Dysregulation
of the Right Brain:
A Fundamental Mechanism of Traumatic Attachment and the
Psychopathogenesis of Posttraumatic Stress Disorder
Allan N. Schore
|
Originally published in: Australian and New Zealand
Journal of Psychiatry, 2002, 36, 9-30. Reprinted at www.trauma-pages.com
with permission of the author.
Correspondence: Allan N. Schore, Department of Psychiatry and
Biobehavioral Sciences, University of California at Los Angeles School of
Medicine, 9817 Sylvia Avenue, Northridge, California 91324. Phone: 818
886-4368; Fax 818 349-4404; Email: anschore@aol.com
|
Abstract
Objective: This review
integrates recent advances in attachment theory, affective neuroscience,
developmental stress research, and infant psychiatry in order to delineate the
developmental precursors of posttraumatic stress disorder.
Method: Existing
attachment, stress physiology, trauma, and neuroscience literatures were
collected using Index Medicus/Medline and Psychological Abstracts.
This converging interdisciplinary data was used as a theoretical base for
modeling the effects of early relational trauma on the developing central and
autonomic nervous system activities that drive attachment functions.
Results: Current
trends that integrate neuropsychiatry, infant psychiatry, and clinical
psychiatry are generating more powerful models of the early genesis of a
predisposition to psychiatric disorders, including PTSD. Data are
presented which suggest that traumatic attachments, expressed in episodes of
hyperarousal and dissociation, are imprinted into the developing limbic and
autonomic nervous systems of the early maturing right brain. These enduring
structural changes lead to the inefficent stress coping mechanisms that lie at
the core of infant, child, and adult posttraumatic stress disorders.
Conclusions: Disorganized-disoriented
insecure attachment, a pattern common in infants abused in the first two years
of life, is psychologically manifest as an inability to generate a coherent
strategy for coping with relational stress. Early abuse negatively impacts the
developmental trajectory of the right brain, dominant for attachment, affect
regulation, and stress modulation, thereby setting a template for the coping
deficits of both mind and body that characterize PTSD symptomatology. These
data suggest that early intervention programs can significantly alter the
intergenerational transmission of postttraumatic stress disorders.
Key words: attachment,
right brain, child abuse, dissociation, trauma.
A
recent large, nationally representative study reports that 60% of men and 50%
of women experience a traumatic event at some point in their lives [1]. And yet
this same study finds that estimates of lifetime posttraumatic stress disorder
(PTSD) are 5% for men and 10% for women. Other research indicates that roughly
only one half of those who have an episode of PTSD develop chronic symptoms of
the disorder [2]. These data underscore a central problem -- although trauma is
a common element of many if not most lives, why do only a certain minor
proportion of individuals exposed to the various forms of trauma develop
chronic pathological reactions of mind and body to catastrophic life events?
A
major change in our approach to this problem is reflected in the shift from
DSM-III-R where the severity of the trauma was considered to be the key factor
in precipitating PTSD, to DSM-IV where characteristics of the victim, including
the reaction to the trauma, is emphasized. In other words, the etiology of PTSD
is best understood in terms of what an individual brings to a traumatic event
as well as what he or she experiences afterward, and not just the nature of the
traumatic event itself [3]. This clearly implies that certain personality
patterns are specifically associated with the unique ways individuals cope or
fail to cope with stress.
Current
psychobiological research on PTSD echoes this principle [4]:
Although
many people are exposed to trauma, only some individuals develop PTSD; most do
not. It is possible that humans differ in the degree to which stress induces
neurobiological perturbations of their threat response systems, which may
result in a differential capacity to cope with aversive experiences (p.
412)…These individual differences exist before trauma exposure and may be used
to test constructs of stress hardiness and stress vulnerability in humans (p.
420).
There
is now agreement that the developmental stage at the time of exposure [5] and
the specific type of trauma exposure [6] are essential factors in PTSD, and yet
they have been de-emphasized in the recent literature [7]. Highlighting these
factors however, brings into the foreground a number of fundamental issues.
What are the short- and long-lasting effects of trauma in the earliest developmental
stages, why does this exposure negatively impact the maturation of the
individual’s stress coping systems, and how is this related to the genesis of
premorbid personality organizations vulnerable to posttraumatic stress
disorder? These questions, which lie at the core of trauma theory, direct
clinical psychiatry into the realms of child and especially infant psychiatry.
Attachment
and the Development of Right Brain Stress Coping Mechanisms
In
fact the exploration of the early development of adaptive coping mechanisms and
of the personality is at the core of attachment theory, "the dominant
approach to understanding early socioemotional and personality development
during the past quarter-century of research" [8, p.145]. In his
groundbreaking volume, Attachment, John Bowlby [9] hypothesized
that the infant’s "capacity to cope with stress" is correlated with
certain maternal behaviors, and that attachment outcome has consequences that
are "vital to the survival of the species." Bowlby’s speculation
that, within the attachment relationship, the mother shapes the development of
the infant’s coping responses is now supported by a large body of experimental
studies that characterize maternal care and the development of stress responses
[10], and the influence of maternal factors on the ontogeny of the
limbic-hypothalamic-pituitary-adrenal axis [11].
Recent
developmental psychobiological models indicate that,
An
individual’s response to stressful stimuli may be maladaptive producing
physiological and behavioral responses that may have detrimental consequences,
or may be adaptive, enabling the individual to better cope with stress. Events
experienced early in life may be particularly important in shaping the
individual’s pattern of responsiveness in later stages of life [12, p. 1435].
These
"events" are attachment experiences, shaped by the interaction of the
infant’s innate psychophysiological predispositions and the social environment
of maternal care [13-22].
Furthermore,
current basic stress research suggests that deprivation of maternal care
represents a source of ‘stressful environmental information’ for the
developmental, maturational pattern of the neural circuitry of the infant’s
stress system [23]. This complements studies indicating that pre- or postnatal
stressors negatively impact later mental health, especially when maternal care
is absent. Such work is derivative of attachment theory’s deep interest in the
etiology of not only normal but also abnormal development. In applying the
theory to links between stress coping features and psychopathology Bowlby [24]
proposed:
In
the fields of etiology and psychopathology [attachment theory] can be used to
frame specific hypotheses which relate different family experiences to
different forms of psychiatric disorder and also, possibly, to the
neurophysiological changes that accompany them.
In
this work I will apply this central principle of attachment theory to the
etiology of posttraumatic stress disorder. Although etiological models of PTSD
have centered primarily on childhood sexual abuse, I will suggest that an
increased focus on the neurobiological consequences of relational abuse and
dysregulated infant attachment can offer a deeper understanding of the
psychoneurobiological stress coping deficits of both mind and body that define
the symptomatic presentation of the disorder.
Stress and the
Right Hemisphere
A
growing body of current evidence shows that the neural circuitry of the stress
system is located in the early developing right brain, the hemisphere that is
dominant for the control of vital functions that support survival and the human
stress response [25]. Because stress coping strategies are deeply connected
into essential organismic functions, they begin their maturation pre- and
postnatally, a time of right brain dominance [26]. A very recent MRI study of
infants reports that the volume of the brain increases rapidly during the first
two years, that normal adult appearance is seen at 2 years and all major fiber
tracts can be identified by age 3, and that infants under 2 years show higher
right than left hemispheric volumes [27]. Attachment experiences of the first 2
years thus directly influence the experience-dependent maturation of the right
brain [14, 21, 28-32]. These include experiences with a traumatizing caregiver,
which are well known to negatively impact the child’s attachment security,
stress coping strategies, and sense of self [33, 34].
Indeed,
current studies in developmental traumatology now conclude that "the
overwhelming stress of maltreatment in childhood is associated with adverse
influences on brain development" [35, p. 1281]. This
"maltreatment" specifically refers to the severe affect dysregulation
of the two dominant forms of infant trauma - abuse and neglect. There is much
support for the principle that social stressors are far more detrimental than
non-social aversive stimuli [36], and therefore attachment or "relational
trauma" from the social environment has more negative impact upon the
infant brain than assaults from the nonhuman or inanimate, physical
environment. And so it is now being emphasized that specifically a
dysfunctional and traumatized early relationship is the stressor that
leads to PTSD, that severe trauma of interpersonal origin may override any
genetic, constitutional, social, or psychological resilience factor, and that
the ensuing adverse effects on brain development and alterations of the
biological stress systems may be regarded as "an environmentally induced
complex developmental disorder" [37].
The
fact that such trauma is "ambient" clearly suggests that the infant
is frequently experiencing not single episode or acute but
"cumulative" and chronic unpredictable traumatic stress in his very
first interactions with another human. The stress literature, which is now
investigating "determinants of individual differences in stress reactivity
in early development" clearly shows that acute stress produces short-term
and reversible deficits, while repeated, prolonged, chronic stress is
associated with long-term patterns of autonomic reactivity, expressed in
"neuronal structural changes, involving atrophy that might lead to
permanent damage, including neuronal loss" [38, p. 183]. Consonant with
this principle, in earlier writings I have suggested that early relational
trauma has a significant negative impact on the experience-dependent maturation
of the right brain, which is in a critical period of growth during the same
temporal intervals as dyadic attachment experiences [14, 39-44].
Because
the early developing right hemisphere is, more so than the later maturing left,
deeply interconnected into the autonomic, limbic, and arousal systems, it is
dominant for the processing of social emotional and bodily information [14,
45-47]. A large number of studies now indicate that this hemisphere is dominant
not only for the reception [48-51], expression [52], and communication [53] of
emotion, but also for the control of spontaneously evoked emotional reactions
[54], the modulation of "primary emotions" [55], and the adaptive
capacity for the regulation of affect [14, 18, 56].
It
has been said that the most significant consequence of the stressor of early
relational trauma is the lack of capacity for emotional self-regulation [57],
expressed in the loss of the ability to regulate the intensity and duration of
affects [58]. Basic developmental neuropsychobiological studies now indicate
that perinatal distress leads to a blunting of the stress regulating response
of the right (and not left) prefrontal cortex that is manifest in adulthood
[59]. In light of the essential role of the right hemisphere in the human
stress response, this psychoneurobiological conception of trauma-induced right
brain pathogenesis bears upon recent data which suggest that early adverse
experiences result in an increased sensitivity to the effects of stress later
in life and render an individual vulnerable to stress-related psychiatric
disorders [60]. Affect dysregulation is now seen to be a fundamental mechanism
of all psychiatric disorders [61].
A
developmental neuropsychopathological perspective dictates that "To
understand neuropsychological development is to confront the fact that the
brain is mutable, such that its structural organization reflects the history of
the organism" [62. p. 297]. A history of early relational traumatic stress
is specifically imprinted into the right brain, which is dominant for
"autobiographical" [63] or "personal" [64] memory. Terr
[65] writes that literal mirroring of traumatic events by behavioral memory can
be established at any age, including infancy. This developmental model suggests
that traumatic attachments, occurring in a critical period of organization of
the right brain, will create an enduring vulnerability to dysfunction during
stress and a predisposition to posttraumatic stress disorders.
Right Brain
Dysregulation, Dissociation, and PTSD Pathogenesis: Introduction
Indeed,
in 1996 van der Kolk [66] proposed that the symptoms of PTSD fundamentally
reflect an impairment of the right brain, known to be dominant for inhibitory
control [67]. This hypothesis subsequently received experimental support in a
number of studies [68-70]. In this same period dysfunction of the frontal
lobes, specifically the orbitofrontal system that is expanded in the right
hemisphere [71] and controls instinctive emotional responses through cognitive
processes, was also implicated in PTSD [72-75]. This line of research has
continued in very recent studies that show right hemispheric and orbitofrontal
dysfunction in PTSD [69, 76-79].
The
emotional disturbances of PTSD have been suggested to have their origins in the
inability of the right prefrontal cortex to modulate amygdala functions [18,
44, 80, 81], especially activity of the right amygdala [82], known to process
frightening faces [83, 84] and "unseen fear" [85]. LeDoux concludes
that without orbital prefrontal feedback regarding the level of threat, the
organism remains in an amygdala-driven defensive response state longer than
necessary [86], that in humans, conditioned fear acquisition and extinction are
associated with right hemisphere dominant amygdala function [87], and that a
defective orbitofrontal system operates in PTSD [88].
In
the present period we are also seeing a parallel interest in developmental
research on the etiology of the primitive defense that is used to cope with
overwhelming affective states -- dissociation. From the perspective of
developmental psychopathology, an outgrowth of attachment theory that
conceptualizes normal and aberrant development in terms of common underlying
mechanisms, dissociation is described as offering "potentially very rich
models for understanding the ontogeny of environmentally produced psychiatric
conditions" [89, p. 582]. Disorganized-disoriented insecure attachment, a
primary risk factor for the development of psychiatric disorders [90], has been
specifically implicated in the etiology of the dissociative disorders [91].
Neuroscience
is now delving into the neurobiology of dissociation, especially in infancy
[44, 92]. It is currently thought that dissociation at the time of exposure to
extreme stress signals the invocation of neural mechanisms that result in
long-term alterations in brain functioning [93]. This principle applies to
long-term alterations in the developing brain, especially the early maturing
right brain, the locus of dissociation [44, 94], withdrawal and avoidance [95],
and a spectrum of psychiatric disorders [29, 39, 96].
Traumatic
Attachment, Dysregulation, and the Pathogenesis of PTSD
Bowlby
postulated that the major negative impact of early traumatic attachments is an
alteration of the organism’s normal developmental trajectory. Over 30 years ago
he wrote [9],
[S]ince
much of the development and organization of [attachment] behavioral systems
takes place whilst the individual is immature, there are plenty of occasions
when an atypical environment can divert them from developing on an adaptive
course.
And
seventy years earlier, Pierre Janet [97] proposed
All
[traumatized] patients seem to have the evolution of their lives checked; they
are attached to an unsurmountable object. Unable to integrate traumatic
memories, they seem to have lost their capacity to assimilate new experiences
as well. It is...as if their personality development has stopped at a certain
point, and cannot enlarge any more by the addition of new elements.
Janet
further postulated that the psychological consequence of trauma is the
breakdown of the adaptive mental processes leading to the maintenance of an
integrated sense of self. Again, recent studies indicate that the right
hemisphere is central to self-recognition [98] and the ability to maintain a
coherent, continuous, and unified sense of self [47], but it also is the locus
of various self-regulation pathologies [14, 29, 30].
The
concept of regulation, now shared by the attachment, PTSD, neuroscience, and
psychiatric literatures, may be a bridging concept for expanding a
biopsychosocial model of psychiatry. According to Taylor, Bagby, and Parker,
The
concept of disorders of affect regulation is consistent with a growing
realization in medicine and psychiatry that most illnesses and diseases are the
result of dysregulations within the vast network of communicating systems that
comprise the human organism [61, p. 270].
A
model of the interactive genesis of psychobiological dysregulation also
supports and provides a deeper understanding of the diathesis-stress concept -
that psychiatric disorders are caused by a combination of a
genetic-constitutional predisposition and environmental or psychosocial stressors
that activate the inborn neurophysiological vulnerability. The unique
contributions of the intrinsic psychobiological perspective of trauma studies
to both clinical psychiatry and neuroscience is articulated by McFarlane :
[T]he
origins of psychiatry in medicine tie the discipline strongly to its biological
roots. The field of traumatic stress has the potential to bridge this
divide…Traumatic stress as a field, has the capacity to show the future
direction of functional neurobiology [99, p. 900, 901].
In
a recent editorial in the American Journal of Psychiatry entitled
"The development of neurodevelopmental psychiatry," Rapoport [100]
calls for deeper studies of the association between pre/perinatal adverse
events or stressors and adult psychiatric outcomes. Towards that end, in the
following I will suggest that recent theoretical models linking developmental
affective neuroscience and attachment theory, updated basic research in
biological psychiatry on stress mechanisms, and current advances in psychophysiology
on the survival functions of the autonomic nervous system may offer us a deeper
understanding of the underlying mechanisms by which early childhood trauma
massively dysregulates and thereby alters the developmental trajectory of the
right hemisphere. This results in an immature personality organization with
vulnerable coping capacities, one predisposed to the pathological hyperarousal
and dissociation that characterizes PTSD at later points of stress. These
psychoneurobiological models, which link infant, child, and adolescent
psychiatry, are offered as heuristic proposals that can be evaluated by
experimental and clinical research.
Overview
of the Neurobiology of a Secure Attachment
The
essential task of the first year of human life is the creation of a secure
attachment bond of emotional communication between the infant and the primary
caregiver. In order to enter into this communication, the mother must be
psychobiologically attuned to the dynamic crescendos and decrescendos of the
infant’s bodily-based internal states of autonomic arousal. During the
sequential signalling of play episodes mother and infant show sympathetic
cardiac acceleration and then parasympathetic deceleration in response to the
smile of the other, and thus the language of mother and infant consist of
signals produced by the autonomic, involuntary nervous system in both parties
[101]. The attachment relationship mediates the dyadic regulation of emotion
[102], wherein the mother co-regulates the infant’s postnatally developing
autonomic nervous system. Also known as the vegetative nervous system, from the
Latin, vegetare, to animate or bring to life, it is responsible for the
generation of what Stern [103] calls vitality affects.
In
heightened affective moments each partner learns the rhythmic structure of the
other and modifies his or her behavior to fit that structure, thereby
co-creating a specifically fitted interaction. In play episodes of affect
synchrony, the pair are in affective resonance, and in such, an amplification
of vitality affects and a positive state occurs especially when the mother’s
psychobiologically attuned external sensory stimulation frequency coincides
with the infant’s genetically-encoded endogenous rhythms. And in moments of
interactive repair the "good-enough" caregiver who induces a stress
response in her infant through a misattunement, reinvokes in a timely fashion a
reattunment, a regulation of the infant’s negative state. Maternal sensitivity
thus acts as an external organizer of the infant’s biobehavioral regulation
[104].
If
attachment is the regulation of interactive synchrony, stress is defined as an
asynchrony in an interactional sequence, and, following this, a period of
re-established synchrony allows for stress recovery and coping. The regulatory
processes of affect synchrony that creates states of positive arousal and
interactive repair that modulates states of negative arousal are the
fundamental building blocks of attachment and its associated emotions, and
resilience in the face of stress is an ultimate indicator of attachment
security. Attachment, the outcome of the child’s genetically encoded biological
(temperamental) predisposition and the particular caregiver environment, thus
represents the regulation of biological synchronicity between organisms, and
imprinting, the learning process that mediates attachment, is defined as
synchrony between sequential infant-maternal stimuli and behavior.
The
optimally regulated communications embedded in secure attachment experiences
directly influence the maturation of both the postnatally maturing central
nervous system (CNS) limbic system that processes and regulates
social-emotional stimuli and the autonomic nervous system (ANS) that generates
the somatic aspects of emotion. The limbic system derives subjective
information in terms of emotional feelings that guide behavior [105], and
functions to allow the brain to adapt to a rapidly changing environment and
organize new learning [106]. As mentioned, the higher regulatory systems
of the right hemisphere form extensive reciprocal connections with the limbic
and autonomic nervous systems [107, 108]. Both the ANS and the CNS continue to
develop postnatally, and the assembly of these limbic-autonomic circuits [109]
is directly influenced by the attachment relationship [14, 18]. In this manner,
the internalized regulatory capacities of the infant develop in relation to the
mother, and thus, as Bowlby suggested, the mother shapes the infant’s stress
coping systems.
Attachment and
Right Cortical Regulation of the Autonomic Nervous System
In
his original formulation Bowlby [9] described a neurophysiological control
system that is centrally involved in regulating instinctive attachment behavior
[31, 101]. In a number of writings I indicate that this system is located in
the right orbitofrontal area and its cortical and subcortical connections [14,
16, 18, 29, 31, 45, 56, 110]. Due to its position at the interface of the
cortex and subcortex, this ventromedial cortex sits at the highest level of the
limbic system. It directly connects into the subcortical reticular formation,
thus regulating arousal, a central component of all emotional states. Indeed
this prefrontal system acts the highest level of control of behavior,
especially in relation to emotion [111]. Referred to as "the thinking part
of the emotional brain," it is situated at the hierarchical apex of what
is now referred to as the "rostral limbic system" [112], or
"anterior limbic prefrontal network" [113], which also includes the
anterior cingulate (medial frontal cortex) and the amygdala [18, 45]. This
"Senior Executive" of the social-emotional brain comes to act in the
capacity of an executive control function for the entire right brain, the locus
of the emotional self [47].
But
in addition, the orbitofrontal cortex also represents the apex of the hierarchy
of control of autonomic functions [114]. Due to its direct connections into the
hypothalamus, the head ganglion of the ANS, it functions as a cortical control
center of involuntary bodily functions that represent the somatic components of
all emotional states, and acts to control autonomic responses associated with
emotional events [115]. Recent studies demonstrate that operation of the right
prefrontal cortex is integral to autonomous regulation, and that the right
hemisphere is dominant for the processing and regulation of self-related
information and the corporeal self [14, 45, 47, 98, 116].
In
optimal early environments that promote secure attachments, a right lateralized
regulatory system organizes with a capacity to modulate, under stress, a
flexible coping pattern of shifting out of autonomic balance into a coupled
reciprocal autonomic mode of control in which homeostatic increases in the
activity in one ANS division are associated with decreases in the other [117].
The two components of the centrally regulated ANS are known to be distinct
modular circuits that control arousal expressions, with the catabolic
sympathetic branch responsible for energy-mobilizing excitatory activity and the
anabolic parasympathetic branch involved in energy-conserving inhibitory
activity. These dissociable autonomic functions reflect the sympathetic
catecholaminergic stimulation of glycogenolysis and parasympathetic vagal and
cortisol stimulation of glycogenesis [118-120].
In
light of the fact that primordial representations of body states are the
building blocks and scaffolding of development [121], the current intense
interest in emotional development is now beginning to focus increasing
attention upon changes in bodily state, mediated by the ANS, that are crucial
to ongoing emotional experience. The right hemisphere, dominant for
somatosensory processing [122], predominantly controls both sympathetic and
parasympathetic activity [123, 124]. The ANS, by regulating the strength of the
heartbeat and controlling vascular calibre, performs a critical role in
ensuring that bloodflow is adequate to supply oxygen and nutrients to the
bodily organs and the brain, according to their relative needs.
A
quick review of the ANS indicates that the sympathetic branch is activated by
any stimulus above an organismic threshold, and that it functions to increase
arousal, trigger an immediate anticipatory state, and rapidly mobilize
resources in response to appraised stressors. Physiological activation is
expressed in the conversion of glycogen to glucose and elevation of blood sugar
for increased energy, quicker and stronger heart beat, increased blood supply
to the muscles, dilation of bronchii and increases in breathing rate, dilation
of the pupils, increased sweating, and speeding up of mental activity. The
opposing parasympathetic branch has a higher threshold of activation and thus
initiates its operations after the sympathetic, and its adaptive functions are
expressed in slowing the heart rate, relaxing the muscles, lowering blood
pressure, and pupillary constriction. Its operations allow for breathing to
return to normal rates, increases in digestion, onset of bowel and bladder
activities, and re-establishment of immune functions.
An
autonomic mode of reciprocal sympathetic-parasympathetic control is
behaviorally expressed in an organism that responds alertly and adaptively to a
personally meaningful (especially social) stressor, yet as soon as the context
is appraised as safe, immediately returns to the relaxed state of autonomic
balance. In very recent thinking, the ANS is not only sensitive to
environmental demands and perceived stresses and threats, but will, in a
predictable order, also rapidly reorganize to different neural-mediated states
[125, p. 20). These ANS changes are regulated by "higher" limbic
structures in the CNS. Indeed, the orbitofrontal cortex acts as a major center
of CNS control over the sympathetic and parasympathetic branches of the ANS
[126], and thereby regulates autonomic responses to social stimuli [127], the
intuitive "gut feelings" that an individual has to other humans.
These right lateralized connections also mediate the adaptive capacity of
empathically perceiving the emotional states of other human beings [14, 18, 29,
110, 128].
The
early forming right hemisphere stores an internal working model of the
attachment relationship [14, 21] that determines the individual’s
characteristic strategies of affect regulation for coping and survival [14,
20]. This working model is encoded in implicit memory, which is primarily
regulatory, automatized, unconscious [129], and right lateralized [130]. This
right frontal system thus plays a unique role in the regulation of motivational
states and the adjustment or correction of emotional responses. It acts as a
recovery mechanism that monitors and regulates the duration, frequency, and
intensity of not only positive but also negative affect states.
In
the securely attached individual this representation encodes an implicit
expectation that homeostatic disruptions will be set right, allowing the child
to self-regulate functions which previously required the caregiver's external
regulation. In this manner, emotion is initially regulated by others, but over
the course of early development it becomes increasingly self-regulated as a
result of neurophysiological development [131]. These adaptive capacities are
central to self-regulation, the ability to flexibly regulate emotional states
through interactions with other humans -- interactive regulation in
interconnected contexts, and without other humans -- autoregulation in
autonomous contexts.
The
orbitofrontal attachment control system is specialized to play a critical role
in strategic memory by supporting the early mobilization of effective
behavioral strategies in novel or ambiguous situations [132]. Operating at
levels beneath awareness, it is activated when there is insufficient
information available to determine the appropriate course of action, and is specialized
to act in contexts of "uncertainty or unpredictability" [133], an
operational definition of stress. Efficient orbitofrontal operations organize
the expression of a regulated emotional response and an appropriate
motivational state for a particular social environmental context, and in this
fashion it contributes to "judicious, adapted behavior" [115].
Anatomical, electrophysiological, and imaging studies indicate that the
orbitofrontal functions are central to "the integration of past, present,
and future experiences, enabling adequate performance in behavioral tasks,
social situation, or situations involving survival" [134, p. 356]. As
mentioned earlier, current neuroscience research indicates that these same
adaptive stress-survival capacities are severely impaired in infant, child, and
adult posttraumatic stress disorders.
The
Neurobiology of Infant Trauma
It
is important to stress that the developmental attainment of an efficient
internal system that can adaptively regulate various forms of arousal and
psychobiological states, and thereby affect, cognition, and behavior, only
evolves in a growth-facilitating emotional environment. The good-enough mother
of the securely attached infant permits access to the child after a separation
and shows a tendency to respond appropriately and promptly to his/her emotional
expressions. She also allows for the interactive generation of high levels of
positive affect in co-shared play states. These regulated events allow for an
expansion of the child’s coping capacities, and account for the principle that
security of the attachment bond is the primary defense against trauma-induced
psychopathology.
In
contrast to this scenario is a relational growth-inhibiting early environment,
in which the abusive caregiver not only shows less play with her infant, but
also induces traumatic states of enduring negative affect in the child. Because
her attachment is weak, she provides little protection against other potential
abusers of the infant, such as the father. This caregiver is inaccessible and
reacts to her infant's expressions of emotions and stress inappropriately
and/or rejectingly, and therefore shows minimal or unpredictable participation
in the various types of arousal regulating processes. Instead of modulating she
induces extreme levels of stimulation and arousal, very high in abuse and/or
very low in neglect. And because she provides no interactive repair the
infant’s intense negative states last for long periods of time.
The
enduring detrimental effects of parent-inflicted trauma on the attachment bond
is now well-established:
The
continued survival of the child is felt to be at risk, because the actuality of
the abuse jeopardizes (the) primary object bond and challenges the child’s
capacity to trust and, therefore, to securely depend [135, p. 62].
Freyd
[136], in describing the effects of childhood abuse and attachment, refers to
"betrayal trauma theory."
In
contexts of relational trauma the caregiver(s), in addition to dysregulating
the infant, withdraw any repair functions, leaving her for long periods in an
intensely disruptive psychobiological state that is beyond her immature coping
strategies. In studies of a neglect paradigm, Tronick and Weinberg [137, p. 56]
describe:
When
infants are not in homeostatic balance or are emotionally dysregulated (e.g.,
they are distressed), they are at the mercy of these states. Until these states
are brought under control, infants must devote all their regulatory resources
to reorganizing them. While infants are doing that, they can do nothing else.
The
"nothing else" these authors refer to is a failure to continue to
develop. These infants forfeit potential opportunities for socioemotional
learning during critical periods of right brain development [44].
Indeed,
we now know that trauma causes biochemical alterations within the developing
brain [39]. The infant’s psychobiological response to trauma is comprised of
two separate response patterns, hyperarousal and dissociation [44, 138]. In the
initial stage of threat, a startle or an alarm reaction is initiated, in which
the sympathetic component of the ANS is suddenly and significantly activated,
resulting in increased heart rate, blood pressure, and respiration. Distress is
expressed in crying and then screaming. In very recent work, this dyadic
transaction is described by Beebe as "mutually escalating
overarousal" of a disorganized attachment pair (139, p. 436]:
Each
one escalates the ante, as the infant builds to a frantic distress, may scream,
and, in this example, finally throws up. In an escalating overarousal pattern,
even after extreme distress signals from the infant, such as ninety-degree head
aversion, arching away...or screaming, the mother keeps going.
The
infant’s state of "frantic distress," or what Perry terms fear-terror
is mediated by sympathetic hyperarousal, expressed in increased levels of the
brain’s major stress hormone, corticotropin releasing factor, which in turn
regulates sympathetic catecholamine activity [140], and so brain adrenaline,
noradrenaline, and dopamine levels are significantly elevated. Noradrenaline is
also released from the locus coeruleus [141, 142]. The resultant rapid and
intensely elevated catecholamine levels trigger a hypermetabolic state within
the developing brain. Catecholamines are among the first neurochemicals to
respond to stressors in response to perceived threat, and repeated stress
triggers their persistent activation [143]. Prolonged stress and elevated
levels of catecholamines in turn induce high levels of thyroid hormones that
accompany hyperarousal [32, 144]. Thyroid hormones are known to be active
agents in brain differentiation and in the regulation of critical period
phenomena [14, 145, 146].
In addition, increased amounts of
vasopressin are expressed, a hypothalamic neuropeptide associated with
sympathetic activation [147, 148]. This condition is specifically triggered
when an environment is perceived to be unsafe and challenging, and resultant
high levels of vasopressin potentiate immobilization responses via sympathetic
activation, behaviorally expressed as fear [125]. Interestingly, high levels of
this neuropeptide are associated with nausea [149], a finding that may explain
the hyperarousal behaviors observed by Beebe.
But
a second later forming reaction to infant trauma is seen in dissociation, in
which the child disengages from stimuli in the external world and attends to an
"internal" world. The child’s dissociation in the midst of terror
involves numbing, avoidance, compliance and restricted affect (the same pattern
as adult PTSD). Traumatized infants are observed to be "staring off into
space with a glazed look". This behavioral strategy is described by
Tronick and Weinberg [137, p. 66]:
[W]hen
infants’ attempts fail to repair the interaction infants often lose postural
control, withdraw, and self-comfort. The disengagement is profound even with
this short disruption of the mutual regulatory process and break in
intersubjectivity. The infant’s reaction is reminiscent of the withdrawal of
Harlow’s isolated monkey or of the infants in institutions observed by Bowlby
and Spitz.
This
parasympathetic dominant state of conservation-withdrawal occurs in helpless
and hopeless stressful situations in which the individual becomes inhibited and
strives to avoid attention in order to become "unseen" [14, 44]. This
metabolic shutdown state is a primary regulatory process, used throughout the
life span, in which the stressed individual passively disengages in order
"to conserve energies...to foster survival by the risky posture of
feigning death, to allow healing of wounds and restitution of depleted
resources by immobility" [150, p. 213). It is this parasympathetic
mechanism that mediates the "profound detachment" [151] of
dissociation. If early trauma is experienced as "psychic catastrophe"
[152], dissociation represents "detachment from an unbearable
situation" [153], "the escape when there is no escape" [154],
and "a last resort defensive strategy" [155].
Most importantly, the neurobiology of
the later forming dissociative reaction is different than the initial
hyperarousal response. In this passive state pain numbing and blunting
endogenous opiates [156] and behavior-inhibiting stress hormones, such as
cortisol, are elevated. Furthermore, activity of the dorsal vagal complex in
the brainstem medulla increases dramatically, decreasing blood pressure,
metabolic activity, and heart rate, despite increases in circulating
adrenaline. This elevated parasympathetic arousal, a survival strategy [157],
allows the infant to maintain homeostasis in the face of the internal state of
sympathetic hyperarousal.
It
is now known that there are two parasympathetic vagal systems, a late
developing "mammalian" or "smart" system in the nucleus
ambiguus which allows for the ability to communicate via facial expressions,
vocalizations, and gestures via contingent social interactions, and a more
primitive early developing "reptilian" or "vegetative"
system in the dorsal motor nucleus of the vagus that acts to shutdown metabolic
activity during immobilization, death feigning, and hiding behaviors [125,
157]. Porges describes that as opposed to the ventral vagal complex that can
rapidly regulate cardiac output to foster engagement and disengagement with the
social environment, the dorsal vagal complex "contributes to severe
emotional states and may be related to emotional states of ‘immobilization’
such as extreme terror" [157, p. 75]. Perry’s description of the
traumatized infant’s sudden state switch from sympathetic hyperarousal into parasympathetic
dissociation is reflected in Porges’ characterization of
…the
sudden and rapid transition from an unsuccessful strategy of struggling
requiring massive sympathetic activation to the metabolically conservative
immobilized state mimicking death associated with the dorsal vagal complex
[157, p. 75].
Meares
[158] also concludes that in all stages "dissociation, at its first
occurrence, is a consequence of a ‘psychological shock’ or high arousal."
Notice that in the traumatic state, and this may be of long duration, both the
sympathetic energy-expending and parasympathetic energy-conserving components
of the infant’s developing ANS are hyperactivated.
Disorganized/Disoriented
Attachment Neuropsychology
The
next question is, how would the trauma-induced neurobiological and
psychobiological alterations of the developing right brain be expressed in the
socioemotional behavior of an early traumatized toddler? In a classic study,
Main and Solomon [159] studied the attachment patterns of infants who had
suffered trauma in the first year of life. This lead to the discovery of a new
attachment category, "Type D", an insecure-disorganized / disoriented
pattern, one found in 80% of maltreated infants [160]. Indeed this group of
toddlers exhibits higher cortisol levels and higher heart rates than all other
attachment classifications [161, 162].
Main
and Solomon conclude that these infants are experiencing low stress tolerance
and that the disorganization and disorientation reflect the fact that the
infant, instead of finding a haven of safety in the relationship, is alarmed by
the parent. They note that because the infant inevitably seeks the parent when
alarmed, any parental behavior that directly alarms an infant should place it
in an irresolvable paradox in which it can neither approach, shift its
attention, or flee. At the most basic level, these infants are unable to
generate a coherent behavioral coping strategy to deal with this emotional
challenge.
Main
and Solomon documented, in some detail, the uniquely bizarre behaviors these
12-month-old infants show in Strange Situation observations. They note that
these episodes of interruptions of organized behavior are often brief,
frequently lasting only 10-30 seconds, yet they are highly significant. For
example, they show a simultaneous display of contradictory behavior patterns,
such as "backing" towards the parent rather than approaching
face-to-face.
The
impression in each case was that approach movements were continually being
inhibited and held back through simultaneous activation of avoidant tendencies.
In most cases, however, proximity-seeking sufficiently "over-rode"
avoidance to permit the increase in physical proximity. Thus, contradictory
patterns were activated but were not mutually inhibited [159, p. 117].
Notice
the simultaneous activation of the energy expending sympathetic and energy
conserving parasympathetic components of the ANS.
Maltreated
infants also show evidence of apprehension and confusion, as well as very rapid
shifts of state during the stress-inducing Strange Situation. These authors
describe:
One
infant hunched her upper body and shoulders at hearing her mother’s call, then
broke into extravagant laugh-like screeches with an excited forward movement.
Her braying laughter became a cry and distress-face without a new intake of
breath as the infant hunched forward. Then suddenly she became silent, blank
and dazed [159, p. 119].
These
behaviors generalize beyond just interactions with the mother. The intensity of
the baby’s dysregulated affective state is often heightened when the infant is
exposed to the added stress of an unfamiliar person. At a stranger’s entrance,
two infants moved away from both mother and stranger to face the wall, and
another "leaned forehead against the wall for several seconds, looking
back in apparent terror".
These
infants exhibit "behavioral stilling" - that is, "dazed"
behavior and depressed affect, behavioral manifestations of dissociation. One
infant "became for a moment excessively still, staring into space as though
completely out of contact with self, environment, and parent." Another
showed "a dazed facial appearance...accompanied by a stilling of all body
movement, and sometimes a freezing of limbs which had been in motion". Yet
another "fell face-down on the floor in a depressed posture prior to
separation, stilling all body movements".
Furthermore,
Main and Solomon point out that type "D" behaviors take the form of
stereotypies that are found in neurologically impaired infants. These behaviors
are overt manifestations of an obviously impaired regulatory system, one that
rapidly disorganizes under stress. Notice that these observations are taking
place at 12 to 18 months, a critical period of corticolimbic maturation [14],
and they reflect a severe structural impairment of the orbitofrontal control
system that is involved in attachment behavior and state regulation. The
orbitofrontal areas specialize in encoding information [163], especially
information contained in emotionally expressive faces and voices, including
angry and fearful faces [133, 164].
The
mother’s face is the most potent visual stimulus in the child’s world, and it
is well known that direct gaze can mediate not only loving but powerful
aggressive messages. In coding the mother’s frightening behavior Hesse and Main
[165, p. 511] describe "in non-play contexts, stiff-legged ‘stalking’ of
infant on all fours in a hunting posture; exposure of canine tooth accompanied
by hissing; deep growls directed at infant." Thus, during the trauma, the infant
is presented with an aggressive expression on the mother’s face. The image of
this aggressive face, as well as the chaotic alterations in the infant’s bodily
state that are associated with it, are indelibly imprinted into limbic circuits
as a "flashbulb memory," and thereby stored in imagistic procedural
memory in the visuospatial right hemisphere, the locus of implicit [130] and
autobiographical [63] memory.
But
in traumatic episodes the infant is presented with another affectively
overwhelming facial expression, a maternal expression of fear-terror. Main and
Solomon [159] note that this occurs when the mother withdraws from the infant
as though the infant were the source of the alarm, and they report that
dissociated, trancelike, and fearful behavior is observed in parents of type
"D" infants. Current studies show a link between frightening maternal
behavior and disorganized infant attachment [166].
I
suggest that during these episodes the infant is matching the rhythmic
structures of the mother’s dysregulated states, and that this synchronization
is registered in the firing patterns of the stress-sensitive corticolimbic
regions of the infant’s brain that are in a critical period of growth. In light
of the fact that many of these mothers have suffered from unresolved trauma
themselves, this spatiotemporal imprinting of the chaotic alterations of the
mother’s dysregulated state facilitates the downloading of programs of
psychopathogenesis, a context for the intergenerational transmission of trauma.
This represents a fundamental mechanism by which maladaptive parental behavior
mediates the association between parental and offspring psychiatric symptoms
[167], and parental PTSD and parental trauma exposure impact the child’s
development of a risk factor for PTSD [168].
Impact
of Relational Trauma on Right Brain Development
In
an early history of traumatic attachment the developing infant/toddler is too
frequently exposed to a massively misattuning primary caregiver who triggers
and does not repair long lasting intensely dysregulated states. These negative
states reflect severe biochemical alterations in the rapidly maturing right
brain, and because they occur during the brain growth spurt [169], the effect
of ambient cumulative trauma is enduring. In the infant brain, states become
traits [138], and so the effects of early relational trauma as well as the
defenses against such trauma are embedded into the core structure of the
evolving personality. According to Bowlby the effect of an atypical environment
is that development is diverted from its adaptive course. This leads to the
question, what do we now know about the psychopathomorphogenetic mechanisms
that underlie such deflections of normal structural development?
The
developing infant is maximally vulnerable to nonoptimal environmental events in
the period of most rapid brain growth. During these critical periods of
genetically encoded synapse overproduction followed by environmentally-driven
synapse elimination, the organism is sensitive to conditions in the external
environment, and if these are outside the normal range a permanent or
semi-permanent arrest of development occurs. Of particular importance is the
identification of various stressful "growth-inhibiting environments"
that negatively influence the critical period organization of limbic cortical
and subcortical connections that mediate homeostatic self-regulatory and
attachment systems. Disruption of attachment bonds in infant trauma leads to a
regulatory failure, expressed in an impaired autonomic homeostasis,
disturbances in limbic activity, and hypothalamic and reticular formation
dysfunction. Developmental psychobiological studies indicate that hyperaroused
attachment stressors are correlated with elevated levels of the
arousal-regulating catecholamines and hyperactivation of the excitotoxic N-methyl-D-aspartate
(NMDA)-sensitive glutamate receptor, a critical site of neurotoxicity and
synapse elimination in early development [170].
The
relational trauma of infant abuse also triggers significant alterations in the
major stress regulating neurochemicals, corticotropin releasing factor and the
glucocorticoid, cortisol, especially in the right hemisphere that is dominant
for the secretion of these hormones [171, 172]. Yehuda points out that the
actions of these two systems are synergistic: "whereas catecholamines
facilitate the availability of energy to the body’s vital organs, cortisol’s
role in stress is to help contain, or shut down sympathetic activation"
[173, p. 257]. It is now well established that stress hormones are protective
in the short run and yet cause damage when they are overproduced or not shut
off when no longer needed [38]. There is a large body of basic research to show
that both stress hormones are regulated (for better or worse) within the
mother-infant relationship [see reference14].
In
situations where the caregiver routinely does not participate in reparative
functions that re-establish homeostasis, the resulting psychobiological
disequilibrium is expressed in a dysregulated and potentially toxic brain
chemistry, especially in limbic areas that are in a critical period of
synaptogenesis. Indeed, this same interaction between high levels of
catecholamines, excitatory transmitters, and corticosteroids is now thought to
mediate programmed cell death [174], and to represent a primary etiological
mechanism for the pathophysiology of neuropsychiatric disorders (see references
39 and 44 for a detailed account of trauma-induced altered calcium metabolism
and oxidative stress damage in neurons and astroglia in the developing brain).
But
in addition, when the attachment trauma exhausts the infant’s active coping
mechanisms, she shifts into hypoarousal and accesses the ultimate survival
strategy, dissociation, "a submission and resignation to the inevitability
of overwhelming, even psychically deadening danger" [135]. If this primary
metabolic shutdown becomes a chronic condition, it will have devastating
effects on the morphogenesis of limbic structures. Dissociation and
conservation-withdrawal, functional expressions of heightened dorsal vagal
activity, induce an extreme alteration of the bioenergetics of the developing
brain. During critical periods of regional synaptogenesis this would have
growth-inhibiting effects, especially in the right brain which specializes in
withdrawal and contains a vagal circuit of emotion regulation. This is because
the biosynthetic processes that mediate the growth and proliferation of
synaptic connections in the postnatally developing brain demand, in addition to
sufficient quantities of essential nutrients, massive amounts of energy [14,
39, 45]. An infant brain that is chronically shifting into hypometabolic
survival modes has little energy available for growth.
In
describing the dorsal vagal complex Porges states that when all else fails, the
nervous system elects a metabolically conservative course; this strategy may be
adaptive in the short term, but lethal if maintained. He also notes that high
levels of dorsal vagal activation are associated with "potentially life-threatening
bradycardia, apnea, and cardiac arrhythmias" [125, p. 136]. This may
describe stresses on the infant’s cardiovasculature and developing blood-brain
barrier during and after relational trauma. I have suggested that in the
developing brain this "lethality’ is expressed in intensified cell death
in "affective centers" in the limbic system [39].
As
opposed to the excitotoxic cell death associated with elevated levels of
corticosteroids, prolonged and intense dorsal vagal activity may be associated
with profoundly low corticosteroid levels, also known to impair brain
development in limbic structures [175]. Hypocortisolism develops subsequent to
extended periods of elevated cortisol in response to trauma, and adverse
conditions in early life that induce elevated levels of cortisol are now
proposed to contribute to the development of hypocortisolism in adulthood
[176], a known predictor of PTSD [177]. Recall that abused type D infants show
higher cortisol levels than all other attachment classifications [161]. It
should be pointed out that infants raised in a neglectful environment show a
low cortisol pattern of circadian cortisol production [176]. This suggests
different neurobiological impairments and neurophysiological deficits in the
two types of infant trauma – abuse and neglect.
In
other words, the caregiver's dysregulating effect on the infant's internal
state, and her poor capacity to psychobiologically regulate excessive levels of
high and/or low arousal negative affect, defines a pathomorphogenetic
influence. Structural limitations in the mother’s emotion processing right
brain are reflected in a poor ability to comfort and regulate her child’s
affective states, and these experiences, central to the intergenerational
transmission of psychopathology, are stamped into the insecurely attached
infant’s right orbitofrontal system and its cortical and subcortical
connections. Harkness and Tucker [178] state that the early traumatic
experiences of childhood abuse, literally kindle limbic areas. In this manner,
early adverse developmental experiences may leave behind a permanent
physiological reactivity in limbic areas of the brain [179], thereby inhibiting
its capacity to cope with future stressors.
In
light of the fact that males, due to delayed rates of cerebral maturation, are
more susceptible than females to a large number of conditions that impair the
developing brain, and that the limbic system of males and females show
different connectivity patterns, gender differences in developmental traumatology
must be considered. These factors indicate that by nature of their CNS and ANS
immaturity males may be more susceptible to relational abuse, and that the
dysregulation of early abused males is psychobiologically biased more towards
hyperarousal, and females more towards dissociation. These would endure as
permanent limbic reactivities that underlie gender predispositions to
externalizing and internalizing disorders.
The
infant posttraumatic stress disorder episodes of hyperarousal and dissociation
imprint the template for later childhood, adolescent, and adult posttraumatic
stress disorders, all of which show disturbances of autonomic arousal [180],
abnormal catecholaminergic function [181, 182], neurologic soft signs [183],
and dissociation [44]. This would be symptomatically expressed as a cycling
between intrusive hypersympathetically-driven terrifying flashbacks and
traumatic images and parasympathetically-driven dissociation, avoidance, and
numbing. Recent models of PTSD refer to stressor-induced oscillations between
traumatic and avoidant states, and cycling between the bidirectional symptoms
of emotional reexperiencing and emotional constrictedness [184].
Trauma-Induced
Excessive Pruning of Right Brain Circuits
Even
more specifically, social-emotional environments that provide traumatizing
attachment histories retard the experience-dependent development of
frontolimbic regions, especially the right cortical areas that are
prospectively involved in affect regulating functions. These descending projections
from the prefrontal cortex to subcortical structures are known to mature during
infancy, and relational traumatic experiences could induce a severe and
extensive pruning of higher limbic connections (orbitofrontal, anterior
cingulate, and amygdala) into the arousal centers in the reticular formation
and autonomic centers in the hypothalamus via a "kindling" [185]
mechanism (see reference 44, Figure 3).
Relational
trauma-induced developmental overpruning of a corticolimbic system, especially
one that contains a genetically encoded underproduction of synapses, represents
a scenario for high-risk conditions. It is now established that
"psychological" factors "prune" or "sculpt"
neural networks in the postnatal brain. In earlier works I have suggested that
excessive pruning of hierarchical cortical-subcortical circuits operates in the
etiology of a vulnerability to later extreme disorders of affect regulation
[14, 29, 39, 44]. In the last decade, a growing body of neurobiological
research on PTSD has uncovered dysfunctional frontal-subcortical systems [186,
187], and altered functional activity of the orbitofrontal cortex [69, 75],
anterior cingulate [188, 189], and amygdala [68].
An
extensive parcellation of axonal connections between orbitofrontal and catecholaminergic
areas of the midbrain and medullary reticular formation would lead to a
predisposition for arousal dysregulation under stress. At the same time severe
pruning of its hypothalamic connections would lead to inefficient regulation of
the ANS by higher centers in the CNS [39, 44], functionally expressed in a
dissociation of central regulation of sympathetic and
hypothalamic-pituitary-adrenal systems [190]. This loss means that under stress
a coupled reciprocal mode of autonomic control would give way to a coupled
nonreciprocal mode of autonomic control, resulting in an intensely high state
of sympathetic plus parasympathetic arousal. Severe dysregulation of both
central and autonomic arousal is a hallmark of posttraumatic stress disorders.
Supporting
this model, a growing body of research demonstrates orbitofrontal dysfunction
in PTSD [69, 77-79]. Recall, this system is specialized to show a flexible
response in stressful contexts of uncertainty. The right orbitofrontal system
is thought to act as the neural basis by which humans control their instinctive
emotional responses through cognitive processes, and the emotional disturbances
of PTSD are proposed to have their origins in the inability of the right
prefrontal cortex to modulate amygdala functions [80]. What could be the origin
of a defective "rostral limbic system"?
Over
the course of postnatal development connections between the orbitofrontal
cortex and amygdala increase, and this hierarchical organization allows this
prefrontal system to take over amygdala functions [191], and for the right
frontotemporal cortex to maintain inhibitory control over intense emotional
arousal [192]. But early traumatic attachment intensifies the parcellation of
these right lateralized connections, and so in posttraumatic stress disorders,
when orbitofrontal inhibitory control is lost, activity of the right amygdala
[193], known to nonconsciously process frightening faces [83] and "unseen
fear" [85] drives the right brain system. Current work on the neurobiology
of stress suggests that chronic stress contributes to atrophy of specifically
the prefrontal cortex and amygdala [38].
It
is now established that a pathological response to stress reflects the
functions of a hyper-excitable amygdala [194], that fear-potentiation of
startle is mediated through the amygdala, which directly projects to the
brainstem startle center [195], and that the memory processes of the amygdala
are amplified by extreme stress [196]. These amygdala-driven startle and
fear-freeze responses would be intense, because they are totally unregulated by
the orbitofrontal (and medial frontal) areas that are unavailable for the
correction and adjustment of emotional responses. In poorly evolved right brain
systems of PTSD-vulnerable personalities even low intensity interpersonal
stressors could activate unmodulated terrifying and painful bodily-based
dysregulated experiences of the individual’s early history that are imprinted
into amygdalar-hypothalamic limbic-autonomic circuits. Early memory is now
being understood as a residual of the basic mechanisms of brain maturation.
According to Valent [20] early handling and misattunements may be deeply
remembered physiologically in later life in the form of disconnected
physiological responses, emotions, and acting out, a description that mirrors
van der Kolk’s [66] assertion that "the body keeps the score."
In
light of the findings that autonomic changes in the body are evoked when angry
facial expressions are subliminally presented at levels beneath awareness to
the right and not the left hemisphere [197], and that the right amygdala is
preferentially activated by briefly presented, subliminal faces [198] and
specialized for the expression of memory of aversively motivated experiences
[199], I suggest that subliminal [200] visual and auditory stressors emanating
from faces, processed in an inefficient right hemisphere, the locus of the
startle mechanism [201], are potent triggers of dysregulation and dissociation
in early traumatized patients. Of special importance is the very rapid right
brain perception [51, 202] and memory retrieval [203, 204] of visual images and
prosodic tones of voice that emanate from subjectively perceived threatening
and humiliating faces [44, 205]. Notice that the dysregulated implicit process
more so than the specific explicit conscious content of the traumatic memory
reveals the underlying pathological mechanism.
The
right, as opposed to the left amygdala is activated when the individual is not
consciously aware of the aversive nature of a nonverbal eliciting stimulus, one
that still triggers an immediate negative representation [206]. Loss of
modulating function of the right anterior cingulate, located anterior and
inferior to the amygdala, would interfere with its known role in inducing a
relaxation of bodily states of sympathetic arousal [207]. Loss of higher
orbital corticolimbic regulation would lead to a deficit in distinguishing
between mental representations of ongoing reality and currently irrelevant
memories [208]. When dissociated from these "top-down" influences, an
"exaggerated amygdala" response to masked facially expressed fearful
reminders of traumatic events occurs in PTSD patients [209].
Thus
in these flashback moments, a right subcortically-driven traumatic re-enactment
encoded in implicit memory would occur in the form of a strong physiological
autonomic dysregulation and highly aversive motivational state of terror and
helplessness, "without reference to reality," and for "no
apparent reason." In other words, the person would not be aware that his
fear has any origin in space, place, and time. This bears upon McFarlane and
Yehuda’s observation, "Essentially, the core of traumatic syndromes is the
capacity of current environmental triggers (real or symbolic), to provoke the
intense recall of affectively charged traumatic memory structures, which come
to drive current behaviour and perception" [7, p. 900]. I would add that a
focus on "cumulative" relational instead of "single-hit"
trauma emphasizes that the traumatic event of the PTSD patient originated as a
personal and social process, thereby suggesting that the "affectively
charged traumatic memory" is not of a specific overwhelming experience
with the physical environment as much as a re-evocation of a prototypical
disorganized attachment transaction with the misattuning social environment
that triggers an intense arousal dysregulation.
Indeed,
there is now evidence to show that early relational trauma is particularly
expressed in right hemispheric deficits in the processing of social-emotional
and bodily information. Very recent studies reveal that maltreated children
diagnosed with PTSD manifest right lateralized metabolic limbic abnormalities
[210], and that right brain impairments associated with severe anxiety
disorders are expressed in childhood [211]. Adults severely abused in childhood
[212] and diagnosed with PTSD [77] show reduced right hemisphere activation
during a working memory task. Neurological studies of adults confirm that
dysfunction of the right frontal lobe is involved in PTSD symptomatology [213]
and dissociative flashbacks [78]. Current neuropsychiatric research indicates
that the paralimbic areas of the right hemisphere are preferentially involved
in the storage of traumatic memories [214], that altered right-sided activity
occurs in panic and social phobic anxiety states [215, 216], and that
dissociation reflects a deficiency of right brain functioning [94].
Neurobiological research thus suggests continuity in the expression of the
stress coping deficits of posttraumatic stress disorders over the course of the
life span.
Continuity
between Infant, Childhood, and Adult PTSD
In
parallel work clinical researchers are describing a continuity in infant and
adult coping deficits [217, p. 253]:
The
stress responses exhibited by infants are the product of an immature brain
processing threat stimuli and producing appropriate responses, while the adult
who exhibits infantile responses has a mature brain that…is capable of
exhibiting adult response patterns. However, there is evidence that the adult
brain may regress to an infantile state when it is confronted with severe
stress.
This
"infantile state" is a disorganized-disoriented state of insecure
attachment. As in infancy, children, adolescents, and adults with posttraumatic
stress disorders can not generate an active coherent behavioral coping strategy
to confront subjectively perceived overwhelming, dysregulating events, and thus
they quickly access the passive survival strategy of disengagement and
dissociation.
Indeed,
the type D attachment classification has been observed to utilize dissociative
behaviors in later stages of life [218], and to be implicated in the etiology
of the dissociative disorders [91]. The characterological use of dissociation
over developmental stages is discussed by Allen and Coyne:
Although
initially they may have used dissociation to cope with traumatic events, they
subsequently dissociate to defend against a broad range of daily stressors,
including their own posttraumatic symptoms, pervasively undermining the
continuity of their experience [219, p. 620].
These
"initial traumatic events" are embedded in the abuse and neglect
experienced by type D infants, the first relational context in which
dissociation is used to autoregulate massive stress. In developmental research
Sroufe and his colleagues conclude that early trauma more so than later trauma
has a greater impact on the development of dissociative behaviors [220].
Dissociation is a common symptom in PTSD patients, and its occurrence at the
time of a trauma is a strong predictor of this disorder [221, 222].
The
fact that dissociation becomes a trait in posttraumatic stress disorders has
devastating effects on self, and therefore psychobiological functions. In neurological
studies of trauma Scaer refers to somatic dissociation, and concludes,
"Perhaps the least appreciated manifestations of dissociation in trauma
are in the area of perceptual alterations and somatic symptoms" [223]. He
further points out that distortion of proprioceptive awareness of the trauma
patient’s body is a most common dissociative phenomenon. Similarly, in clinical
psychiatric studies Nijenhuis [224] is now describing not just psychological
(e.g., amnesia) but "somatoform dissociation," which is associated
with early onset traumatization, often involving physical abuse and threat to
life by another person. Somatoform dissociation is expressed as a lack of
integration of sensorimotor experiences, reactions, and functions of the
individual and his/her self-representation.
This
shift from the cognitive to the affective-somatic aspects of dissociation is
echoed in the current neuroscience literature, which describes "a
dissociation between the emotional evaluation of an event and the physiological
reaction to that event, with the process being dependent on intact right
hemisphere function" [225, p. 643]. Posttraumatic stress disorders
therefore reflect a severe dysfunction of the right brain’s vertically
organized systems that perform attachment, affect regulating, and stress
modulating functions, which in turn impair the capacity to maintain a coherent,
continuous, and unified sense of self. Although the right brain’s growth spurt
is maximal in the first two years, it continues to enter into cycles of
experience-dependent growth [226] and forms connections with the later
developing left, which would be impacted by later relational trauma such as
sexual abuse in childhood [227]. It is now thought that the effectiveness of
newly formed and pruned networks in these later stages is limited by the
adequacy of already-formed, underlying networks, and therefore maturation is
optimal only if the preceding stages were installed optimally [228].
Traumatic
attachment experiences negatively impact the early organization of the right
brain, and thereby produce deficits in its adaptive functions of emotionally
understanding and reacting to bodily and environmental stimuli, identifying a
corporeal image of self and its relation to the environment, distinguishing the
self from the other, and generating self-awareness [14, 47, 98, 229]. Optimal
attachment experiences allow for the emergence of self-awareness, the ability
to sense, attend to, and reflect upon the dynamic changes of one’s subjective
self states, but traumatic attachments in childhood lead to self-modulation of
painful affect by directing attention away from internal emotional states.
From
a psychoneurobiological perspective, dissociation reflects the inability of the
right brain cortical-subcortical system to recognize and co-process (integrate)
external stimuli (exteroceptive information coming from the environment) and
internal stimuli (interoceptive information from the body, the corporeal self).
According to van der Kolk and McFarlane [230] a central feature of PTSD is a
loss of the ability to physiologically modulate stress responses which leads to
a reduced capacity to utilize bodily signals as guides to action, and this
alteration of psychological defense mechanisms is associated with an impairment
of personal identity.
These
deficits are the expression of a malfunctioning orbitofrontal
cortical-subcortical system, the senior executive of the right brain [14, 18,
29, 31, 45, 56]. In light of the finding that the orbitofrontal cortex is
involved in critical human functions that are crucial in defining the
‘personality’ of an individual [231], personality organizations that
characterologically access dissociation can be described as possessing an
inefficient orbital frontolimbic regulatory system and a developmentally
immature coping mechanism. And because adequate limbic function is required to
allow the brain to adapt to a rapidly changing environment and organize new
learning [106], a metabolically altered orbitofrontal system would interfere
with ongoing social emotional development. Early failures in attachment thus
skew the developmental trajectory of the right brain over the rest of the life
span, thereby engendering what Bowlby described as a diverting of development
from its adaptive course, and precluding what Janet called an
"enlargement" of personality development.
De-Evolution of
Right Brain Limbic Circuits and PTSD Pathogenesis
According
to Krystal [232], the long-term effect of infantile psychic trauma is the
arrest of affect development. Because emotions involve rapid nonconscious
appraisals of events that are important to the individual [233] and represent
reactions to fundamental relational meanings that have adaptive significance
[234], this enduring developmental impairment is expressed in a variety of
critical dysfunctions of the right brain. PTSD patients, especially when
stressed, show severe deficits in the preattentive reception and expression of
facially expressed emotion, the processing of somatic information, the
communication of emotional states, the maintaining of interactions with the
social environment, the use of higher level more efficient defenses, the
capacity to access an empathic stance and a reflective function, and the
psychobiological ability to regulate, either by autoregulation or interactive
regulation, and thereby recover from stressful affective states. Most of these
dysfunctions represent pathological alterations of early acting, rapid,
implicit, unconscious mechanisms. Note that they also describe the deficits of
borderline personality disorders, a condition that correlates highly with PTSD
and shares both a history of early attachment trauma and orbitofrontal and
amygdala dysfunction (see reference 44).
Furthermore,
the observations that in human infancy, the right brain, the neurobiological
locus of the stress response, organizes in an affective experience-dependent
fashion, and that the emotion processing and stress coping limbic system
evolves in stages, from the amygdala, to anterior cingulate, to orbitofrontal
cortex [14, 18], supports the concept of de-evolution as a mechanism of symptom
generation in PTSD. Wang, Wilson, and Mason [235] describe "stages of
decompensation" in chronic PTSD, reflected in incremental impairments in
amplified hyperarousal symptoms and defensive dissociation, decreased range of
spontaneity and facial expression, heightened dysregulation of self esteem,
deepening loss of contact with the environment, reduced attachment and insight,
and increased probability of destruction and suicide. Intriguingly, they posit
the existence of specifically three stages beneath a level of good to maximum
functioning, and suggest each stage is physiologically distinct.
The
concept of "decompensation" describes a condition in which a system
is rapidly disorganizing over a period of time. This construct derives from
Hughling Jackson’s [236] classic principle that pathology involves a
"dissolution," a loss of inhibitory capacities of the most recently
evolved layers of the nervous system that support higher functions (negative
symptoms), as well as the release of lower, more automatic functions (positive
symptoms). This principle applies to the dissolution of the vertical
organization of the right brain, dominant for inhibitory control [67], and the
disorganization of the complex circuit of emotion regulation of orbital frontal
cortex, anterior cingulate, and amygdala [18, 45, 237]. And so it is tempting
to speculate that the stage model of Wang and her colleagues describes a
Jacksonian de-evolution of the "rostral limbic system" [112], in
reverse developmental order, from orbitofrontal loss, to anterior cingulate
loss, and finally to amygdala dysfunction. At a certain threshold of stress,
the frontolimbic systems of PTSD patients would be unable to perform a higher
regulatory function over lower levels, thereby releasing lower level right
amygdala activity, without the adaptive capacity of flexibly re-initiating
higher control functions.
In
addition, in light of the fact that the orbitofrontal, anterior cingulate, and
amygdala systems each connect into the ANS [18], the mechanism of de-evolution
dynamics would also apply to the hierarchical disorganization of the autonomic
nervous system. This would be manifest in long-lasting episodes of a coupled
nonreciprocal mode of autonomic control, in which concurrent increases (or
decreases) occur in both sympathetic and parasympathetic components, or
uncoupled nonreciprocal mode of autonomic control, in which responses in one
division of the ANS occur in absence of change in the other. In other words,
the ANS would too easily be displaced from a state of autonomic balance, and
once displaced, have difficulty in re-establishing balance, that is, show a
poor capacity for vagal rebound and recovery from psychological stress [238].
This
de-evolution would also be manifest in a stress-associated shift down from the
higher ventral vagal complex (which is known to be defective in posttraumatic
stress disorder [239]) to the dorsal vagal complex that mediates severe
emotional states of terror, immobilization, and dissociation. Ultimately higher
vagal functions would be metabolically compromised, and dorsal vagal activity
would predominate even in a resting state. This lowest level may be seen in
infants raised in a neglectful environment [176], chronic PTSD patients with
low cortisol levels [240, 241], suicidal patients with severe right brain
deficiencies experiencing intense despair [94], and Wang, Wilson, and Mason’s
[235] final stage of depression-hopelessness. This conception therefore
suggests qualitative physiological as well as symptomatic differences between
acute and chronic PTSD populations, and it relates developmental models of
early organization to later clinical models of disorganization.
The
ultimate endpoint of chronically experiencing catastrophic states of
relational-induced trauma in early life is a progressive impairment of the
ability to adjust, take defensive action, or act on one’s own behalf, and a
blocking of the capacity to register affect and pain, all critical to survival.
Ultimately these individuals perceive themselves as different from other people
and outside of, as well as unworthy of, meaningful attachments [242]. Henry
echoes this conclusion:
The
ability to maintain personally relevant bonds is vital for our evolutionary
survival. The infant’s tie to the mother’s voice and odor is recognized even by
the newborn [243], yet this personal relevance and recognition of the familiar
can be impaired by anxious insecurity resulting from difficult early
experiences or traumatic stress. The vital task of establishing a personally
relevant universe and the solace derived from it depend on right hemispheric
functioning. If this function is indeed lost in the insecurely attached, much
has been lost (cited in reference 32).
These
survival limitations may negatively impact not just "psychological"
but essential organismic functions in coping with physical disease. Very recent
studies are linking attachment, stress, and disease [244] and childhood
attachment and adult cardiovascular and cortisol function [245], as well
documenting effects of childhood abuse on multiple risk factors for several of
the leading causes of death in adults [246].
This
developmental neurobiological model has significant implications for psychiatry
and the other mental health professions. The organization of the brain’s
essential coping mechanisms occurs in critical periods of infancy. The
construct of critical periods implies that certain detrimental early influences
lead to particular irreversible or only partially reversible enduring effects.
But the flip side of the critical period concept emphasizes the extraordinary
sensitivity of developing dynamic systems to their environment, and asserts
that these systems are most plastic in these periods. The development of the
right brain is experience-dependent, and this experience is embedded in the
attachment relationship between caregiver and infant.
Attachment
researchers in association with infant mental health workers are now devising interventions
that effectively alter the affect-communicating capacities of mother-infant
systems, and thereby the attachment experiences of high risk dyads. Early
interventions that are timed to critical periods of development of the right
brain, the locus of the human stress response, can facilitate the maturation of
neurobiologically adaptive stress coping systems, and thereby have lifelong
effects on the adaptive capacities of a developing self. Early treatment and
prevention programs, if expanded onto a societal scale, could significantly
diminish the number of individuals who develop pathological reactions of mind
and body to catastrophic life events. These efforts could, in turn, make deep
inroads into not only altering the intergenerational transmission of
posttraumatic stress disorders but improving the quality of many lives
throughout all stages of human development.
References
1. Kessler DC.
Sonnega A, Bromet E, Hughes M, Nelson CB. Posttraumatic stress disorder in the
National Comorbidity Survey. Archives of General Psychiatry 1995;
52:1048-1060.
2. Zlotnick C,
Warshaw M, Shea MT, Allsworth J, Pearlstein T, Keller MB. Chronicity in
posttraumatic stress disorder (PTSD) and predictors of course of comorbid PTSD
in patients with anxiety disorders. Journal of Traumatic Stress 1999;
12:89-100.
3. Schnurr PP,
Friedman MJ. An overview of research findings on the nature of posttraumatic
stress disorder. In Session: Psychotherapy in Practice 1997; 3:11-25.
4. Morgan CA
III, Wang S, Rasmusson A, Hazlett G, Anderson G, Charney D.S. Relationship
among plasma cortisol, catecholamines, neuropeptide Y, and human performance
during exposure to uncontrollable stress. Psychosomatic Medicine 2001;
63:412-422.
5. Pynoos RS.
Traumatic stress and developmental psychopathology in children and adolescents.
In: Oldham JM, Riba MB, Tasman, A. eds. Review of psychiatry.
Washington: American Psychiatric Press, 1993:239-272.
6. Davidson JRT,
Foa E. Post traumatic stress disorder: DSM-IV and beyond. Washington:
American Psychiatric Press, 1993.
7. McFarlane AC,
Yehuda R. Clinical treatment of posttraumatic stress disorder: conceptual
challenges raised by recent research. Australian and New Zealand Journal of
Psychiatry 2000; 34:940-953.
8. Thompson RA.
The legacy of early attachments. Child Development 2000; 71:145-152.
9. Bowlby J. Attachment
and loss. Vol. 1: Attachment. New York: Basic Books, 1969.
10. Francis DD,
Meaney MJ. Maternal care and the development of stress responses. Current
Opinion in Neurobiology 1999; 9:128-134.
11. Levine S. The
ontogeny of the hypothalamic-pituitary-adrenal axis. The influence of maternal
factors. Annals of the New York Academy of Sciences 1994; 746:275-288.
12. Kehoe P,
Shoemaker WJ, Triano L, Hoffman J Arons C. Repeated isolation in the neonatal
rat produces alterations in behavior and ventral striatal dopamine release in
the juvenile after amphetamine challenge. Behavioral Neuroscience 1996;
110:1435-1444.
13. Nachmias M,
Gunnar MR, Mangelsdorf S, Parritz R, Buss K. Behavioral inhibition and stress
reactivity: moderating role of attachment security. Child Development
1996; 67:508-522.
14. Schore AN. Affect
regulation and the origin of the self: The neurobiology of emotional
development. Mahwah, NJ: Lawrence Erlbaum, 1994.
15. Schore AN.
Early shame experiences and the development of the infant brain. In: Gilbert P,
Andrews B. eds. Shame: interpersonal behaviour, psychopathology, and culture.
London: Oxford University Press, 1998:57-77.
16. Schore AN.
Foreword to the reissue of Attachment and Loss, Vol. 1: Attachment
by John Bowlby. New York: Basic Books, 2000.
17. Schore AN.
Plenary Address: Parent-infant communications and the neurobiology of emotional
development. In: Proceedings of Head Start’s Fifth National Research
Conference, Developmental and contextual transitions of children and families.
Implications for research, policy, and practice, 2000:49-73.
19. Henry JP Wang
S. Effects of early stress on adult affiliative behavior. Psychoneuroendocrinology
1998; 23:863-875.
20. Valent, P. From
survival to fulfillment. A framework for the life-trauma dialectic.
Philadelphia, PA: Brunner/Mazel, 1998.
21. Siegel DJ. The
developing mind: Toward a neurobiology of interpersonal experience. New
York: Guilford Press, 1999.
22. Streeck-Fischer
A, van der kolk BA. Down will come baby, cradle and all: diagnostic and
therapeutic implications of chronic trauma on child development. Australian
and New Zealand Journal of Psychiatry 2000; 34:903-918.
23. Korte SM.
Corticosteroids in relation to fear, anxiety and psychopathology. Neuroscience
and Biobehavioral Reviews 2001; 25:117-142.
24. Bowlby J.
Attachment theory and its therapeutic implications. In: Feinstein SC
Giovacchini PL, eds. Adolescent psychiatry: Developmental and clinical
studies. Chicago: University of Chicago Press, 1978.
25. Wittling W.
The right hemisphere and the human stress response. Acta Physiologica
Scandinavica, Supplement 1997; 640:55-59.
26. Chiron C,
Jambaque I, Nabbout R, Lounes R, Syrota A, Dulac O. The right brain hemisphere
is dominant in human infants. Brain 1997; 120:1057-1065.
27. Matsuzawa J,
Matsui M, Konishi T, Noguchi K, Gur RC, Bilker W, Miyawaki T. Age-related
changes of brain gray and white matter in healthy infants and children. Cerebral
Cortex 2001; 11:335-342.
28. Henry JP.
Psychological and physiological responses to stress: The right hemisphere and
the hypothalamo-pituitary-adrenal axis, an inquiry into problems of human
bonding. Integrative Physiological and Behavioral Science 1993;
28:369-387.
29. Schore AN.
The experience-dependent maturation of a regulatory system in the orbital
prefrontal cortex and the origin of developmental psychopathology. Development
and Psychopathology 1996; 8:59-87.
30. Schore AN.
Interdisciplinary developmental research as a source of clinical models. In:
Moskowitz M, Monk C, Kaye C, Ellman S, eds.The neurobiological and
developmental basis for psychotherapeutic intervention. New York: Jason
Aronson, 1997: 1-71.
31. Schore AN.
Attachment and the regulation of the right brain. Attachment & Human
Development 2000; 2: 23-47.
32. Wang S.
Traumatic stress and attachment. Acta Physiologica Scandinavica, Supplement
1997; 640:164-169.
33. Crittenden
PM, Ainsworth MDS. Child maltreatment and attachment theory. In: Cicchetti D,
Carlson V. eds. Child maltreatment: Theory and research on the causes and
consequences of child abuse and neglect. New York: Cambridge University
Press, 1989:432-463.
34. Erickson MF,
Egeland B, Pianta R. The effects of maltreatment on the development of young
children. In: Cicchetti D, Carlson V. eds. Child maltreatment: Theory and
research on the causes and consequences of child abuse and neglect. New
York: Cambridge University Press, 1989:647-684.
35. deBellis MD,
Baum AS, Birmaher B, Keshavan MS, Eccard CH, Boring AM, Jenkins FJ, Ryan ND.
Developmental traumatology Part I: Biological stress systems. Biological
Psychiatry 1999; 45:1259-1270.
36. Sgoifo A,
Koolhaas J, De Boer S, Musso E, Stilli D, Buwalda B, Meerlo P. Social stress,
autonomic neural activation, and cardiac activity in rats. Neuroscience and
Biobehavioral Reviews 1999; 23:915-923.
37. de Bellis,
MD. Developmental traumatology: the psychobiological development of maltreated
children and its implications for research, treatment, and policy. Development
and Psychopathology 2001; 13:539-564.
38. McEwen BS.
The neurobiology of stress: from serendipity to clinical relevance. Brain
Research 2000; 886:172-189.
39. Schore AN.
Early organization of the nonlinear right brain and development of a
predisposition to psychiatric disorders. Development and Psychopathology
1997; 9:595-631.
40. Schore AN.
Early trauma and the development of the right brain. Unpublished keynote
address, Royal Australian and New Zealand College of Psychiatrists, Faculty of
Child and Adolescent Psychiatry 11th Annual Conference, Sydney, Australia,
October, 1998.
41. Schore AN.
Early trauma and the development of the right brain. Unpublished keynote
address, C.M. Hincks Institute Conference, "Traumatized parents and
infants: The long shadow of early childhood trauma", University of
Toronto, Toronto, Canada, November, 1998.
42. Schore AN.
Early trauma and the development of the right brain. Unpublished keynote
address, Boston University School of Medicine Conference, "Psychological
trauma: Maturational processes and therapeutic interventions," Boston, MA,
April, 1999.
43. Schore AN.
The enduring effects of early trauma on the right brain. Unpublished address,
Annual Meeting of the American Academy of Child and Adolescent Psychiatry,
Symposium, "Attachment, trauma, and the developing mind", Chicago,
IL, October, 1999.
45. Schore AN.
The self-organization of the right brain and the neurobiology of emotional
development. In: Lewis MD, Granic I, eds. Emotion, development, and
self-organization. New York: Cambridge University Press, 2000:155-185.
46. Schore AN.
The right brain as the neurobiological substratum of Freud’s dynamic
unconscious. In: Scharff D, ed. The psychoanalytic century: Freud’s legacy
for the future. New York: The Other Press, 2001: 61-88.
47. Devinsky O.
Right cerebral hemisphere dominance for a sense of corporeal and emotional
self. Epilepsy & Behavior 2000; 1:60-73.
48. Adolphs R,
Damasio H, Tranel D, Damasio, AR. Cortical systems for the recognition of
emotion in facial expressions. Journal of Neuroscience, 1996;
23:7678-7687.
49. George MS,
Parekh PI, Rosinsky N, Ketter TA, Kimbrell TA, Heilman KM, Herscovitch P, Post
RM. Understanding emotional prosody activates right hemispheric regions. Archives
of Neurology 1996; 53:665-670.
50. Borod J,
Cicero BA, Obler, LK, Welkowitz J, Erhan HM, Santschi C, Grunwald IS, Agosti
RM, Whalen JR. Right hemisphere emotional perception: Evidence across multiple
channels. Neuropsychology 1998; 12:446-458.
51. Nakamura K,
Kawashima R, Ito K, Sugiura M, Kato T, Nakamura A, Hatano K, Nagumo S, Kubota
K, Fukuda H, Kojima S. Activation of the right inferior frontal cortex during
assessment of facial emotion. Journal of Neurophysiology 1999;
82:1610-1614.
52. Borod J, Haywood
CS, Koff E. Neuropsychological aspects of facial asymmetry during emotuional
expression: A review of the adult literature. Neuopsychology Review
1997; 7:41-60.
53. Blonder LX,
Bowers D, Heilman KM. The role of the right hemisphere in emotional communication.
Brain, 1991;114:1115-1127.
54. Dimberg U,
Petterson M. Facial reactions to happy and angry facial expressions: Evidence
for right hemsphere dominance. Psychophysiology 2000; 37:693-696.
55. Ross ED,
Homan RW, Buck R. Differential hemispheric lateralization of primary and social
emotions. Implications for developing a comprehensive neurology for emotions,
repression, and the subconscious. Neuropsychiatry, Neuropsychology, and
Behavioral Neurology 1994; 7:1-19.
56. Schore AN.
The experience-dependent maturation of an evaluative system in the cortex. In:
Pribram KH, ed. Fifth Appalachian conference on behavioral neurodynamics,
"Brain and values". Mahweh, NJ: Lawrence Erlbaum,
1998:337-358.
57. Toth SC,
Cicchetti D. Remembering, forgetting, and the effects of trauma on memory: a
developmental psychopathologic perspective. Developmental and
Psychopathology 1998; 10:580-605.
58. van der Kolk
BA, Fisler RE. Childhood abuse and neglect and loss of self-regulation. Bulletin
of the Menninger Clinic 1994; 58:145-168.
59. Brake WG, Sullivan
RM, Gratton A. Perinatal distress leads to lateralized medial prefrontal
cortical dopamine hypofunction in adult rats. Journal of Neuroscience
2000; 20: 5538-5543.
60. Graham YP,
Heim C, Goodman SH, Miller AH, Nemeroff CB. The effects of neonatal stress on
brain development: implications for psychopathology. Development and
Psychopathology 1999; 11:545-565.
61. Taylor GJ,
Bagby RM, Parker JDA. Disorders of affect regulation: Alexithymia in medical
and psychiatric illness. Cambridge, UK: Cambridge University Press, 1997.
62. Luu P, Tucker
DM. Self-regulation and cortical development: Implications for functional
studies of the brain. In: Thatcher RW, Reid Lyon G, Rumsey J, Krasnegor N, eds.
Developmental neuroimaging: Mapping the development of brain and behavior.
San Diego, Academic Press,1996:297-305.
63. Fink GR,
Markowitsch HJ, Reinkemeier M, Bruckbauer T, Kessler J, Heiss W-D. Cerebral
representation of one’s own past: Neural networks involved in autobiographical
memory. Journal of Neuroscience 1996; 16:4275-4282.
64. Nakamura K,
Kawashima R, Ito K, Sato N, Nakamura A, Sugiura M, Kato T, Hatano K, Ito K,
Fukuda H, Schorman T, Zilles K. Functional delineation of the human
occipito-temporal areas related to face and scene processing. A PET study. Brain
2000; 123:1903-1912.
65. Terr LC. What
happens to early memories of trauma? Journal of the American Academy of
Child and Adolescent Psychiatry 1988; 1:96-104.
66. van der Kolk,
B.A. (1996). The body keeps the score. Approaches to the psychobiology of
posttraumatic stress disorder. In: van der Kolk BA, McFarlane AC, Weisaeth L,
eds. Traumatic stress: the effects of overwhelming experience on mind, body,
and society. New York, Guilford Press, 1996:214-241.
67. Garavan H,
Ross TJ, Stein E.A. Right hemisphere dominance of inhibitory control: An
event-related functional MRI study. Proceedings of the National Academy of
Sciences of the United States of America 1999; 96:8301-8306.
68. Rauch SL, van
der Kolk BA, Fisler RE, Alpert NM, Orr SP, Savage CR, Fischman AJ, Jenike MA,
Pitman RK. A symptom provocation study of posttraumatic stress disorder using
positron emission tomography and script-driven imagery. Archives of General
Psychiatry 1996; 53:380-387.
69. Shin LM,
McNally RJ, Kosslyn SM, Thompson WL, Rauch SL, Alpert NM, Metzger LJ, Lasko NB,
Orr SP, Pitman RK. Regional cerebral blood flow during script-driven imagery in
childhood sexual abuse-related PTSD: a PET investigation. American Journal
of Psychiatry 1999; 156:575-584.
70. Schuff N,
Marmar CR, Weiss DS, Neylan TC, Schoenfield F, Fein G, Weiner MW. Reduced
hippocampal volume and n-acetyl aspartate in posttraumatic stress disorder. Annals
of the New York Academy of Sciences 1997; 821:516-520.
71. Falk D,
Hildebolt C, Cheverud J, Vannier M, Helmkamp, RC, Konigsberg, L. Cortical
asymmetries in frontal lobes of Rhesus monkeys (Macaca mulatta). Brain
Research, 1990; 512: 40-45.
72. Semple, WE,
Goyer P, McCormick R, Morris E. Compton B, Donvan B, Berridge M, Miraldi F,
Schulz SC. Increased orbital frontal cortex blood flow and hippocampal
abnormality in PTSD: a pilot PET syudy. Biological Psychiatry 1992;
31:129A.
73. Charney DS,
Deutch AY, Southwick SM, Krystal JH Neural circuits and mechanisms of
post-traumatic stress disorder. In: Friedman MJ, Charney DS eds. Neurobiological
and clinical consequences of stress: from normal adaptation to post-traumatic
stress disorder. Philadelphia: Lippincott Williams & Wilkins, 1995.
74. Deutch AY,
Young CD. A model of the stress-induced activation of prefrontal cortical
dopamine systems: Coping and the development of post-traumatic stress disorder.
In: Friedman MJ, Charney DS eds. Neurobiological and clinical consequences
of stress: from normal adaptation to post-traumatic stress disorder Philadelphia:
Lippincott Williams & Wilkins, 1995:163-175.
75. Bremner JD,
Innis RB, Ng CK, Staib LH, Salomon RM, Bronen RA, Duncan J, Southwick SM,
Krystal JH, Rich D, Zubal G, Dey H, Soufer R, Charney DS. Positron emission
tomography measurement of cerebral metabolic correlates of yohimbe
administration in combat-related posttraumatic stress disorder. Archives of
General Psychiatry 1997; 54:246-254.
76. Vasterling
JJ, Brailey K, Sutker PB. Olfactory identification in combat-related
posttraumatic stress disorder. Journal of Traumatic Stress 2000;
13:241-253.
77. Galletly C.
Clark CR, McFarlane AC, Weber DL Working memory in posttraumatic stress
disorder – an event-related potential study. Journal of Traumatic Stress
2001; 14:295-309.
78. Berthier ML,
Posada A, Puentes C. Dissociative flashbacks after right frontal injury in a
Vietnam veteran with combat-related posttraumatic stress disorder. Journal
of Neuropsychiatry and Clinical Neuroscience 2001; 13:101-105.
79. Koenen KC,
Driver KL, Oscar-Berman M, Wolfe J, Folsom S, Huang MT, Schlessinger L.
Measures of prefrontal system dysfunction in posttraumatic stress disorder. Brain
and Cognition 2001; 45:64-78.
80. Hariri AR,
Bookheimer SY Mazziotta JC. Modulating emotional responses: effects of a
neocortical network on the limbic system. NeuroReport 2000; 11:43-48.
82. Adamec RE.
Transmitter systems involved in neural plasticity underlying increased anxiety
and defense - implications for understanding anxiety following traumatic
stress. Neuroscience and Biobehavioral Reviews 1997; 21:755-765.
83. Whalen PJ,
Rauch SL, Etcoff N, McInerney SC, Lee MB, Jenike, MA. Masked presentations of
emotional facial expressions modulate amygdala activity without explicit
knowledge. Journal of Neuroscience 1998; 18:411-418.
84. Adolphs R,
Tranel D, Damasio H. Emotion recognition from faces and prosody following
temporal lobectomy. Neuropsychology 2001; 15:396-404.
85. Morris JS,
Ohman, A, Dolan RJ. A subcortical pathway to the right amygdala mediating
"unseen" fear. Proceedings of the National Academy of Sciences of
the Unitted States of America 1999; 96:1680-1685.
86. Morgan MA
LeDoux JE. Differential acquisition of dorsal and ventral medial prefrontal
cortex to the acquisition and extinction of conditioned fear in rats. Behavioral
Neuroscience 1995; 109:681-688.
87. La Bar KS,
Gatenby JC, Gore JC, Le Doux JE, Phelps EA. Human amygdala activation during
conditioned fear acquisition and extinction: A mixed-trial fMRI study. Neuron
1998; 20:937-945.
88. Morgan MA,
Romanski LM, LeDoux JE. Extinction of emotional learning: contribution of
medial prefrontal cortex. Neuroscience Letters 1993; 163:109-113.
89. Putnam FW.
Development of dissociative disorders. In: Cicchetti D, Cohen, DJ, eds. Developmental
psychopathology: Vol. 2 Risk, disorder, and adaptation. New York: Wiley,
1995: 581-608.
90. Main M.
Introduction to the special section on attachment and psychopathology: 2.
Overview of the field of attachment. Journal of Consulting and Clinical
Psychology 1996; 64:237-243.
91. Liotti G.
Disorganized/disoriented attachment in the etiology of the dissociative
disorders. Dissociation 1992; IV:196-204.
92. Schore AN.
Early relational trauma and the development of the right brain. Unpublished
keynote address, Joint Annual Conference, Australian Centre for Posttraumatic
Mental Health and The Australasian Society for Traumatic Stress Studies,
Canberra, Australia, March, 2001.
93. Chambers RA,
Bremner JD, Moghaddam B, Southwick SM, Charney DS, Krystal JH. Glutamate and
post-traumatic stress disorder: toward a psychobiology of dissociation. Seminars
in Clinical Neuropsychiatry 1999; 4: 274-281.
94. Weinberg I.
The prisoners of despair: right hemisphere deficiency and suicide. In Neuroscience
and Biobehavioral Reviews 2000; 24:799-815.
95. Davidson RJ,
Hugdahl K. Brain asymmetry. Cambridge: MA. MIT Press. 1995.
96. Cutting J.
The role of right hemisphere dysfunction in psychiatric disorders. British
Journal of Psychiatry 1992; 160:583-588.
97. Janet P. L’Automatisme
psychologique. Paris: Alcan, 1889.
98. Keenan JP,
Nelson A, O’Connor M, Pascual-Leone A. Self-recognition and the right
hemisphere. Nature 2001; 409:305.
99. McFarlane AC.
Traumatic stress in the 21st century. Australian and New Zealand Journal of
Psychiatry 2000; 34:896-902.
100.Rapoport S. The development of neurodevelopmental
psychiatry. American Journal of Psychiatry 2000; 157:159-161.
101.Basch MF. The concept of affect: A
re-examination. Journal of the American Psychoanalytic Association 1976;
24:759-777.
102.Sroufe L.A. Emotional development: The
organization of emotional life in the early years. New York: Cambridge
Universty Press, 1996.
103.Stern D. N. The interpersonal world of the
infant. New York: Basic Books, 1985.
104.Spangler G. Schieche M, Ilg U, Maier U, Ackerman
C. Maternal sensitivity as an organizer for biobehavioral regulation in
infancy. Developmental Psychobiology 1994; 27:425-437.
105.MacLean PD. Evolutionary psychiatry and the
triune brain. Psychological Medicine 1985; 15:219-221.
106.Mesulam M-M. From sensation to cognition. Brain
1998; 121:1013-1052.
107.Tucker DM. Developing emotions and cortical
networks. In: Gunnar MR, Nelson CA eds. Minnesota symposium on child
psychology. Vol. 24, Developmental behavioral neuroscience Hillsdale, NJ:
Erlbaum, 1992:75-128.
108.Spence S, Shapiro D, Zaidel E. The role of the
right hemisphere in the physiological and cognitive components of emotional
processing. Psychophysiology 1996; 33:112-122.
109.Rinaman L, Levitt P, Card JP. Progressive
postnatal assembly of limbic-autonomic circuits revealed by central
transneuronal transport of pseudorabies virus. Journal of Neuroscience,
2000; 20:2731-2741.
110.Schore AN. The Seventh Annual John Bowlby
Memorial Lecture, Minds in the making: attachment, the self-organizing brain, and
developmentally-oriented psychoanalytic psychotherapy. British Journal of
Psychotherapy 2001; 17:299-328.
111.Price JL, Carmichael ST, Drevets WC. Networks
related to the orbital and medial prefrontal cortex; a substrate for emotional
behavior? Progress in Brain Research 1996; 107:523-536.
112.Devinsky O, Morrell MJ, Vogt BA. Contributions of
anterior cingulate cortex to behaviour. Brain 1995;118:279-306.
113.Carmichael ST, Price JL. Limbic connections of
the orbital and medial prefrontal cortex in macaque monkeys. Journal of
Comparative Neurology 1995; 363:615-641.
114.Pribram, KH. Emotions. In: Filskov SB & T.J.
Boll TJ, eds. Handbook of clinical neuropsychology. New York: Wiley,
1981:102-134.
115.Cavada C, Company T, Tejedor J, Cruz-Rizzolo RJ,
Reinoso-Suarez F. The anatomical connections of the macaque monkey
orbitofrontal cortex. A review. Cerebral Cortex 2000; 10:220-242.
116.Ryan RM, Kuhl J, Deci EL. Nature and autonomy: An
organizational view of social and neurobiological aspects of self-regulation in
behavior and development. Development and Psychopathology 1997;
9:701-728.
117.Berntson GG, Cacioppo JT, Quigley KS. Autonomic
determinism: The modes of autonomic control, the doctrine of autonomic space,
and the laws of autonomic constraint. Psychological Review 1991; 98:459-487.
118.Hilz HW, Tarnowski W, Arend P. Glucose
polymerisation and cortisol. Biochemical and Biophysical Research
Communications 1963; 10:492-502.
119.Shimazu T. Regulation of glycogen metabolism in
liver by the autonomic nervous system. IV. Activation of glycogen synthetase by
vagal stimulation. Biochimica Biophysica Acta 1971:252, 28-38.
120.Shimazu T, Amakawa A. Regulation of glycogen
metabolism in liver by the autonomic nervous system. II. Neural control of
glycogenolytic enzymes. Biochimica Biophysica Acta 1968;165:335-348.
121.Damasio AR. Descartes' error. New York:
Grosset/Putnam, 1994.
122.Coghill RC, Gilron I, Iadorola MJ. Hemispheric
lateralization of somatosensory processing. Journal of Neurophysiology
2001; 85:2602-2612.
123.Yoon B-W, Morillo CA, Cechetto DF, Hachinski V.
Cerebral hemsipheric lateralization in cardiac autonomic control. Archives
of Neurology 1997; 54:741-744.
124.Erciyas AH, Topaktas S, Akyuz A, Dener S.
Suppression of cardiac parasympathetic functions in patients with right
hemispheric stroke. European Journal of Neurology 1999; 6:685-690.
125.Porges SW. The polyvagal theory: phylogenetic
substrates of a social nervous system. International Journal of
Psychophysiology, 2001; 42: 123-146.
126.Neafsey EJ. Prefrontal cortical of the autonomic
nervous system: Anatomical and physiological observations. Progress in Brain
Research 1990; 85:147-166.
127.Zald DH, Kim SW. Anatomy and function of the
orbital frontal cortex, II: Function and relevance to obsessive-compulsive
disorder. Journal of Neuropsychiatry 1996; 8:249-261.
128.Adolphs R, Damasio H, Tranel D, Cooper G, Damasio
AR. A role for somatosensory cortices in the visual recognition of emotion as
revealed by three-dimensional lesion mapping. Journal of Neuroscience
2000; 20:2683-2690.
129.Bargh JA, Chartrand TL. The unbearable
automaticity of being. American Psychologist 1999; 54:462-479.
130.Hugdahl, K. Classical conditioning and implicit
learning: The right hemisphere hypothesis. In: Davidson RJ, Hugdahl K, eds. Brain
asymmetry. Cambridge, MA: MIT Press, 1995:235-267.
131.Thompson RA. Emotion and self-regulation. Nebraska
Symposium on Motivation. Lincoln: University of Nebraska Press, 1990:
367-467.
132.Savage CR, Deckersbach T, Heckers S, Wagner AD,
Schacter DL, Alpert NM, Fischman AJ, Rauch SL. Prefrontal regions supporting
spontaneous and directed application of verbal learning strategies. Evidence
from PET. Brain 2001; 124:219-231.
133.Elliott R, Dolan RJ, Frith CD. Dissociable
functions in the medial and lateral orbitofrontal cortex: evidence from human
neuroimaging studies. Cerebral Cortex 2000; 10:308-317.
134.Lipton PA., Alvarez, P, Eichenbaum H. Crossmodal
associative memory representations in rodent orbitofrontal cortex. Neuron
1999; 22:349-359.
135.Davies JM, Frawley MG. Treating the adult
survivor of childhood sexual abuse. A psychoanalytic perspective. New York:
Basic Books, 1994.
136.Freyd JJ. Betrayal trauma theory: The logic of
forgetting childhood abuse. Cambridge, MA: Harvard University Press, 1996.
137.Tronick EZ, Weinberg MK. Depressed mothers and
infants: failure to form dyadic states of consciousness. In: Murray L, Cooper,
PJ., eds. Postpartum depression in child development. New York: Guilford
Press, 1997:54-81
138.Perry BD, Pollard RA, Blakely TL, Baker WL,
Vigilante D. Childhood trauma, the neurobiology of adaptation, and
"use-dependent" development of the brain. How "states"
become "traits". Infant Mental Health Journal 1995;
16:271-291.
139.Beebe B. Coconstructing mother-infant distress:
the microsychrony of maternal impingement and infant avoidance in the
face-to-face encounter. Psychoanalytic Inquiry 2000; 20:412-440.
140.Brown MR, Fisher LA, Spiess J, Rivier C, Rivier
J, Vale W. Corticotropin-releasing factor: actions on the sympathetic nervous
system and metabolism. Endocrinology 1982; 111:928-931.
141.Butler PD, Weiss JM, Stout JC, Nemeroff CB.
Corticotropin-releasing factor produces fear-enhancing and behavioral
activating effects following infusion into the locus coeruleus. Journal of
Neuroscience 1990; 10:176-183.
142.Aston-Jones G, Valentino RJ, Van Bockstaele EJ,
Meyerson AT. Locus coeruleus, stress, and PTSD: neurobiological and clinical
parallels. In: Marburg MM, ed. Catecholamine function in PTSD.
Washington, DC: American Psychiatric Press, 1996:17-62.
143.Sabban EL, Kvetnansky R. Stress-triggered
activation of gene expresion in catecholaminergic systems: dynamics of
transcriptional events. Trends n Neuroscience 2001; 24:91-98.
144.Galton VA. Thyroid hormone-catecholamine
relationships. Endocrinology 1965; 77:278-284.
145.Nunez J. Effects of thyroid hormones during brain
differentiation. Molecular and Cellular Endocrinology 1984; 37:125-132.
146.Lauder JM, Krebs H. Do neurotransmitters,
neurohumors, and hormones specify critical periods? In: Greenough WT, Juraska
JM, eds. Developmental Neuropsychobiology Orlando, FL: Academic Press,
1986:119-174.
147.Kvetnansky R, Dobrakovova M, Jezova D, Oprsalova
Z, Lichardus B, Makara G. Hypothalamic regulation of plasma catecholamine
levels during stress: Effect of vasopressin and CRF. In: Van Loon GR,
Kvetnansky R, McCarty R, Axelrod J, eds. Stress: Neurochemical and humoral
mechanisms. New York: Gordon and Breach Science Publishers: 1989: 549-570.
148.Kvetnansky R, Jezova D, Oprsalova Z, Foldes O,
Michjlovskij N, Dobrakovova M, lichardus B, Makara GB. Regulation of the
sympathetic nervous system by circulating vasopressin. In Porter JC, Jezova D,
eds. Circulating regulatory factors and neuroendocrine function. New
York: Plenum Press; 1990: 113-134.
149.Koch KL, Summy-Long J, Bingaman S, Sperry N,
Stern, RM. Vasopressin and oxytocin responses to illusory self-motion and
nausea in man. Journal of Clinical and Endocrinological Metabolism 1990;
71:1269-1275.
150.Powles WE. Human development and homeostasis.
Madison, CT: International Universities Press, 1992.
151.Barach PMM. Multiple personality disorder as an
attachment disorder. Dissociation, 1991; IV:117-123.
152.Bion WR. Learning from experience. London:
Heinemann, 1962.
153.Mollon P. Multiple selves, multiple voices:
working with trauma, violation and dissociation. Chichester: John Wiley
& Sons, 1996.
154.Putnam FW. Dissociation in children and
adolescents: a developmental perspective. New York: Guilford Press, 1997
155.Dixon AK Ethological strategies for defense in
animals and humans: Their role in some psychiatric disorders. British
Journal of Medical Psychology 1998; 7: 417-445.
156.Fanselow, M.S. Condtioned fear-induced opiate
analgesia: A compelling motivational state theory of stress analgesia. In:
Kelly DD, eds. Stress-induced analgesia. New York: The New York Academy
of Sciences, 1986: 40-54.
157.Porges SW. Emotion: an evolutionary by-product of
the neural regulation of the autonomic nervous system. Annals of the New
York Academy of Sciences 1997; 807:62-77.
158.Meares R. The contribution of Hughlings Jackson
to an understanding of dissociation. American Journal of Psychiatry 1999;
156:850-1855.
159.Main M, Solomon J. Discovery of an
insecure-disorganized / disoriented attachment pattern: Procedures, findings
and implications for the classification of behavior. In: Brazelton TB, Yogman
MW, eds. Affective development in infancy, Norwood, NJ: Ablex,
1986:95-124.
160.Carlson V, Cicchetti D, Barnett D, Braunwald K.
Disorganized/disoriented attachment relationships in maltreated infants. Developmental
Psychology 1989; 25:525-531.
161.Hertsgaard L, Gunnar M, Erickson MF, Nachimias M.
Adrenocortical responses to the strange situation in infants with
disorganized/disoriented attachment relationships. Child Development
1995; 66:1100-1106.
162.Spangler G, Grossman K. Individual and
physiological correlates of attachment disorganization in infancy. In: Solomon
J, George C, eds. Attachment disorganization. New York: Guilford Press,
1999:95-124.
163.Frey S, Petrides M. Orbitofrontal cortex: a key
prefrontal region for encoding information. Proceedings of the National
Academy of Sciences of the Unitted States of America 2000; 97:8723-8727.
164.Kawasaki H, Adolphs R, Kaufman O, Damasio H,
Damasio AR, Granner M, Bakken H, Hori T, Howard MA. Single-neuron responses to
emotional visual stimuli recorded in human ventral prefrontal cortex. Nature
Neuroscience 2001; 4:15-16.
165.Hess E, Main MM. Second-generation effects of
unresolved trauma in nonmaltreating parents: dissociated, frightened, and
threatening parental behavior. Psychoanalytic Inquiry 1999; 19:481-540.
166.Schuengel C, Bakersmans-Kranenburg MJ, Van
Ijzendoorn MH. Frightening maternal behavior linking unresolved loss and
disorganized infant attachment. Journal of Consulting and Clinical
Psychology 1999; 67:54-63.
167.Johnson JG, Cohen P, Kasen S, Smailes E, Brook
JS. Association of maladaptive parental behavior with psychiatric disorder
among parents and their offspring. Archives of General Psychiatry 2001;
58:453-460.
168.Yehuda R, Halligan SL, Grossman R. Childhood
trauma and risk for PTSD: relationship to intergenerational effects of trauma,
parental PTSD, and cortisol excretion. Development and Psychopathology
2001; 13:733-753.
169.Dobbing J, Sands J. Quantitative growth and
development of human brain. Archives of Diseases of Childhood 1973;
48:757-767.
170.McDonald JW, Silverstein FS, Johnston MV.
Neurotoxicity of N-methyl-D-aspartate is markedly enhanced in developing
rat central nervous system. Brain Research 1988; 459:200-203.
171.Wittling W, Pfluger M. Neuroendocrine hemisphere
asymmetries: Salivary cortisol secretion during lateralized viewing of
emotion-related and neutral films. Brain and Cognition 1990; 14:243-265.
172.Kalogeras KT, Nieman LK, Friedman TC, Doppman JL,
Cutler GB Jr, Chrousos GP, Wilder RL, Gold PW, Yanovski JA. Inferior petrosal
sinus sampling in healthy human subjects reveals a unilateral
corticotropin-releasing hormone-induced arginine vasopressin release associated
with ipsilateral adrenocorticotropin secretion. Journal of Clinical
Investigation 1996; 97:2045-2050.
173.Yehuda R. Linking the neuroendocrinology of
post-traumatic stress disorder with recent neuroanatomic findings. Seminars
in Clinical Neuropsychiatry 1999;4:256-265.
174.Margolis RL, Chuang DM, Post RM. Programmed cell
death: Implications for neuropsychiatric disorders. Biological Psychiatry
1994: 35: 946-956.
175.Gould E, Wooley CS, McEwen, BS. Adrenal steroids
regulate postnatal development of the rat dentate gyrus: I. Effects of
glucocorticoids on cell death. Journal of Comparative Neurology 1991;
313:479-485.
176.Gunnar MR, Vazquz DM. Low cortisol and a
flattening of expected daytime rhythm: potential indices of risk in human
development. Development and Psychopathology 2001; 13:515-538.
177.Yehuda R, McFarlane AC, Shalev AY. Predicting the
development of posttraumatic stress disorder from the acute response to a
traumatic event. Biological Psychiatry 1998; 44:1305-1313.
178.Harkness KL, Tucker DM. Motivation of neural
plasticity: neural mechanisms in the self-organization of depression. In: Lewis
MD, Granic I, eds. Emotion, development, and self-organization. New
York: Cambridge University Press, 2000:186-208.
179.Post RM, Weiss RB, Leverich GS. Recurrent
affective disorder: Roots in developmental neurobiology and illness progression
based on changes in gene expression. Development and Psychopathology,
1994; 6:781-813.
180.Prins A, Kaloupek DG, Keane T.M. Psychophysiological
evidence for autonomic arousal and startle in traumatized adult populations.
In: Friedman MJ, Charney DS eds. Neurobiological and clinical consequences
of stress: from normal adaptation to post-traumatic stress disorder Philadelphia:
Lippincott Williams & Wilkins, 1995: 291-314.
181.Southwick SM, Krystal JH, Morgan A, Johnson D,
Nagy LM, Nicolaou A, Heninger GR, Charney DS. Abnormal noradrenergic function
in posttraumatic stress disorder. Archives of General Psychiatry 1993;
50:266-274.
182.Geracioti TD, Baker DG, Ekhator NN, West, SA,
Hill KK, Bruce AB, Scmidt D, Rounds-Kugler RN, Yehuda R, Keck PE, Kasckow JW.
CSF norepinephrine concentrations in posttraumatic stress disorder. American
Journal of Psychiatry 2001; 158:1227-1330.
183.Gurvits TV, Gilbertson MW, Lasko NB, Tarhan AS,
Simeon D, Macklin ML, Orr SP, Pitman RK. Neurologic soft signs in chronic
posttraumatic stress disorder. Archives of General Psychiatry 2000;
57:181-186.
184.Antelman SM, Caggiula AR, Gershon S, Edwards DJ,
Austin MC, Kiss S, Kocan D. Stressor-induced oscillation. A possible model of
the bidirectional symptoms in PTSD. Annals of the New York Academy of
Sciences, 1997; 821:296-304.
185.Post RM, Weiss SRB, Smith M, Li H, McCann U.
Kindling versus Quenching: implications for the evolution and treatment of
posttraumatic stress disorder. In: Yehuda R, McFarlane, AC, eds. Psychobiology
of posttraumatic stress disorder. New York Academy of Sciences, 1997;
821:285-295.
186.Sutker PB, Vasterling JJ, Brailey K, Allain AN
Jr. Memory, attention, and executive deficits in POW survivors: Contributing
biological and psychological factors. Neuropsychology 1995; 9:118-125.
187.Uddo M, Vasterling JJ, Brailey K, Sutker, PB.
Memory and attention in combat-related post-traumatic stress disorder (PTSD). Journal
of Psychopathology and Behavioral Assessment 1993; 15:43-52.
188.Bremner JD, Staib LH, Kaloupek D, Southwick SM,
Soufer R, Charney DS. Neural correlates of exposure to traumatic pictures and
sound in combat veterans with and without posttraumatic stress disorder: A positron
emission tomography study. Biological Psychiatry 1999; 45:806-818.
189.Hamner MB, Lorberbaum JP, George MS. Potential
role of the anterior cingulate cortex in PTSD: review and hypothesis. Depression
and Anxiety 1999; 9:1-14.
190.Young JB, Rosa RM, Landsberg L. Dissociation of
sympathetic nervous system and adrenal medullary responses. American Journal
of Physiology 1984; 247:E35-E40.
191.Rolls, E.T. The orbitofrontal cortex. Philosophical
Transactions of the Royal Society of London B 1996; 351:1433-1444.
192.Kinsbourne M, Bemporad, B. Lateralization of
emotion: A model and the evidence. In: Fox NA & RJ Davidson eds. The
psychobiology of affective development. Hillsdale, NJ: Erlbaum,
1984:259-291.
193.Adamec RE. Evidence that limbic neural plasticity
in the right hemisphere mediates partial kindling induced lasting increases in
anxiety-like behavior: effects of low frequency stimulation (Quenching?) on
long-term potentiation of amygdala efferents and behavior following kindling. Brain
Research 1999 839:133-152.
194.Halgren, E. Emotional neurophysiology of the
amygdala within the context of human cognition. In: Aggleton JP ed. The
amygdala: neurobiological aspects of emotion, memory, and mental dysfunction.
New York: Wiley-Liss, 1992:191-228.
195.Davis M. (1989). The role of the amygdala and its
efferent projections in fear and anxiety. In: Tyrer P ed. Psychopharmacology
of anxiety. Oxford: Oxford University Press, 1989:52-79.
196.Corodimas KP, LeDoux JE, Gold PW, Schulkin J.
Corticosterone potentiation of learned fear. Annals of the New York Academy
of Sciences 1994; 746:392-393.
197.Johnsen BH, Hugdahl K. Hemispheric asymmetry in
conditioning to facial emotional expressions. Psychophysiology 1991;
28:154-162.
198.Morris JS, Ohman, A, Dolan RJ. Conscious and
unconscious emotional learning in the human amygdala. Nature 1998;
393:467-470.
199.Coleman-Mensches K, McGaugh JL. Differential
involvement of the right and left amygdalae in expression of memory for
aversively motivated training. Brain Research 1995; 670:75-81.
200.Mogg K., Bradley BP, Williams R, Mathews A.
Subliminal processing of emotional information in anxiety and depression. Journal
of Abnormal Psychology 1993;102: 304-311.
201.Bradley M, Cuthbert BN, Lang PJ. Lateralized
startle probes in the study of emotion. Psychophysiology 1996; 33:156-161.
202.Braeutigam S, Bailey AJ, Swithenby SJ.
Task-dependent early latency (30-60ms) visual processsing of human faces and
other objects. Neuroreport 2001; 12:1531-1536.
203.Funnell MG, Corballis PM, Gazzaniga MS.
Hemispheric processing asymmetries: Implications for memory. Brain &
Cognition 2001; 46:135-139.
204.Simons JS, Graham KS, Owen AM, Patterson K,
Hodges JR. Perceptual and semantic components of memory for objects and faces:
A PET study. Journal of Cognitive Neuroscience 2001; 13:430-443.
205.Schore AN. Clinical implications of a
psychoneurobiological model of projective identification. In: Alhanati S, ed. Primitive
mental states. Volume II: Psychobiological and psychoanalytic perspectives on
early trauma and personality development. New York, Other Press, 2002: pp.
1-65.
206.Phelps EA, O’Connor KJ, Gatenby JC, Gore JC,
Grillon C, Davis M. Activation of the left amygdala to a cognitive
representation of fear. Nature Neuroscience 2001; 4:437-441.
207.Critchley HD, Melmed RN, Featherstone E, Mathias
CJ, Dolan RJ. Brain activity during biofeedback relaxation. A functional
neuroimaging investigation. Brain 2001; 124:1003-1012.
208.Schnider A, Treyer V, Buck A. Selection of
currently relevant memories by the human posterior medial orbitofrontal cortex.
Journal of Neuroscience 2000; 20:5880-5884.
209.Rauch SL, Whalen PJ, Shin LM, McInerney SC,
Macklin ML, Lasko NB, Orr SP, Pitman RK. Exaggerated amygdala response to
masked facial stimuli in posttraumatic stress disorder: A functional MRI study.
Biological Psychiatry 2000;47:769-776.
210.de Bellis MD, Keshaven MS, Spencer S, Hall J. N-acetylaspartate
concentration in anterior cingulate with PTSD. American Journal of
Psychiatry 2000; 157:1175-1177.
211.de Bellis MD, Casey BJ, Dahl RE, Birmaher B,
Williamson DE, Thomas KM, Axelson DA, Frustaci K, Boring AM, Hall J, Ryan ND. A
pilot study of amygdala volume in pediatric generalized anxiety disorder. Biological
Psychiatry 2000; 48:51-57.
212.Raine A, Park S, Lencz T, Bihrle S, Lacasse L,
Widom CS, Louai A-D, Singh M. Reduced right hemisphere activation in severely
abused violent offenders during a working memory task: An fMRI study. Aggressive
Behavior 2001; 27:111-129.
213.Freeman TW, Kimbrell, T. A "cure" for
chronic combat-related posttraumatic stress disorder secondary to a right
frontal lobe infarct: a case report. Journal of Neuropsychiatry and Clinical
Neuroscience 2001; 13:106-109.
214.Schiffer F, Teicher MH, Papanicolaou AC. Evoked
potential evidence for right brain activity during the recall of traumatic
memories. Journal of Neuropsychiatry and Clinical Neurosciences 1995;
7:169-175.
215.Davidson RJ, Marshall JR, Tomarken AJ, Henriques
JB. While a phobic waits: Regional brain electical and autonomic activity in
social phobics during anticipation of public speaking. Biological Psychiatry
2000; 47:85-95.
216.Galderisi S, Bucci P, Mucci A, Bernardo A, Koenig
T, Maj M. Brain electrical microstates in subjects with panic disorder. Psychophysiology
2001; 54:427-435.
217.Nijenhuis ERS, Vanderlinden J, Spinhoven, P.
Animal defensive reactions as a model for trauma-induced dissociative reations.
Journal of Traumatic Stress 1998; 11:242-260.
218.van Ijzendoorn MH, Schuengel C,
Bakermans-Kranenburg MJ. Disorganized attachment in early childhood:
Meta-analysis of precursors, concomitants, and sequelae. Development and
Psychopathology 1999; 11:225-249.
219.Allen JG, Coyne L. Dissociation and vulnerability
to psychotic experience. The Dissociative Experiences Scale and the MMPI-2. Journal
of Nervous and Mental Disease 1995; 183:615-622.
220.Ogawa JR, Sroufe LA, Weinfield NS, Carlson EA,
Egeland B. Development and the fragmented self: Longitudinal study of
dissociative symptomatology in a nonclinical sample. Development and
Psychopathology 1997; 9:855-879.
221.Koopman C, Classen C Spiegel D. Predictors of
posttraumatic stress symptoms among survivors of the Oakland/Berkeley, Calif,
firestorm. American Journal of Psychiatry 1994; 151:888-894.
222.Shalev AY, Peri T, Canetti L, Schreiber S.
Predictors of PTSD in injured trauma survivors: a prospective study. American
Journal of Psychiatry 1996;153:219-225.
223.Scaer RC. The body bears the burden: Trauma,
dissciation, and disease. New York: The Haworth Press, 2001.
224.Nijenhuis ERS. Somatoform dissociation: major
symptoms of dissociative disorders. Journal of Trauma & Dissociation
2000; 1:7-32.
225.Crucian GP, Hughes JD, Barrett AM, Williamson
DJG, Bauer RM, Bowers D, Heilman KM. Emotional and physiological responses to
false feedback. Cortex 2000; 36:623-647.
226.Thatcher RW. Cyclical cortical reorganization:
Origins of human cognitive development. In Dawson D, Fischer KW, eds. Human
behavior and the developing brain, New York: Guilford Press, 1994: 232-266.
227.Teicher MH, Ito Y, Gold CA, Andersen SL, Dumont
N, Ackerman E. Prelliminary evidence for abnormal cortical development in
physically and sexually abused children using EEG coherence and MRI. Annals
of the New York Academy of Sciences 1997; 821:160-175.
228.Epstein H.T. An outline of the role of brain in
human cognitive development. Brain and Cognition 2001; 45:44-51.
229.Ruby P, Decety J. Effect of subjective
perspective taking during stimulation of action: a PET investigation of agency.
Nature Neuroscience 2001; 4:546-550.
230.van der kolk BA, McFarlane AC. The black hole of
trauma. In: van der Kolk BA, McFarlane AC, Weisaeth L, eds. Traumatic
stress: the effects of overwhelming experience on mind, body, and society.
New York, Guilford Press, 1996:3-23.
231.Cavada C, Schultz W. The mysterious orbitofrontal
cortex. Foreword. Cerebral Cortex 2000; 10:205.
232.Krystal H. Integration and self-healing:
Affect-trauma-alexithymia. Hillsdale, NJ: The Analytic Press, 1988.
233.Frijda NH. The laws of emotion. Amerian
Psychologist 1988;43:349-358.
234.Lazarus, RS. Progress on a
cognitive-motivational-relational theory of emotion. American Psychologist
1991; 46:819-834.
235.Wang S, Wilson JP, Mason JW. Stages of
decompensation in combat-related posttraumatic tress disorder: a new conceptual
model. Integrative Physiological and Behavioral Science 1996;
31:237-253.
236.Jackson JH. Selected writings of J.H. Jackson.
Vol. I. London: Hodder and Soughton, 1931.
237.Davidson RJ, Putnam KM, Larson CL. Dysfunction in
the neural circuitry of emotion regulation-a possible prelude to violence. Science
2000; 289:591-594.
238.Mezzacappa ES, Kelsey RM, Katkin ES, Sloan RP.
Vagal rebound and recovery from psychological stress. Psychosomatic Medicine
2001; 63:650-657.
239.Sahar T, Shalev AY, Porges SW. Vagal modulation
of responses to mental challenge in posttraumatic stress disorder. Biological
Psychiatry 2001; 49:637-643.
240.Mason JW, Kosten TR, Southwick S,
Giller EL. The use of psychoendocrine strategies in posttraumatic stress
disorder. Journal of Applied Social Psychology 1990: 20;1822-1846.
241.Mason JW, Wang S, Yehuda R, Riney S,
Charney DS, Southwick SM. Psychogenic lowering of urinary cortisol levels
linked to increased emotional numbing and a shame-depressive syndrome in
combat-related posttraumatic stress disorder. Psychosomatic Medicine 2001;
63:387-401.
242.Lansky MR. Posttraumatic nightmares:
Psychodynamic explorations. New York: Analytic Press, 1995.
243.Van Lancker D. Personal relevance and the human
right hemisphere. Brain and Cognition 1991; 17:64-92.
244.Maunder RG, Hunter JJ. Attachment and
psychosomatic medicine: Developmental contributions to stress and disease. Psychosomatic
Medicine 2001; 63:556-567.
245.Luecken, LJ. Childhood attachment and loss
experiences affect adult cardiovascular and cortisol function. Psychosomatic
Medicine 1998; 60:765-772.
246.Felitti VJ, Anda RF, Nordenberg D, Williamson DF,
Spitz AM, Edwards V, Koss MP, Marks JS. Relationship of childhood abuse and
household dysfunction to many of the leading causes of death in adults. The
adverse childhood experiences (ACE) study. American Journal of Preventive
Medicine 1998; 14:245-258.
David Baldwin's Trauma Information Pages
http://www.trauma-pages.com
Eugene, Oregon USA
(541) 686 2598
