Abstract Environmental factors affecting the nervous system and health

The Nervous System and the Environment of Early Relationships

Copyright (c) Veronique Mead, MD, MA Boulder, CO 2004 (303) 527-0551 [email protected] www.veroniquemead.com

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Excerpt adapted from Master’s Thesis, Naropa University, May 2003:

Somatic Psychology Theory as a Mode for Understanding the Origins of ChronicIllness: A Case Study of Type 1 Diabetes

Chapter 2: Literature Review: Attachment

Revised September, 2004

Gene-environment interactions play an important and as yet rarely recognized role incontributing to our long-term physical as well as emotional and behavioral health. Earlyrelationships shape our developing nervous systems and are increasingly understood to influenceour risk for physical symptoms and disease. Since the nervous system is intimately involved inthe regulation of a large number of (if not all) physiological activities in the body, the process bywhich it learns to self-regulate plays an important role in our long-term physiological rhythms aswell as in our behavioral and emotional patterns.

This article is based primarily on the neurodevelopmental research of Allan Schore, Ph.D. Itexplains the role of the bond between caregiver and child during the first months and years of life,a period referred to in the psychological literature as the period of attachment. During attachment,the nervous system is shaped by gene-environment interactions in the process of experience-dependent maturation of the nervous system. This developmental process trains our nervoussystems to competently and easily change from states of arousal to states of inactive alertness andrest, and back again. By learning how to tolerate states of high arousal or immobility, and bygaining the capacity to inhibit certain states such as the stress response, experience-dependentmaturation facilitates the capacity for enhanced autonomic self-regulation. This article describesthe four stages of the attachment period, during which synapse formation, selection, andstrengthening is understood to be shaped by both genetics and the environment of parent-childinteractions.

Abstract

Environmental factors affecting the nervous system and health:The role of early relationships



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Table of Contents

The Role of Attachment in the Development of the Nervous System ............................. 3Introduction ..................................................................................................................................... 3

The Role of Attachment............................................................................................................................... 4Brief Overview of the Developmental Neurophysiology of Brain Growth............................................... 4

The Development of the Nervous System..................................................................................... 5The Four Periods of Attachment.............................................................................................................. 6I. Symbiosis, Gaze Transactions, and the Developing ANS ...................................................................... 6

Gaze interactions as mediators of nervous system growth.................................................................... 6Gaze interactions and sympathetic nervous system development......................................................... 7Gaze interactions and parasympathetic nervous system development. ................................................ 8The role of misattunement in mediating tolerance for increased levels of arousal. ........................... 10

II. The Early Practicing Period: Active Arousal and Sympathetic Growth .................................... 11The Caregiver as a “Secure Base” and an Indicator of Safety. ........................................................... 11Interactions and alternating sympathetic parasympathetic dominance............................................... 12Characteristics of the maturing brain. .................................................................................................. 13

Dopamine. ........................................................................................................................................ 13Excitation versus Inhibition. ............................................................................................................ 13Internalized Images .......................................................................................................................... 13

III. The Late Practicing Period: Shame, Passive Arousal, and Parasympathetic Growth ............ 14Misattunement and shame-induced states of low arousal.................................................................... 15The role of reunion episodes following misattunement. ..................................................................... 16Effects of optimal and dysregulated attunement.................................................................................. 16Attachment and Stress........................................................................................................................... 17Summary: III. ........................................................................................................................................ 18

IV. The Role of the Father and the Developing Verbal Left Hemisphere ........................................ 18The paternal-experience-dependent maturation of the dorsolateral cortex......................................... 19

Relationship between Parts of the ANS...................................................................................... 20Conclusion.................................................................................................................................................. 21

Table of Contents



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The Role of Attachment in theDevelopment of the Nervous System

IntroductionAttachment consists of a period beginning

2 months after birth and lasting untilapproximately 3 years of age. The founder ofattachment theory, John Bowlby (1969, ascited in Maunder, 2001), explained that thisdrive for attachment serves a survival functionthrough the recruitment of protection fromadults and the social group, but also promotesthe development of the nervous system toenable the infant to learn how to manage his orher own internal physiological processes.

Before the emergence of organizedattachment behavior (i.e., beforelearning) infant signaling of needs isinnate and responsive to immediatestimuli. In this … period appropriateproximity relies on parentalanticipation of infant needs andsensitivity to infant signals. Thus, thesame processes of mutual engagementand interaction that initially serve tomaintain proximity as an end in itselfare the crucial prerequisites of bothemotional attachment security andphysiological self-regulation. T h e s eintertwined developmental processesultimately result in an organism thatcan independent ly mainta inhomeos tas i s and mount aphysiological response to externalthreat [italics added]” (Bowlby, 1969,as cited in Maunder p 558).

The manner in which the developingnervous system is intimately influenced by theenvironment of the attachment bond with thecaregiver is described in great detail by AllanN. Schore, a psychoanalyst in the Departmentof Psychiatry and Biobehavioral Sciences atthe University of California at Los Angeles,School of Medicine. Unless otherwise stated,this section on attachment refers entirely to theideas presented by Schore in his book “AffectRegulation and the Origin of the Self: TheNeurobiology of Emotional Development”(1994). Page numbers are provided for salient

points to enable the interested reader toexamine key areas in more depth.

In his work, Schore examines thepsychological developmental stages describedin the psychoanalytic and object relationsliterature and correlates behavior with specificbrain structures known to develop during eachof the psychological stages. The resultingdevelopmental neuroscientific theoryintegrates research from over 2500 studies in anumber of fields to provide a detailedexplanation of the socioemotional factors thatinfluence the physiology, endocrinology, andpsychological processes associated with theexperience-dependent maturation of thenervous system (Schore, 1994). Schoredescribes the role of the primary caregiver asbeing the key environmental factor involved inshaping the infant’s developing nervoussystem stating that, “for the developing infant,the mother is the environment” (1994, p. 78).

“Increasingly complex self-regulatorystructural systems mature during infancy, andtheir development is a product of earlydynamic object relational environmentalinteractions that shape the outcome of geneticpredispositions”(Schore, 1994, p. 34). In afascinating evolutionary adaptation thatenables increased plasticity and flexibility inthe human brain, infants are extremelyvulnerable at birth and in early life. The infanttherefore needs an external regulator, and thisfunction is filled by the primary caregiver.

In Schore’s (1994) detailed analysis of thedevelopment of the nervous system, it becomesevident that the interdependence betweenemotions and their physiological correlatesprovide the foundation on which the nervoussystem matures and develops its excitatory andinhibitory capacities for self-regulation.“Emotional expression is mediated by theenergy-mobilizing sympathetic and energy-conserving parasympathetic components of theautonomic nervous system (Truex &Carpenter, 1964, as cited in Schore, 1994, p.30), and these components continue to developpostnatally” (Schore, 1994, p. 30).

In this (1994) and other works (2001a;2001b), Schore emphasizes how interactionsinfluence the regulation of nervous systemactivities that determine secure and insecure

The Role of Attachment



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styles of attachment expressed at physiologicalas well as psychological levels. These earlyexperiences shape the short and long-termphysiological capacities of the nervous systemthat are involved in coping with stress. Thephysiological responses to stress involvevarying levels of sympathetic (SNS1) andparasympathetic nervous system (PNS)activity, as well as autonomic (ANS) andcentral nervous system (CNS) regulation andinhibition.

This information provides a foundationfor understanding ways in which stimuli areintegrated by the brain to formulate responsesto a particular environment. Early interactionsinfluence these responses (Schore, 1994) inways that maximize, or interfere with, thecapacity of the organism to engage in the moreenergy-efficient recent evolutionary strategiesof nervous system responses to threat (2001).The capacity of the organism to fluidly movebetween a range of attachment and defensivestrategies as its environment changes isrelevant to the origins of disease (1994). Thissection seeks to present sufficient detailconcerning the manner in which the nervoussystem is affected during development toenable the reader to consider the role ofattachment in early life as a possible source ofrisk for, as well as protection against, thedevelopment of disease such as diabetes,multiple sclerosis, and Parkinsons’ as well asunusual symptoms such as globus, chronicpain, and nervous tics.

The Role of AttachmentThe attachment process has a major

influence on the growing nervous system,particularly during critical periods of intensegrowth and pruning in the first few years oflife. The quality of the behavioral andphysiological interactions between infant andmother is related to the degree to which they

1 ANS: Autonomic Nervous System; PNS:Parasympathetic Nervous System; SNS:Sympathetic Nervous System; CNS: CentralNervous system

bond2. This bond imprints the developingbrain in such a way as to influence theindividual’s capacity for autonomousphysiological as well as psychological self-regulation. It helps an infant regulate basicmetabolic processes such as body temperatureand digestion, and gradually facilitates thelearning of patterns of CNS, SNS and PNScommunication, dominance, and regulatorycapacity. These patterns of nervous systemregulation generally last into adulthood.

Schore (1994) describes the manner inwhich an infant progresses from physiologicalstages of total dependence on the motherduring the psychological developmental stageof symbiosis, to the capacity to self-regulate ata physiological level during theseparation/individuation phase. The followingoverview briefly summarizes these stages andis followed by a detailed description of eachstage (see Table 2-6). This section is notexhaustive although the degree of detailpresented sets the stage for a clearunderstanding of environment-braininteractions that influence differences inindividual responses to stress. Stress isthought to play a role in the development ofmany chronic illnesses as well as in day-to-dayvariation in symptoms.

Brief Overview of the DevelopmentalNeurophysiology of Brain Growth

I. The attachment period begins atapproximately 8 weeks, when geneticallyprogrammed synapse formation reaches aparticular phase in the development of thevisual cortex. Following this period, mother-infant gaze transactions intensify. During theearly symbiotic period occurring between 2and 8 months of age, these gaze transactionsspecifically foster growth of SNS circuits fromthe subcortex to centers in the maturing frontalcortex, which have greater hierarchicalregulatory capacity.

II. The next phase begins at 10-12 monthsas growth in the frontal cortex promotes

2 The mother is generally referred to by Schore andother authors as being the primary caregiver.



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locomotion and upright stance, which enablesthe infant to engage or disengage more activelywith his environment (Schore, 1994, p.93).This phase of increased mobility, described asthe practicing period in developmentalpsychoanalytic terms, is associated with highsympathetic arousal and a correspondingemotional tone of elation in which the infantseems impervious to failure. This early part ofthe practicing phase is specifically associatedwith development of the prefrontal cortex, andits more dominant right side. Nervous systemdevelopment at this time is predominantlymediated by sympathetic hyperarousal, whichpromotes elation, interest, and exploration ofthe environment. Such mobilization activitiesmature early because the activities and energylevels they foster literally promote the growthof an abundance of nerves and nerveconnections.

III. At 16-18 months the toddler enters thelate practicing phase. During this time,anatomical development in brain growth isassociated with the beginning of inhibitorybehavior as the mother (unconsciously) beginsto socialize her child by prohibiting certainactivities now deemed unacceptable. These“socializing” activities curb the state of highsympathetic arousal to promote thedevelopment of important energy-conservingstates of moderate arousal. These interactionsenable the cortex to inhibit states of high SNSarousal and to grow the capacity for PNScircuits that foster levels of moderate arousal.These activities also enable the nervous systemto learn to transition from one state of arousalto another, a skill vital to adaptation and themaintenance of homeostasis.

During this late practicing phase, nervecircuits begin to grow downward from thecortex to the subcortical structures of the ANS.These circuits are inhibitory in nature, and areparasympathetic. In this stage, the toddler isno longer impervious or elated. Instead, he isquite sensitive to his mother’s inhibitingbehavior and easily experiences “shame”,which Schore (1994) describes as the state thatshuts off SNS activity. The physiological stateof low PNS arousal is related to theimmobility/freeze response.

The quality of the reunions following theshame-inducing interactions facilitates atransition to a new state of arousal. This newarousal state is a PNS mediated moderate levelof energy associated with inactive alertness.Inactive alertness is optimal for learning,restoration, and integrative functions andoccurs as a result of the capacity to inhibitimpulsive behavior. The experiencesassociated with moderate arousal influence theselective pruning of nerves and nerveconnections and inhibitory function thereforematures later than growth-promoting states ofhyperarousal. By the middle of the secondyear, maternal-infant transactions haveincreased the infant’s capacity to self-regulate,and he is able to transition from SNSdominance to PNS dominant states and backagain in response to external and internal cueseven when he is not in the presence of hiscaregiver (Schore, 1994, p. 230).

IV. The end of the late practicing periodmarks a transition into the rapprochementphase, which is characterized by ambivalencetowards the mother and takes place from 15 to18 months of age. During this time, the fatherplays an increasing role in arousal modulationthat influences the development of the leftcerebral cortex, which is “the last area of thebrain to attain functional maturation” (Schore,1994, p. 234). This part of the brain interactswith the right hemisphere to facilitate ANSregulation and continues to develop at leastuntil adolescence (Diamond, 1990,Huttenlocher 1982, and Thatcher 1991, ascited in Schore, 1994).

The Development of the Nervous System

The immaturity of the nervous system atbirth allows it to be shaped by its environment,which facilitates its capacity to adapt to itsown unique circumstances (Siegel, 1999). Thehuman brain undergoes dramatic growthbeginning in approximately the third month ofpregnancy and continuing until 18-to-24months of age (Allan N. Schore, 2001b). Ashas been mentioned, the primary processes that



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drive brain growth are genetic andenvironmental. The process of brain growthconsists of the development of nerves and anoverabundance of synapses and connectionswhich are then shaped, selected, and pruned asa result of genetically programmed timing(Bruer, 1998) as well as by interaction with theenvironment (Kotulak, 1998; NCRIM, 2000;A. N. Schore, 1994; Siegel, 1999). Theprocess during which environmental factorsinfluence the genetically timed development ofthe nervous system is referred to asexperience-dependent maturation.

The experience-dependent maturation ofthe brain occurs primarily through the socialand emotional context of interactions with theprimary caregiver, in which affect regulatesbrain growth (Trevarthen, 1989, as cited inSchore, 1994, p. 78).

Although the caregiver’s role in nervoussystem development is central, it is not the soleenvironmental contributor. Factors outside ofa caregiver’s control, including his or her ownchildhood experiences and the culturalenvironment in which these have occurred,also shape the manner in which interactionsoccur between parent and child (Brazelton &Cramer, 1990; Klaus & Kennell, 1976; A. N.Schore, 1994).

In addition, prenatal and perinatal eventsinfluence 3 shape the manner in which parentsand infants are able to bond with one other, anevent that greatly affects their ability to attuneduring attachment (Klaus & Kennell, 1976).Prenatal and perinatal events also shape thenervous system and influence its capacity torespond to stress, including the stress thatoccurs in interactions during the attachmentperiod and beyond (Klaus & Kennell, 1976).Finally, these prenatal and perinatal eventsmay also influence the infant in ways that canevoke particular styles of attachment behaviorfrom caregivers and that contribute to theunique style of interaction that occurs betweena parent and child (NRCIM, 2000). Forexample, an infant who has experienced adisruption in bonding may cry more 3 see Thesis Section / Article on Prenatal andPerinatal Factors, which can be downloaded fromhttp://veroniquemead.com/library.php

frequently. Instead of eliciting increasedcaretaking behaviors, however, this expressionof distress may overwhelm a similarly poorlybonded mother and result in distancing anddissociation.

The Four Periods of Attachment

I. Symbiosis, Gaze Transactions, and theDeveloping ANS

While infants and mothers gaze at eachother from birth (Klaus & Kennell, 1976),fixation on the mother’s eyes increases afterthe second month (Maurer & Salapatke, 1976,as cited in Schore, 1994, p. 72), during thesymbiotic phase of “pronounced dependency”(Corey, 2001). This shift in the importance ofgaze transactions occurs following a growthspurt of the visual cortex during the weeks thatprecede the onset of this period. Gazetransactions influence the infant’s growingnervous system through imprinting (Schore,1994, p. 75), a process by which the“heightened energy in the new parent andsmall baby … leads them to attach to and learnabout each other” (Brazelton & Cramer, 1990).

The visual perception of facialexpressions has been shown to be the mostsalient channel of nonverbal communication(Izard, 1971, as cited in Schore, 1994), andvisual modes of communication that precedevocal modes of mutual communication(Schaffer 1984, as cited in Schore, 1994) aredominant in the forging of preverbal affectiveties in the first year of life (Schore, 1994, p.72).

Gaze interactions as mediators of nervoussystem growth.

The process of imprinting specificallyaffects the earlier maturing right hemisphere ofthe brain (Schore, 1994, p.76), which isdominant for gaze behavior (Meador et al.,1989, as cited in Schore, 1994, p. 75). Thishemisphere is also specialized for attending tofacial emotion (Etcoff, 1983a, as cited inSchore, 1994), and controls the ANS andendocrine systems involved in emotionalfunctions (Schore, 1994, p. 59). The mannerin which caregivers modulate gaze transactions



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directly affects nervous system development.These experiences affect the infant’ssympathetic nervous system by fostering his 4

capacity to tolerate increasing levels ofarousal, and influence the development of hismore slowly growing PNS through the mannerin which he learns to recover from theseperiods.

This process of visual interaction isfacilitated by naturally occurring events suchas the fact that infants, who are able to focusmost clearly on objects 10 inches away(Haynes, White, & Held, 1965, as cited inSchore, 1994), tend to be held by mothers atthis distance (Papousek & Papousek, 1979, ascited in Schore, 1994). This is also thedistance between the face of mother and infantduring breastfeeding, when she cradles herinfant in her arms.

Interactive states are intensely pleasurableto infants (Stern, 2000) as well as to theircaregivers (Schore, 1994), and represent aprocess by which inherent biologicalmechanisms stimulate or drive attachmentbehaviors. During periods of mutual gazebetween mother and infant, “the emotionalexpressions of one member of the mother-infant … relationship tend to elicit emotions inthe other” (Termine & Izard, 1988, as cited inSchore, 1994, p. 80). Attuned mothersstimulate their infants to increasing levels ofarousal through natural, unconscious behaviorsthat are particularly evoked by the eyes.

“The sight of her infant is physiologicallyarousing to the mother” (Wiesenfeld &Klorman, 1978, as cited in Schore, 1994) andmothers’ eyes dilate when they see theirinfants. Experimenters with dilated eyes evokemore smiles in infants, and dilatation ininfants’ pupils releases caregiver behavior. Inaddition, pupil dilatation in one individualevokes dilatation in another’s (Hess, 1965, ascited in Schore, 1994).

Pupil dilatation is regulated byhypothalamic centers that regulate the SNS(Truex & Carpenter 1964, as cited in Schore,1994) and occurs with states of interest(Schore, 1994, p.73), as well as in the arousal 4 the use of masculine and feminine pronouns isvaried throughout this document

of fight/flight (Ganong, 2001). The type ofpupil dilatation involved in maternal-childinteractions appears to be different from that offight/flight, however. In attachmentinteractions, pupil dilatation is described ascoming from “a state of alert inactivity inwhich the eyes are open and have a ‘brightshiny appearance’” (Demos, 1988, as cited inSchore, 1994, p. 73) and corresponds to asimilar state in the infant (Brazelton & Cramer,1990). This is also supported in research byTronick, Ricks, & Cohn, (1982, as cited inSchore, 1994), who find that infants exposed tomothers with no ‘brightness’ in their eyesexpress negative states. This author (V Mead)speculates as to whether the gaze and facialinteractions of early life relate to activity of theparasympathetic aspects of the socialengagement system mediated by the VVC 5

(Porges, 2001), or in instead by a process ofvagal withdrawal that facilitates SNS activityin an energy-conserving manner. Insufficientinformation is available to pursue thisexploration at this time.

Gaze interactions and sympatheticnervous system development.

Prolonged gaze is “the most intense formof interpersonal communication” (Tomkins,1963, as cited in Schore, 1994, p. 72) andinstigates high levels of arousal in bothparticipants. This high level of arousal isfacilitated by dopamine and opioids in thereward centers of the brain (Schore, 1994, p.91). Dopamine is a SNS catecholamine whoseeffect differs from norepinephrine-mediatedstates of arousal such as fight/flight in that it isassociated with pleasure and reward systems.The dopamine system connects subcorticalareas of the SNS to the cortex, and morespecifically, to the right hemisphere. Whilethis growth occurs as part of the geneticallyprogrammed development that is associatedwith this period of infant development, thehigh arousal in gaze transactions facilitatesbrain growth by influencing the density andstrength of the connections. The specificdopamine pathway by which the lower or 5 ventral vagal complex of the social engagementsystem as described by Porges



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subcortical parts of the brain connect with thecortex is called the “ventral tegmental”dopamine circuit (Schore, 1994, p. 83).

This ventral tegmental circuit extends tothe orbitofrontal cortex, which is an area in thefront of the brain that is located above andbehind the eye. This functional designation isdivided into two areas, the early maturingorbitofrontal cortex and the later maturingdorsolateral cortex (see figure 2-8 on the nextpage). The orbitofrontal cortex is responsiblefor the regulation of socioemotionalfunctioning and therefore mediates relevantANS functions, such as relational interactionsand arousal states such as fight/flight.

Gaze interactions and parasympatheticnervous system development.

Another factor involved in gazetransactions and nervous system developmentis associated with PNS function, which cycleswith SNS activity to support optimal levels ofarousal in the infant. These cycles are brief,often lasting only seconds, but are measurablein microanalysis of frame-by-frame videoobservations in studies cited by Brazelton &Cramer (1990), Stern (2000), and Schore(1994).

When an infant reaches her tolerance ofstimulation she “gaze averts to self-regulateemotional arousal and … reduces her input soas to provide an optimal level of arousal(Brazelton and Cramer, 1990, p. 105).Psychobiologically, gaze aversion is a ‘cut-off’arousal reducing mechanism (Chance, 1962, ascited in Schore, 1994, p.85) which dischargesan overload of social information processing”([italics added] Schore, 1994, p. 85). Schoredoes not expand on the process by which asystem “discharges” although the term isdescribed in somatic psychology as a functionby which the nervous system physicallyreleases a high energy state (Caldwell, 2001).

The discharging activity may consist oftiny movements such as gaze aversion with orwithout head turn. Discharge behavior canrange from the large muscular activity offight/flight to subtle invisible processes(Caldwell, 2001) that might occur as a result of

physiological activity. 6PNS development, which occurs during

gaze transactions, relates to the degree ofbonding and attunement between mother andchild (Schore, 1994). The more attuned amother is to her infant, the more she respondsto gaze aversion by modulating her ownbehavior to foster the delivery of appropriateamounts of information that can be processedby the infant’s developing right hemisphere(Schore, 1994, p.87).

The more the mother “tunes” heractivity level to the infant during periods ofsocial engagement, and the more she allowshim to recover quietly in periods ofdisengagement, the more synchronized theirinteraction (Penman, Meares, and Milgrom-Friedman, 1983, p. 1, as cited in Schore, 1994,p. 86).

The decrease in maternal stimulation in anattuned dyad allows the infant to recuperate ina state of moderate rather than elevated ordepressed arousal. When ready, the infantinitiates eye contact as a signal that she isready for more stimulation. By facilitatingthese transactions, the mother acts as anexternal regulator (Schore, 1994, p. 87) or“auxiliary cortex” (Hofer, 1984, as cited inSchore, 1994) for her developing infant.Consistent experience of this type of arousalmodulation enables the infant to learn that shecan engage according to her own state of

6 The process by which discharge occurs is an

interesting one in that it appears to consist of ameans by which organisms integrate andmetabolize information. Based on the discussionpresented above, physical and physiologicaldischarge and integration appear to be the means bywhich the ANS transitions from states of high tolow arousal. This is an interesting issue to considerbecause the capacity of the nervous system totransition between states of arousal is important tothe ability of an organism to adapt, and hence, mayaffect risk for disease.

From this perspective, the physiologicalprocess by which glucose is removed from thebloodstream through the actions of fighting orfleeing may also represent a form of discharge.One hypothesis of this thesis is that lack ofdischarge may eventually become visible as type 1diabetes. This concept is discussed in Chapter 3.



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readiness.In disorganized or less optimal

attunement interactions, a mother maycontinue to talk to and stimulate her child after

gaze aversion, resulting in further stimulationof an infant that has already reached hertolerance level.

Figure 2-8. The Prefrontal Cortex.Image adapted from “The prefrontal cortex” in Affect Regulation and the Origin of the Self: TheNeurobiology of Emotional Development (Schore, 1994, p. 36).

Infant responses to this consequent overloadare expressed as increased PNS arousal and areassociated with distress generally expressedthrough crying. In somatic psychology theory(Caldwell, 2001), crying can be consideredanother form of discharge, and one that couldbe considered more energetically demandingthan quiet gaze aversion.

There are less than optimal consequencesof misattunement for the developing PNS.When a caregiver consistently and repeatedlymisses gaze aversion cues and continues toprovide stimulation, the infant does not

experience the opportunity to quietly recover,and consequently, neither does her PNS(Schore, 1994). Furthermore, the infant learnsthat her signals telling her environment thatshe has had enough are not effective. In thelong-term, this experience affects the mannerin which this individual behaves in futureinteractions and if persistent, becomesincorporated into preverbal memory and in theway she perceives her environment (Schore,1994). She may learn, at a physiological level,that her interpretation of having had enoughstimulation is “incorrect”. She may also



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develop difficulty in her capacity to self-soothe, which is a part of the self-regulatingprocess of regenerative periods that occur inquiet states (Schore, 1994). If theseoverwhelming experiences are sufficientlyfrequent or intense, the infant may learn todischarge the intolerable levels of arousalthrough dissociative behaviors in an attempt toself-soothe (2001). Such behaviors maybecome patterns of dissociation that last intoadulthood. These are consistent withdisplacement behaviors, which Caldwell refersto as “movement tags” (2001).

Caldwell refers to movement tags as aform of somatic addiction, an addiction tocertain body habits used in an ineffectiveattempt to discharge intolerable states throughmovement (2001). She defines a tag in thefollowing way:

A tag is a small movement or gesturedone anywhere in the body thatdistracted a person from the movementsequence they had been developing. Inorder for a movement to qualify as atag, it had to exhibit all five of thefollowing features: 1) it repeats, …often to the point of exhaustion, 2) itdoesn’t develop – the movement nevergoes anywhere … never progresses, 3)it doesn’t complete – it never feelsfinished, never comes to a relaxedconclusion, 4) it doesn’t satisfy – itmay feel familiar and comfortable,even initially soothing, but the moreyou do it the less soothing it feels ….5) it’s difficult to watch [because] wefeel disturbed in the presence ofsomeone dissociating (p. 8).

Dissociative patterns of discharge may last intoadulthood and affect the capacity forphysiological transitions between states ofarousal (Caldwell, 2001; A. N. Schore, 1994).An infant consistently exposed tooverwhelming levels of stimulation may learnto discharge intolerable levels of arousalthrough patterns of less efficient, more energy-demanding behaviors. Such behaviors may,according to the hypotheses presented in thisthesis, be expressed as chronic illness andphysical symptoms, representing physiological“movement tags”.

The role of misattunement in mediatingtolerance for increased levels of arousal.

Periods of misattunement are commonbetween caregiver and child, and serve animportant function. The manner in which themother instigates as well as “repairs”misattuned transactions influences the growingnervous system. If she ignores gaze aversionsor overstimulates her infant, arousal states toooverwhelming for the infant to regulate on herown can ensue.

The effects of misattunement areparticularly influenced by the manner in whicha mother reattunes following a period ofoverwhelming stimulus. If a motherrecognizes this and has the capacity toreattune, the infant gradually learns that thepossibility of repair exists. The experience ofbrief and slight overwhelm during misattunedinteractions generates a greater capacity in theinfant to tolerate undischarged SNS arousal,and fosters the growth of a more robust SNS.“An essential function of the mother is topermit the child to bear increasingly intenseaffective tension, but then to step in andcomfort the child before his emotionsoverwhelm him” (Krystal, 1978, as cited inSchore, 1994). “ The mother’s prevailingtendency to overshoot, just by a little, herinfant’s tolerance boundaries induces the infantto stretch and grow” (McLaughlin, 1989, ascited in Schore, 1994, p. 89).

‘In the “symbiotic” state, the adult’sand infant’s individual homeostaticmechanisms are linked together in asuperordinate organization whichallows for ‘mutual regulation of vitalendocrine, autonomic, and centralnervous systems of both mother andinfant by elements of their interactionwith each other’ [Hofer, 1990, p. 71]’…. Indeed, … [Hofer, (1984a)]provides evidence to show that themother is t h e regulator of thefunctioning of the infant’s developingautonomic nervous system (Schore,1994, p.78).

The child’s increasing ability to tolerateemotional intensity is visible during thisperiod, and is correlated physiologically with



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changes in heart rate (Schore, 1994). At theage of 3 months, infants’ heart rates decreasewith smiling and by 9 months, babies showheart-rate acceleration during smiling (Emde,Campos, Reich, & Gaensbauer, 1978, as citedin Schore, 1994, p. 89). Schore’s point is thatthis represents an augmented capacity totolerate the high SNS arousal states that occurin the increasingly intense and joyfulattachment interactions, and is associated withdevelopment of the SNS. The capacity totolerate high levels of arousal influences theinfant’s ability to regulate the high levels ofintensely positive affect that are the hallmarkof the early practicing phase known asseparation/individuation, which followssymbiosis.

II. The Early Practicing Period: ActiveArousal and Sympathetic Growth

The onset of the early practicing periodbegins at the end of the first year. It is definedby changes in locomotion and mobility as theinfant enters the vertical plane and begins towalk, and is also described in object relationsterms as the phase of separation/individuation(Mahler, 1980, as cited in Schore, 1994). Thistime period is particularly associated with theformation of an enduring attachment bond,which fosters nervous system growth andshapes the manner in which this individual willrespond to his or her socioemotionalenvironment.

Schore (1994) considers the affectivequalities of this stage to be the most uniqueand definitional, saying, “mobile infants showdifferent types of emotional reactions thanprelocomotor infants” (Bertenthal, Campos,and Barrett, 1983, as cited in Schore, 1994, p93). These dramatic affective transformationsare critical to the establishment of permanentcharacteristics of the emerging personality.Perhaps more than any other time in thelifespan, the individual’s internal state isexternally observable and susceptible tosocioenvironmental influences (Schore, 1994,p. 93).

This period is characterized by high levelsof arousal, elevated activity level, and anemotional tone of elation, all of which areassociated with an increase in sympathetic

activity (Schore, 1994). These qualities, whichdefine active infant play, fulfill anevolutionarily adaptive function for learningand stimulation that foster the growth of nervesand brain structure (Schore, 1994). The degreeto which the infant experiences motivation,interest, and elation are dependent on the levelto which he has learned to tolerate states ofarousal during the previous symbiotic phase.ANS growth in the preceding period,particularly sympathetic development, isimportant to the ability of the sympathetic tofoster behaviors that support brain growth inthis phase.

In concordance with his overall theory,Schore (1994) explains that the structures thatare developing during this time are influencedby genetic factors that affect behavior (byfostering high activity levels and elation duringthis time period, for example). Thesebehaviors, and the interactions that occur withcaregivers as a result, in turn influence thematuration of these brain structures.Excitement and interest foster stimulation-seeking behaviors that promote the explorationof the newly available nonmaternalenvironment, and are specifically associatedwith the development of connections that linkthe ANS structures, such as the hypothalamus,with the higher structures of the cortex. Theseconnections form as a result of an expansion ofthe ventral tegmental dopamine circuit as itconnects upward to the orbitofrontal region ofthe right prefrontal cortex.

The orbitofrontal cortex is particularlyimportant in the ability to assess one’senvironment, and perception determines howan individual responds. The early part of thepracticing period imprints this system in a waythat “for the rest of the lifespan appraises theaffective and motivational significance ofenvironmental stimuli” (Schore, 1994, p. 113).The relationship dynamics between caregiverand infant during this time therefore have aparticular impact on the manner in whichstructures and connections mature thatinfluence the perceptions of the growinginfant.

The Caregiver as a “Secure Base” and anIndicator of Safety.



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During this period of infant curiosity andexploration, the mother continues to serve as apsychobiological regulator (Taylor, 1987, ascited in Schore, 1994, p. 26). She helps herinfant transition into optimal levels of arousalby energizing him at appropriate times whenhe is in low energy states, as well as bymodulating or “down-regulating” when he is innonoptimal high levels of arousal (Schore,1994, p. 107). As the infant now movesbetween his new environment and his motherhe begins to learn to self-regulate, which nowoccurs when he is “alone” yet still in herpresence.

The infant is motivated to leave thepresence of his mother by his sympatheticallygenerated curiosity, interest and high energylevels, and is capable of leaving because sherepresents a locus of safety. The safetyfunction of the attachment bond thus provides“a ‘secure base’ from which the mobile toddlermay sortie to explore the world and then returnin the face of physiological need or danger”(Bowlby, 1988a, as cited in Schore, 1994, p.102). In this context, the infant, who is“increasingly sensitive to her gaze, keeps aneye on the feelings expressed on the mother’sface. The child thereby uses the mother’saffective expressions as a signal, an indicatorof her appraisal of danger or safety in aparticular environmental circumstance”(Oakley & Jenkins, 1992, as cited in Schore,1994, p. 102).

The mother’s facial expressions,including those that are highly transient andinvisible to conscious awareness, transmitinformation to her child. The child’s ability tointerpret this meaning is therefore vital to hissurvival from an evolutionary perspective.The capacity for appraisal of the environmentis highly tuned to facial expression, and isspecifically facilitated by the developing rightorbitofrontal cortex. Because infant states ofhigh arousal and interest facilitate brain andstructural growth, maternal behaviors thataffect the capacity to experience these statesalso influence this phase of brain development(Schore, 1994, p. 102).

Interactions and alternating sympatheticparasympathetic dominance.

During the period that the child is awayfrom his mother, sympathetically drivenexploration and locomotion enable him toexplore the environment under his ownvolition. These periods of sympathetic arousalare interspersed by states of parasympatheticarousal and are followed by a return to statesof sympathetic activity through reuniontransactions with the mother. Althoughinteractions during this period arepredominantly mediated by sympatheticarousal, they also support oscillation innervous system balance.

The mother, through her entrainedinteractions, directly influences thedeveloping rhythmic pattern of thechild’s activity-passivity cycles. Inthis manner the primary caregiver’sunique patterns of psychobiologicalattunement, misattunement, andreattunement effect the creation ofcycles of social engagement anddisengagement in the infant... Themother’s rhythmic responsivenessregulates the autonomic, behavioral,neurochemical, and hormonalfunctions of the infant” (Anders andZeanah, 1984, as cited in Schore,1994, p. 107).

States of low energy followingexploratory behavior are visible in the tiredchild who has limp arms and drooping face,and who is in a state of parasympatheticdominance. Schore once again describes thetransition into this state as occurring through“discharge”. This discharge seems to mark thetransition from states of sympatheticdominance to parasympathetic dominance andthe term has been described in an earliersection with respect to the regulatory functionof gaze aversion.

When the child is in the low energy statefollowing sorties, he is also in a state ofparasympathetic receptivity in which he can beinfluenced by interaction with his mother, whocan increase his arousal and reenergize him toexplore. This transition from parasympatheticto sympathetic dominance occurs duringreunion episodes, and may occur at a distancethrough visual cues, or through proximityand/or contact. During reunions, mothers read



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their infants’ faces to appraise their internalstates and adjust their output to provide theoptimal level of response or stimulus (Schore,1994, p. 103). This maternal capacity occursat an unconscious level, and is most developedin dyads that are “biologically attuned”(Schore, 1994).

In psychobiological attunement, “thelanguage of mother and infant consists ofsignals produced by the autonomic,involuntary nervous system in both partners “(Basch, 1976, as cited in Schore, 1994, p. 105).Maternal regulation of the behavioral and ANSstates of the infant occurs at a nonverbal level,and is primarily regulated by the maturingright prefrontal cortex. The right prefrontalcortex is also influenced by these transactions.

The manner by which the mother is ableto reenergize her infant is increasinglyunderstood in the scientific community(Schore, 1994). As described earlier, theattachment bond is pleasurable, and during thisdevelopmental period pleasure is associatedwith sympathetic dopamine activity. Duringthe energizing process that Mahler refers to as“refueling” (Mahler, 1980, as cited in Schore,1994, p. 104), interactions with the motherresult in increases in heart rate in her toddler.During reunion episodes, the mother serves asan “amplifier of positive arousal, and “acts as agenerator of energy required for furtherphysical exploration of the environment by theinfant. This allows for ongoing separationsand reconnections” (Schore, 1994, p. 102).

Characteristics of the maturing brain.Characteristics of nervous system

development relevant to this stage of infantdevelopment are presented below, including 1)the role of dopamine in brain growth, 2) thedominance of nervous system excitation overinhibition, and 3) the “internalization” ofvisual experiences. These processes helpshape conditioned responses and thedevelopment of self-regulation duringexperience-dependent maturation.

Dopamine.During the early practicing period, the

dopamine circuit that connects thehypothalamus and other subcortical areas tothe right (and not the left) orbitofrontal cortex

matures. While a number of dopamine-mediated brain structures grow during thisdevelopmental period, research shows that incomparison with other structures, thedevelopment of the orbitofrontal structurerequires social stimulation for optimaldevelopment (Holson, Ali, and Scallet, 1988,as cited in Schore, 1994, p. 131). During theearly part of the practicing period, pleasurablequalities of social interaction, which areimportant to SNS fostered nervous systemgrowth, are mediated and intensified bydopamine. During the formation of theenduring attachment bond in this period,“amplified [high] levels of arousal act as asignal for the imprinting of new circuits in theorbitofrontal cortex” (Schore, 1994, p. 134).Dopamine supports nervous system growth byincreasing availability of fuel to the developingtissues. This fuel is glucose, and dopaminemakes it available by “degrading glycogen toglucose and … converting glucose to [specifictypes of] sugars (Schore, 1994, p. 134).

Excitation versus Inhibition.The characteristic high arousal of this

period represents an imbalance in total brainfunctioning in which excitation is morepredominant than inhibition. Dopamine playsa role in that it mediates general arousal that“produces energy-expending increasedexcitability of the orbitofrontal cortex”(Schore, 1994, p. 134).

Internalized Images The developing right orbitofrontal cortex

has many different functions, including acapacity to regulate the ANS through a verydirect one-synapse connection to thehypothalamus (Schore, 1994). This part of thebrain also controls arousal and aggression inaddition to homeostasis. Connections betweenthe visual cortex and the orbitofrontal cortexthat form during this period allow thedeveloping right frontal brain to receive,appraise, and respond to cues coming fromboth the external and the internal environment.

As a result of repeated exposure toexperiences of the caregivers’ behavioral,physiologic, and emotional responses, whichare expressed through facial gestures, visualimages that correlate with these experiencesbecome “internalized” in the infant through the



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process of conditioned procedural memory”(Scaer, 2001a; Schore, 1994). These visualsnapshots become “flashbulb memories” andare recalled unconsciously when similarsituations recur throughout life, including attimes when the mother is not present. Thecapacity to form memories and to evokeresponses to previous experiences serves thefunction of enabling the infant to develop thecapacity to self-regulate behavior.

The process of internalization results inadaptive (or maladaptive) conditionedresponses in the infant that are affected byinternal cues, such as sensations coming fromhis own physiology, and external cues, such asthe experience of seeing people’s emotionallyexpressive faces.

The internalization of images ofpsychobiologically regulating others, as wellas other types of experiences, is a memory thatserves an affect regulating function. When achild or adult encounters a new person, forexample, the imprinted flashbulb memory isaccessed as a reference from which to interpretthe meaning of the newcomer’s facialexpressions, and guides the response andassociated activation levels. The accessedmemory is the internalized visual image of hismother’s face and gestures, organized throughhis unique experience of her. This process alsooccurs with respect to inanimate objects. If achild comes up to a burning fire in thefireplace, for example, the recollection of hismother’s misattuning facial gesture that onceconveyed a message of “NO!” is accessed andprovides the internal cue that fosters the self-regulatory action of impulse inhibition.

In the further course of development,repeated experiences of separation andreunion are remembered andanticipated, providing the structuralbasis for progressively more variedand modulated affective responses,whether basically painful or basicallypleasurable (Pao, 1971, p. 788, as citedin Schore, 1994, p. 103).

III. The Late Practicing Period: Shame,Passive Arousal, and ParasympatheticGrowth

The late practicing period consists of a

transition away from positive emotional statestowards more fearful states. This transition isinfluenced in part by maternal behavior, whichchanges from the high affection, play, andcaregiving activities of the early practicingperiod to behavior associated with prohibitionand socialization. The mother’s behaviorseems to occur in response to a child who nowhas a well developed sympathetic high arousalsystem that leads him to get into things and toseek to have his way despite knowing what hisparents want (Schore, 1994, p. 200). Thesematernal expectations change in a way thatnow fosters the growth of inhibitory impulsesas she demands that her child delay behaviorthat is eminently pleasurable. This maternalbehavior fosters the child’s capacity to curbimpulse behavior and facilitates thedevelopment of the inhibitory parasympatheticsystem.

The transition from states of high arousalto low arousal and back again occur in thisperiod, with an emphasis this time on the lowarousal state. This activity helps establish twomature branches of the ANS and influences thecapacity of the higher brain to regulate thesefunctions. Orbitofrontal regulation isimportant since this area of the CNS canintegrate information from outside as well asinside of the body to coordinate the mostappropriate response. Following this stage, theinfant develops the capacity for an efficientlevel of arousal called the “alert inactive” state,which consists of neither high nor low arousaland is associated with the capacity to maintainfocused interest and attention. This author (V.Mead) hypothesizes that misattunement duringthis period, which involves frequentexperiences of shame, transitions to states ofparasympathetic dominance may play a role inchronic illness such as some forms of chronicfatigue, to name one example.

This late stage of the practicing period isgenerally known for its cognitive, social, andbehavioral prohibitions. Schore, however,views the role of affective communication(rather than behavioral and cognitive activities)as the key to nervous system maturation. Theaffective interaction emphasized by (1994) isnonverbally communicated through maternalfacial expressions that convey misattunement



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and foster what Schore (1994) classifies as“shame” in the child (Schore, 1994, p. 200).Active misattunement induces stress in thechild, and results in a change from asympathetic state of high arousal to one ofparasympathetic low arousal. Misattunementstops the dopamine and opioid fostered growthof sympathetic hyperarousal in theorbitofrontal cortex and the resultant stressfrom the unfamiliar and unpleasant interactionleads to increased levels of cortisol. Cortisolfosters the growth of cholinergicparasympathetic nerve connections from theorbitofrontal cortex to the hypothalamus andother lower brain centers. This new nervepathway enables higher cortical centers toinhibit the SNS.

Schore (1994) explains that the lowarousal states evoked by shame transactions,which are then modulated by importantreunion episodes with the mother, provide theoptimal condition of stress and stimulationrequired for the maturation of the inhibitoryfunctions of the cortex- parasympatheticconnections. As a part of the continuedprogrammed growth of the infant’s nervoussystem, the mother’s behavior changes as anunconscious and adaptive means of providingappropriate environments for her child.

Misattunement and shame-inducedstates of low arousal.

In this late practicing period, the child isno longer impervious to frustration and isinstead quite sensitive to the inhibitory actionsof his mother. Increased levels of adrenalcortisol production that occur as a result ofprogrammed brain development appear tofoster this change in infant affect, and thestress arising from the change in interactiondynamics influences further production ofcortisol. “Stress is defined as a change or athreat of change demanding organismicadaptation” (Schneiderman & McCabe, 1985,as cited in Schore, 1994, p. 209) and can thusoccur in response to a novel stimulus, even if itis a positive event such as a birthday party.

During this stage, toddlers have fairlymature sympathetic nervous systems and livein increasingly active states of high arousal.When seeking interaction with their mothers,

they come to her in states of high arousal andexcitement and expect to be greeted bysatisfyingly positive states of high arousal andjoy as they have in the past. During thisperiod, however, the toddler is greeted with anunfamiliar and “different” mother, one whoactively misattunes. This experience isunexpected and therefore stressful, and “theinfant is ... propelled into an intensified lowarousal state which he cannot yet autoregulate”(Schore, 1994, p. 203).

The shift in the infant from a state ofactive arousal to one of passive arousal isinduced by an experience of what Schore(1994) terms “shame”. Shame is evoked bythe facial expressions used by the mother.Shame fosters the rapid transition from apreexisting high arousal positive hedonic stateto a low arousal negative hedonic state ... andoccurs only when the individual isexperiencing interest-excitement or enjoyment-joy. This negative affect, a specific inhibitionof ongoing positive affects, is thus the infant’simmediate... physiological-emotional responseto an interruption in the flow of an anticipatedmaternal regulatory ... function” (Schore,1994, p. 203).

Misattunement therefore precipitates animbalance in the regulation of affect, as it hasin earlier periods. The child’s experience oflow arousal in this period, however, isassociated with decreased tone in the face,neck, and body and is visible as a “motionlessheadhang, ... loss of social smile, [eyeaversion], and the hallmark of shame, blushing(which is known to be absent in earlyinfancy)” (Schore, 1994, p. 204). Schore’sreference to the fact that blushing is absent inearly infancy implies that the PNS is immatureand incapable of this function at a younger age.This state of low arousal is associated withother parasympathetic qualities includingdecreased mobility and interest consistent withconservation-withdrawal.

The state of shame evokes apsychophysiological stress reaction thatactivates the HPA axis and results in elevationsof cortisol. Schore (1994) describes HPA axisactivity as being a parasympathetic function(Schore, 1994, p. 211) associated with theonset of vagal function and further maturation



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of the orbitofrontal cortex. Shame-inducedcortisol deactivates the ventral tegmentaldopamine system that fosters sympatheticgrowth and as a result, influences the growthof the parasympathetic lateral tegmental circuit(Schore, 1994, p. 214). The growth of thisparasympathetic inhibitory system is evidentduring this period as heart rate and bloodpressure begin to decrease (Schore, 1994, p.205).

To summarize, the role of shame isconsidered to be adaptive in an active childwho is at risk of potential harm due to hisincreased mobility and exploratory behavior.Rapid appraisal of his mother’s facial cuesserves a protective function in a child whoseright orbitofrontal cortex has become highlysensitized to interpreting her nonverbalgestures, even at a distance (Schore, 1994, p.205). Indeed, this process facilitates behaviorsthat will endure into adulthood as visualexperiences become internalized. As a resultof these stored visual messages, memories ofthe prohibiting mother recur when the childencounters particular types of events requiringhim to regulate his impulsive behavior. Theseevents might be an encounter with a hot stove,a stranger, or some other form of threat, aswell as novelty. Internalized experiences fromthis period help regulate impulsive behavior bypromoting the capacity to delay responses,which are an important function of theparasympathetic system.

The role of reunion episodes followingmisattunement.

As in earlier periods, reunion episodesare very important for the optimal flexibility ofnervous system regulatory capacity, and themother plays an important role. The goal ofmaternal prohibition behavior is to prevent thechild from getting hurt, and is thus aimed at hisbehavior, not his whole persona. Clarificationthrough nonverbal interaction that it is thebehavior that is being prohibited is a part of thereunion function.

Following a stressful misattunementinteraction, the child “attempts to rebound”and looks up to and reaches for solace from hismother. If the caregiver is sensitive,responsive, and emotionally approachable,

especially if she initiates and reenters intoarousal-inducing affect-regulating mutual gazevisuoaffective (as well as tactile and auditoryaffect modulating) transactions, the dyad ispsychobiologically reattuned, the objectrelations link (attachment bond) isreconnected, the arousal deceleration isinhibited, and shame is metabolized andregulated. These events define what Izard(1991) calls a positive socialization of shame(Schore, 1994, p. 243).

This psychobiological process is fosteredby the reappearance of the toddler’s “familiar”mother, as well as by touch and laughter.These activities inhibit the toddler’s pituitary-adrenal response to stress and reduce cortisollevels (Schore, 1994, p. 243), and can occur inas little as 10 seconds (Schore, 1994, p. 244).The reunion reignites the sympathetic systemand fosters mobilization behavior. Adifference in level of arousal occurs however,as the infant transitions from the SNSdominant state of hyperarousal, to the lowarousal of parasympathetic dominance inducedby shame, into a new state following reunions.This change in arousal proceeds from alertactivity, to frozen inactivity, to a new blendconsisting of alert inactivity, and promotesresiliency of the nervous system and theorganism’s capacity to cope with stress.Resilience is learned and is not geneticallyencoded.

The caregiver’s dual function in arousalreduction and induction facilitates theestablishment of a moderate level of infantarousal, a state known to be associated withfocused attention and positive affect” (Malmo,1959, as cited in Schore, 1994, p. 245). “Theprocess of reexperiencing positive affectfollowing negative experience may teach achild that negativity can be endured andconquered” (Malatesta-Magai 1991, as cited inSchore, 1994, p. 218). “Demos (1991)characterizes infant resilience as the capacityof the child and the parent to transition frompositive to negative back to positive affect” (ascited in Schore, 1994, p. 245).

Effects of optimal and dysregulatedattunement.

The experience of optimal attachment



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bonds leads to the formation of secureattachment, and the internalization ofexpanded positive and minimized negativeaffective experiences. Consistent and effectiveregulation by another results in an adaptableindividual who can flexibly navigate into andout of states of SNS and PNS arousal. Thisfunction fosters the capacity to self-regulate,which continues through life as a result of theincorporation of effective internalized models.

Under the aegis of a caregiver who issensitive and cooperative in [the]reparative process, the infant developsan internal representation of himself aseffective, of his interactions as positiveand reparable, and of the caregiver asreliable... Salient ‘distress-reliefsequences’ initiated by an accessiblemother facilitate a transition in theinfant to a state of controlled arousal,quiet alertness, and responsiveness.This allows the infant to recover fromnegative affect states, ... and permitshim to develop the capacity foranticipation of relief and a sense of hisown efficacy .... [Internalized modelsfrom effective interactive experiencesare] stored as a unitary ‘interactiverepresentation’, allowing for thedevelopmental transition of external tointernal regulation via increasinglevels of internalization .... Suchrepresentations can be accessed in thefuture in order to autoregulate shamestates (Schore, 1994, p. 246-8).

Experiences of a “psychobiologicallydysregulating mother,” on the other hand,result in insecure attachments and animbalance in nervous system regulatorycapacity as well as in the capacity to self-regulate. “Without access to the mother’saffect regulating function, the child remainsstuck fast for long periods of time in aparasympathet ic-dominant s ta te ofconservation-withdrawal” (Schore, 1994, p.247). Humiliation is a particular state thatinduces intensely negative affect in the childand stimulates both sympathetic andparasympathetic arousal. Shame-humiliationis one particular combination that is alwaysassociated with child abuse (Schore, 1994). As

a result of the inability to autoregulate in suchstates, the child experiences helplessness andhopelessness.

In helplessness, the distressed persondepends (unsuccessfully) on theenvironment for relief, and feelspersonally powerless to changematters ... the child who learnshopelessness comes to believe that theself is inadequate, that one’sdeficiencies are to blame for one’spowerlessness, and that there is nohope that others will come to therescue (Powles, 1992, p. 416, as citedin Schore, 1994, p. 247-248).

As a result of frequent or consistentexperiences of this type of state, children growup using behaviors that attempt to utilizeexternal objects to support their incompletecapacity for self-regulation. These attempts,however, are just as unsuccessful as they werein childhood. This type of behavior isconsidered to be the result of insecureattachment in early life.

Attachment and Stress. The role of the attachment bond in

facilitating regulation in response to stress hassignificant implications for the capacity of thedeveloping infant to cope with stressful eventsthroughout his life. As a result of optimalreunion transactions in early life, an infantresponds to future stress exposure with lesscortisol output, and a more rapid return tobaseline (Schore, 1994, p. 243). He is thusexposed to less intense levels and shorterperiods of cortisol than his counterpart withinsecure attachment. Increased facility inresponding quickly and in energy efficientways to stress is in large part due to the long-term effects of handling and contact early inlife, including in the prenatal and earlypostpartum period. These early experiencesinfluence the concentrations of cortisolreceptors, known as glucocorticoid receptors,in the frontal cortex of animals.“Glucocorticoid-sensitive neurons are involvedin terminating the adrenocortical stressresponse (Sapolsky, Krey, & McEwen, 1984,as cited in Schore, 1994, p. 243).

Optimal early experiences also result in



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the increased production of corticotropinreleasing factor (CRF) in response to stress.High CRF levels increase exploratorybehavior, and activate the SNS. Increaseduptake of cortisol inhibits CRF expression, andrepresents the high cortisol parasympatheticstate of low arousal seen during the shame-induced responses of the late practicing period.Cortisol and CRF levels thus play an importantrole in organismic response to stress and bothare regulated by the orbitofrontal region. Infact, the orbitofrontal cortex overrides lowermechanisms of homeostasis regulation in timesof stress (Schore, 1994, p. 225). Thisunconscious process is referred to as a “top-down” mechanism of arousal regulation(Hakomi somatics: trauma training manual,2001). As a result, “the environmentallyattuned prefrontal cortical system … canrapidly uncouple arousal and switch offsympathetic cardiac acceleration and switch onparasympathetic cardiac deceleration. In thisway, this structure acts as a cortical systemwhich regulates autonomic responses toaffective [emotionally related] cues” (Schore,1994, p. 225).

Summary: III.The late practicing period occurs in an

environment of increased cortisol related to amaturing parasympathetic system, and shame-induced experiences of stress further increasecortisol levels. High cortisol levels and theparasympathetic state of shame inactivate thepreviously dominant SNS and foster growth ofthe lateral tegmental circuit down from thematuring orbitofrontal cortex. In ongoingpursuit of clarification concerning the methodsby which discharge occurs, one wonders ifthere may be a difference between“inactivation” of SNS activity by PNS onset,and “truncation” of SNS activity by the samePNS state. This remains to be seen.

The connections between the orbitofrontaland subcortical ANS processes allowbidirectional communication to occur. Theseconnections enable the CNS to regulate andoverride ANS responses, particularly in theevent of stress. In optimal attachmentexperiences, misattunement from the motherfosters brief experiences of PNS dominance

associated with the withdrawal and immobilityresponse, and reunion transactions with themother rapidly transform them into a new stateof alert inactivity.

Prolonged stressful states are associatedwith high levels of cortisol. Elevated cortisolis associated with fear, helplessness anddespair, depression, and decreased awarenessof sensory input. While brief experiences ofthis state promote PNS development,prolonged or recurrent intense exposure fosterpassive coping and avoidance strategiesassociated with unconscious patterned ANSresponses for coping with stress.

IV. The Role of the Father and theDeveloping Verbal Left Hemisphere

During the late practicing period, thechild has an increase in oppositional behaviorand progressively goes to her father. Whileshe still goes to her mother during periods ofstress, this behavior marks the end of theperiod of maternal imprinting and thetransition to a developmental period thatculminates when the mother and childsuccessfully renegotiate their relationshipthrough “rapprochement”. The period ofopposition begins at 15 to 18 months of age,and is associated with an increased interest inthe father as a source of arousal induction andreduction.

The father’s role, which is notcharacterized by Schore (1994) to the degree towhich the mother’s role was described inpreceding phases, serves an important functionin facilitating safety. The “early experience ofbeing protected by the father and caringlyloved by him becomes internalized as alifelong sense of safety” (Blos, 1984, as citedin Schore, 1994, p. 236). This period fostersgrowth of the second area of the prefrontalcortex, the dorsolateral cortex, which is the lastarea of the brain to functionally mature.

The dorsolateral cortex develops thecapacity to regulate the dominant verbal lefthemisphere and is non limbic. This prefrontalcortex is thus not involved with emotionallimbic systems other than through itsconnection to the earlier maturing prefrontalcortex in the right hemisphere. The primaryfunctions of the dorsolateral cortex include



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conscious awareness, verbal memory, andcommunication. Dominance of this lefthemisphere over the right begins at 3 to 4 yearsof age and maturation continues until puberty.This stage of physiological brain growthrepresents a shift from the maternal-experience-dependent maturation of theorbitofrontal part of the prefrontal cortex to apaternal-experience-dependent maturation ofthe dorsolateral cortex (Schore, 1994).

The dorsolateral cortex forms circuits ofconnection with subcortical structurescompletely different from previous rightcortical-subcortical connections. Thedorsolateral cortex connects to thehippocampus, an important center for memory,as well as the locus coeruleus, which providesmost of the norepinephrine stimulation to thecentral nervous system, both in general and intimes of stress. A dopamine circuit thatoperates within this system promotes motorreadiness in striated, voluntary muscles, whichare involved with high levels of anxiety. Thisis in comparison to the right-sided ANS-influenced dopamine circuit (ventraltegmental) that fosters sympathetic motormovement in involuntary muscles and organs.The developing dorsolateral dopamine circuittherefore differs from the right-sided system ofdopaminergic SNS control and norepinephrinemediated PNS regulation. As such, the stressresponse of the two systems differs.

The dorsolateral cortex is associated withanxiety stress states related to negative affectsuch as fear, while the orbitofrontal cortexmanages positive stress states associated witharousal during attachment interactions.Interestingly, in a reference to the polyvagalsystem, Schore (1994) states that only the rightside connects to and regulates the DVC .

Individuals with problems of theorbitofrontal cortex show lack of inhibition,explosiveness, and high motor activity, whichis similar to the behavior of the practicingtoddler. Those with dorsolateral lesions, onthe other hand, demonstrate little overtemotion, are depressed, and show reducedspontaneity of behavior (Schore, 1994, p. 234).These developmental differences may alsoeventually present themselves as diseases withrelated characteristics, such as physiological

states of high arousal (high blood pressure)versus low arousal (depression, chronicfatigue).

The paternal-experience-dependentmaturation of the dorsolateral cortex

Repeated or intense exposure tooverwhelming experiences that cannot beautoregulated, such as occur in misattunementwithout the support of helpful reuniontransactions, results in pathology. Thepathology comes from the internalization ofrepeated experiences of misattuneddysregulated transactions. Early enduringunmodulated painful emotional experiencesinterfere with the organization of the rightcortical system that can regulate and therebytolerate pain .... These models are imprintedwith painful and disorganizing negative affectsthat cannot be intra- or interpersonallyregulated, and are therefore stored in‘unconscious memory’ (Schore, 1994, p 446-447).

These memories interfere with the abilityof the right hemisphere to effectively interactwith the maturing left hemisphere, whichconsciously avoids the experience ofoverwhelming pain through mechanisms oftenreferred to as “repression” or dissociation.

The ‘ubiquitous and unrelieved’experience of of [sic] shame, “one ofthe least tolerable affects for humans’(Malatesta-Magai, 1991), thereforebecomes associated with anexpectation of a painful disorganizingstate which cannot be interpersonallynor intrapersonally regulated, andtherefore is consciously avoided or‘bypassed’ (Schore, 1994, p. 248).

Overwhelming unconscious memories arethe cause of dissociation between left and righthemispheres and are one, if not the onlyprimary source of physiological as well aspsychological pathology. These repressedunmetabolized experiences stored inunconscious memory remain unprocessed andshow up in other forms, often expressed asnonverbal unconscious symptoms. Themanner in which unconscious repressedmemories influence symptomatology areexplored in more detail in the section on



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trauma (see separate article on trauma).Relationship between Parts of the ANS

The ability to transition between statesof autonomic function is important to theadaptive capacity of the organism.

The ability to cycle back and forthbetween these organismic modes [ofparasympathetic and sympatheticstates] in response to environmentalcondit ions increases survivalefficiency. … Chisolm (1990) definesadaptabili ty in the face ofsocioecological stressors as: ‘thecapacity of an organism to make asuccessful response to perturbations inits physical and social environmentssuch that the next time it encountersthat same perturbation, or onesufficiently similar, it can respondwith less cost’ (p. 240, as cited inSchore, 1994, p. 366).

Schore refers to three different modes ofautonomic control that affect this capacity toadapt. These modes include:

a coupled reciprocal mode, a couplednonreciprocal mode, and an uncoupledmode. In the first, increases in activityin one ANS division are associatedwith a decrease in the other; in thesecond, concurrent increases(coactivation) or concurrent decreases(coinhibition) occur in bothcomponents; in the third, responses inone division occur in the absence ofchanges in the other (Berntson,Cacioppo, and Quigley, 1991, as citedin Schore, 1994, p. 323).

These modes are also referred to by anotherresearch group, who describe them as“reciprocal inhibition, mutual antagonism, andunilateral activity” (Grossman, Stemmler, andMeinhardt, 1990, as cited in Schore, 1994, p.324).

Schore’s (1994) analysis of theresearch regarding these modes has lead him toconclude that in the immature organism thetwo branches of the ANS are initiallyuncoupled (unilateral activity), and as a resultof development in the prenatal and postnatalenvironment, gradually become reciprocally



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coupled (reciprocal inhibition). The lattermode provides a wider range of capacity torespond to the environment.

Reciprocal modes can yield largedirectionally stable shifts, and aresuited for well-defined adaptiveadjustments to survival challenges.…One adaptive feature of reciprocalmodes of control is a shift in therelative dominance of the two ANSdivisions (Berntson et al., 1991, p.473, as cited in Schore, 1994, p. 324).

The shift mentioned above refers to the gradualincrease in parasympathetic dominance thatoccurs during development. Thisparasympathetic state is associated with thepreviously mentioned arousal level of alertinactivity or the conservation-withdrawalmode that enables the organism to respond tostress with “as little involvement, cost or riskas possible” (Schmale and Engel, 1975, ascited in Schore, 1994). This appears to relateto Schore’s description of the importance ofthe phase of misattunement in the latepracticing period, which stimulates thedevelopment of impulse control and theattainment of moderate, rather than high orlow, states of arousal.

The facility with which an organismtransitions between ANS states is learned, andis stored as an internal representation.

The development of more complexforms of self-organization in the firsttwo years is mediated by theappearance of internal representationsthat shape spontaneous patterns ofenergy dissipation (Schwalbe, 1991).These stored images come toautomodulate processes of energy flowthat support survival in a particularenvironment …. This resilienceinvolves an ability to tolerate signalsof negative affect in environmentalcontexts where threat and lack ofsocial success will interfere with theattainment of biosocial goals (Schore,1994, p. 367).

The capacity to transition between ANS statesis therefore strongly influenced by transactionsthat occur between caregiver and infant.

Practicing interactions permanentlyinfluence the determination of a setpoint that reflects the autonomicbalance between the sympathetic andparasympathetic components of theANS, and the reciprocal andnonreciprocal activities of the twolimbic circuits. This homeostaticmechanism enables the child to moreefficiently self-regulate affect,especially negative affect (Schore,1994, p. 368-9).

As an organism develops, the ANSresponse to a novel threat progresses from anuncoupled reaction (in which the responsepresumably consists of either sympathetic orparasympathetic activity), to one ofnonreciprocal coactivation in which bothsympathetic and parasympathetic divisions ofthe ANS increase (Berntson et al., 1991, ascited in Schore). With optimal development,the organism responds to stress with the mostadaptive reciprocally coupled ANS response,in which one branch decreases when the otherincreases. The reciprocally coupled responsestyle consists of a parasympatheticallydominant response and is the most energy-efficient mode of interacting with theenvironment (Schmale and Engel, 1972, ascited in Schore, 1994, p. 367). Such aresponse is consistent with Porges’ (2001)description of the functions of the VVC andthe social engagement system. States in whichboth SNS and PNS are either high or low maybe associated, in the long-term, with certaintypes of diseases. Some forms of chronicfatigue, for example, appear to include anunderlying state of high metabolism(associated with hunger, constipation, the needto be active and to “do”) with a simultaneousinhibition by a more dominant PNS state(overall fatigue, being cold and depressed, andlow blood pressure). Such states appearconsistent with the freeze response referred toby Levine (Levine, 1997), in which the state ofinhibition is often the most visible.

ConclusionThe development of the maturing nervous

system is intimately intertwined with the socialemotional environment during the attachment



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period. The role of both parents is importantto the optimal development of this system,which influences psychophysiologicalprocesses necessary for emotional and bodilyself-regulation. These early experiences alsoinfluence the capacity to cope with stress andto have satisfying relationships throughout life.

The interconnections and roles of thevarious components of the nervous system arecomplex, and patterns of autonomic andcentral regulation that arise are unique to eachindividual as a result of his or her set of lifeexperiences. Decreased flexibility andadaptability in transitioning between states ofANS dominance is the result of internalizedrepresentations that are formed during theprenatal time frame and the attachment period(Schore, 1994). Imbalances in ANS regulationthat develop from nonoptimal environmentscan consist of inappropriate sympathetic orparasympathetic dominance, a combination ofhigh levels of both (nonreciprocalcoactivation), or the independent action of twouncoupled systems.

With sufficient or intense enoughexposure to unregulated emotionallyoverwhelming stimuli in early life, dominanceof one or both systems can become thepreferred, internalized, patterned response tofuture stimuli. These responses arise fromperceptions that are formed as a result of thesum of experience in life, particularly duringthe attachment period.

Individuals with secure attachment tend toperceive the world as a safe place withadequate support while those with insecureattachments perceive the world as unsafe andlacking in the capacity to provide support andsuccessful regulation.

Imbalances in nervous system regulationaffect metabolic, immune, and endocrinehomeostasis as well as psychologicalprocesses, and are associated with thedevelopment of symptomatology and disease.“Early unregulated shame experiences [play acentral role] in the etiology of all primitivepsychopathologies and psychosomaticdiseases” (Schore, 1994, p. 248). The articleon trauma will elucidate the physiology of thisprocess greater more detail.



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References

Brazelton, T. B., & Cramer, B. G. (1990). Theearliest relationship: Parents, infants,and the drama of early attachment.Cambridge, MA: Perseus.

Bruer, J. T. (1998). The brain and childdevelopment: time for some criticalthinking. Public Health Rep, 113(5),388-397.

Caldwell, C. (2001). Addiction as somaticdissociation. In M. Heller & P. Lang(Eds.), Flesh of the soul: The body wework with. Berne, Switzerland.

Hakomi somatics: trauma training manual.(2001). (unpublished manual availablefrom Hakomi Somatics Institute, P. O.Box 19438, Boulder, CO 80308www.hakomisomatics.com).

Klaus, M. H., & Kennell, J. H. (1976).Maternal-infant bonding: the impactof early separation and loss on familydevelopment. St. Louis: Mosby.

Kotulak, R. (1998). Inside the brain:revolutionary discoveries of how themind works. Prev Med, 27, 246-247.

Levine, P. (1997). Waking the tiger. Berkeley:North Atlantic Books.

National Research Council and Institute ofMedicine. (2000). From neurons toneighborhoods: the science of earlychildhood development. Committee onintegrating the science of earlychildhood development. Board onchildren, youth, and families,Commission on behavioral and socialsciences and education. Washington,D.C.: National Academy Press.

NRCIM (Ed.). (2000). From neurons toneighborhoods: The science of earlychildhood development. Committee onintegrating the science of earlychildhood development. Board onchildren, youth, and families,Commission on behavioral and socialsciences and education. Washington,D.C.: National Academy Press.

Schore, A. N. (1994). Affect regulation and theorigin of the self: the neurobiology ofemotional development. Hillsdale, NJ:Lawrence Erlbaum.

Schore, A. N. (2001a). The effects of earlyrelational trauma on right braindevelopment, affect regulation, andinfant mental health. Infant MentHealth J, 22(1-2), 201-269.

Schore, A. N. (2001b). The effects of secureattachment relationship on right braindevelopment, affect regulation, andinfant mental health. Infant MentHealth J, 22, 7-66.

Siegel, D. (1999). The developing mind. NewYork:NY: Guilford.

Stern, D. (2000). The interpersonal world ofthe infant: A view from psychoanalysisand developmental psychology: BasicBooks.

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Abstract Environmental factors affecting the nervous system and health