC and
ACC is thought to lower the threshold of amygdala response to fearful
stimuli and is central to symptom mediation (Pitman, Shin, & Rauch,
2001; Villarreal & King, 2001). Thus, dysfunction of the mPFC areas
may provide a neural correlate of a failure of extinction of fearful
stimuli in PTSD.
Recall induction of emotion specifically activated the ACC. This
brain structure is critically involved in cognitive induction of emo-
tional responses and processes attention, executive functions, and
semantic and episodic memory. ACC activation represents a normal
brain response to traumatic stimuli that serves to inhibit feelings of
fearfulness when there is no true threat. Failure of activation in this
area and/or decreased blood flow in the adjacent subcallosal gyrus
(area 25) may lead to increased fearfulness that is not appropriate for
the context, facilitating exaggerated emotional and behavioral re-
sponses (hyperarousal) to conditioned stimuli (Hamner, Lorberbaum,
296 ERIC VERMETTEN AND J. DOUGLAS BREMNER
& George, 1999). Posterior cingulate cortex (PCC) and motor cortex
and anterolateral prefrontal cortex are also known to modulate
emotion and fear responsiveness (Bremner, 2002). PCC plays an
important role in visuospatial processing and is therefore an impor-
tant component in the preparation for coping with a physical threat.
PCC also has functional connections with the hippocampus and
adjacent cortex.
In a meta-analysis of PET and fMRI studies of general emotional
activation reviewing 43 PET and 12 fMRI activation studies spanning
almost a decade of research, Phan, Wager, Taylor, and Liberzon (2002)
describe brain areas that are involved in emotion induction with
cognitive demand, typical paradigms of the recall of autobiographical
elements or visual imagery: