Schore Pediatrics in Review (2011) Attachment & Emotion

BACK TOBASICS

A review of the scientificfoundations of current clinicalpractice

Author Disclosure

Dr Schore did not disclose any

financial relationships relevant to

this article.

Attachment, AffectRegulation, and theDeveloping Right Brain:Linking DevelopmentalNeuroscience to PediatricsAllan N. Schore, PhD*

Editor’s Note: This article is a de-parture from our usual review in thatit discusses new frontiers in the corre-lation of brain, mind, and emotions indeveloping children as well as areas ofcollaboration between pediatrics andsister disciplines. Dr Schore hasadapted a substantial amount of tech-nical information to the viewpoint ofthe pediatrician. At the same time,many readers will encounter perspec-tives and language that seem unfa-miliar. We urge clinicians to invest theeffort needed for a careful reading toappreciate exciting new ways to look atdevelopment and emotional copingmechanisms. Readers desiring an ab-breviated version will find it in theprint version. —LFN

IntroductionWe are in the midst of an excitingperiod for clinical practitioners, onein which the connections betweenthe basic and applied sciences are be-ing more tightly forged. A powerfulengine driving this progression ofknowledge is the recent remarkableadvance in biotechnology, especiallyimaging technologies. Noninvasivestudies of organ systems have in-creased substantially our understand-

ing of the biologic processes that un-derlie various diseases of the body. Atthe same time, neuroimaging re-search of both psychological func-tions and psychiatric conditions hasgenerated more complex models ofnormal and abnormal operations ofthe human mind. Another catalystof the continuing dramatic increasein information is the rapid expansionof collaborative interdisciplinary re-search. Of particular relevance to pe-diatrics, this same time period hasseen an explosion in infant researchthat integrates neurobiological stud-ies of brain development and psycho-logical studies of emotional, social,and cognitive development. De-velopmental studies, which span aspectrum of scientific and medicaldisciplines, now are serving as a con-vergence point for complex modelsof structure and function, brain,mind, and body.

A paradigm shift is occurring inthe basic sciences that underlie pedi-atrics. Research in developmental bi-ology and physiology now stronglysupports a model of the “develop-mental origins of health and disease.”(1) Although the role of early ex-pressed genetic factors is an essentialfocus of current study, it has becomeclear that genes do not specify behav-ior absolutely; prenatal and postnatalenvironmental factors play criticalroles in these developmental origins.The social environment, particularlythe one created together by themother and infant, directly affectsgene-environment interactions and,thereby, has long-enduring effects.

*Department of Psychiatry and BiobehavioralSciences, University of California at Los AngelesDavid Geffen School of Medicine, Los Angeles, Calif.

Dr Schore is a member of the Commission onChildren at Risk, Report on Children and CivilSociety, “Hardwired to Connect,” DartmouthMedical School, the YMCA of the USA, and theInstitute of American Values.

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(2) The newer interdisciplinary mod-els, therefore, detail the mechanismsby which “mother nature meetsmother nurture.” (3) Compliment-ing this conception of the nature-nurture problem, studies in neuro-science indicate that developmentrepresents an experiential shaping ofgenetic potential and that early expe-riences with the social environmentare critical to the maturation of braintissue. Thus, nature’s potential canbe realized only as it is facilitated bynurture. (4)

In parallel advances in develop-mental psychology and child psychi-atry, attachment theory, initially pro-posed more than 35 years ago byJohn Bowlby (5) as a conception ofthe mother-infant relationship, hasbecome the dominant model of hu-man social-emotional developmentavailable to researchers and cliniciansover a broad array of disciplines. Inhis attempt to integrate psychologyand psychiatry with behavioral biol-ogy, Bowlby speculated that the at-tachment system, an evolutionarymechanism common to both hu-mans and animals, ultimately wouldbe located in specific areas of thebrain. Updated models of attach-ment theory that emphasize bothemotional and social functions andneurobiological structures now areinterfacing with developmental neu-roscience to generate a large body ofinterdisciplinary studies.

This recent information on thedevelopmental origins of health anddisease can be translated directly intoclinical practice. It has both ex-panded the amount of factual knowl-edge and altered the theoretical con-structs that model the diagnoses andtreatments of a variety of psycholog-ical and physical disorders of child-hood. These advances are, in turn,directly relevant to pediatricians’ in-terest in the normal and abnormalfunctions of the developing child’s

mind and body. The commonground of the expanding body ofknowledge in the developmental sci-ences, therefore, can strengthen theties of pediatrics to the allied fieldsthat border it: developmental neu-rology, child psychiatry, and devel-opmental psychology.

This ongoing paradigm shift inthe basic and applied sciences is ex-pressed in three converging themes.The first arises from the wealth ofneurobiological data that becameavailable in the last decade, the “de-cade of the brain.” These findingsstrongly support the idea that themost powerful conception of devel-opment may come from a deeper un-derstanding of the brain’s own self-organizing operations. Currently,there is an intense focus on the hu-man brain growth spurt, which be-gins in the last trimester of pregnancyand continues to 18 to 24 months ofage. Myelinization of the brain is sorapid and extensive at this time thatthe brain takes on an “adultlike” ap-pearance by the end of the first post-natal year. (6) Neuroscientists areconcluding that the acceleratedgrowth of brain structure during crit-ical periods of infancy is dependenton experience and influenced by “so-cial forces.” Neuropsychiatrists referto “the social construction of the hu-man brain” and posit that the cellulararchitecture of the cerebral cortex issculpted by input from the social en-vironment embedded in the early at-tachment relationships. These datasuggest that “the self-organization ofthe developing brain occurs in thecontext of a relationship with an-other self, another brain.” (7)

Furthermore, we now are awarethat “the brain” actually is a systemof two brains, each of which has verydifferent structural and functionalproperties. Of particular interest tothe developmental sciences is theearly maturing right brain, which un-

dergoes a growth spurt in the first 2years, before the verbal left, and isdominant in the first 3 years afterbirth. (8) This growth is not encodedtotally by the genome, but it isshaped indelibly by the emotionalcommunications within attachmenttransactions. Because the right hemi-sphere is dominant for the emotionaland corporeal self, (9) the socialexperience-dependent maturation ofthe right brain in human infancy isequated with the early developmentof the self. (10) The early develop-ment of the brain-mind-body, theorigin of the self, therefore, is a re-flection of the development of theright brain and its unique functions.

The second theme emerges fromtransformations within the psychiat-ric and psychological sciences. Allsubdisciplines within psychology,from developmental through abnor-mal, are shifting their focus fromcognition to emotion. Research sug-gests that the attainment of an at-tachment bond of emotional com-munication and the maturation ofaffect represent the key events ininfancy more so than does the devel-opment of complex cognitions.Models have moved from Piagetiantheories of cognitive development topsychobiological models of social-emotional development. Clinicalpsychology and psychiatry are mov-ing from cognition to emotion as thecentral force in psychopathology andpsychotherapy. This emphasis onemotion also is reflected in: 1) theemergence of affective neuroscienceand its focus on the specializations ofthe right hemisphere for processingaffective states, and 2) psychiatry’scurrent interest in the emotion-processing limbic system, the brainsystem that derives subjective infor-mation in terms of emotional feelingsthat guide behavior and functions toallow the individual to adapt to a

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rapidly changing environment andorganize new learning.

The third theme revolves aroundthe critical concept of self-regulation.The process of development itself isbelieved to represent a progressionof stages in which adaptive self-regulatory structures and functionsenable new interactions between theindividual and the social environ-ment. It now is established thatemotions are the highest order directexpressions of bioregulation in com-plex organisms, that the maturationof the neural mechanisms involvedin self-regulation is experience-dependent, and that these critical af-fective experiences are embedded inthe attachment relationship.

In other words, attachment rela-tionships are essential because theyfacilitate the development of thebrain’s self-regulatory mechanism.Studies reveal that these essentialself-regulatory structures are locatedin the right (and not left) brain.(11)(12) Consensus now indicatesthat attachment can be defined as thedyadic regulation of emotion, thatthe attainment of the self-regulationof affect is a major developmentalachievement, and that normal devel-opment represents the enhancementof self-regulation.

I now use the perspective of regu-lation theory (10)(11)(12) to discussand interpret recent studies on at-tachment, affect regulation, and de-velopment of the right brain. Theseadvances in understanding the neu-robiology of attachment are beingincorporated into clinical models ofthe development of childhood men-tal health and mental illness, areasthat are directly relevant to pediat-rics. The mission statement of theAmerican Academy of Pediatricsstates its commitment to “the attain-ment of optimal physical, mental,and social health for all infants, chil-dren, adolescents, and young

adults.” (http://www.cispimmunize.org/mission.html)

For a more extensive discussion ofregulation theory and an index of thereferences of studies cited here, thereader is referred to two books bySchore. (10)(11)

Interactive Affect Regulation:A Fundamental Mechanismof Attachment DynamicsThe primary goals for the infant dur-ing the first postnatal year are thecreation of an attachment bond ofemotional communication with theprimary caregiver and the develop-ment of self-regulation. From birthonward, infants use their expandingcoping capacities to interact with thesocial environment. In the earliestproto-attachment experiences, in-fants use their maturing motor anddeveloping sensory capacities, espe-cially smell, taste, and touch, to inter-act with the social environment.(13)(14) At around 8 weeks of age,there is a dramatic progression of so-cial and emotional capacities. Withinepisodes of mutual gaze, the care-taker (usually the mother) and infantengage in nonconscious and sponta-neous facial, vocal, and gestural com-munications. Such highly arousing,affect-laden, face-to-face interactionsallow the infant to be exposed tohigh levels of social and cognitiveinformation.

In face-to-face emotional transac-tions, the mother makes herself con-tingent, easily predictable, and ma-nipulatable by the infant. To regulatethe high positive arousal, the dyadsynchronizes the intensity of their af-fective behavior within split seconds.These episodes of “affect synchrony”occur in the first expression of socialplay and generate increasing levels ofjoy and excitement. In these interac-tions, both partners match states andsimultaneously adjust their social at-tention, stimulation, and accelerat-

ing arousal to each other’s responses.According to Lester, Hoffman, andBrazelton, “synchrony develops as aconsequence of each partner’s learn-ing the rhythmic structure of theother and modifying his or her be-havior to fit that structure.” (15) Insuch moments, the empathic caregiv-er’s sensory stimulation coincideswith the infant’s endogenousrhythms, allowing the mother to ap-praise the nonverbal expressions ofher infant’s internal arousal and psy-chobiological states, regulate them,and communicate them back to theinfant.

In this process of “contingent re-sponsivity,” the tempo of their en-gagement, disengagement, and reen-gagement is coordinated. The morethe empathic mother tunes her activ-ity level to the infant during periodsof social engagement, the more sheallows him or her to recover quietlyin periods of disengagement. Themore she attends to the child’s reini-tiating cues for re-engagement, themore synchronized becomes their in-teraction. Thus, the caregiver facili-tates the infant’s information pro-cessing by adjusting the mode,amount, variability, and timing ofthe onset and offset of stimulationto the infant’s unique, temperamen-tally determined integrative capaci-ties. These interactively regulated,synchronized interactions promotethe infant’s regulatory capacities andare fundamental to his or her healthyaffective development.

In such interactions the mothermust be attuned not so much to thechild’s overt behavior as to the reflec-tions of the rhythms of his or herinternal state, enabling the dyad tocreate “mutual regulatory systems ofarousal.” To regulate the infant’sarousal, she must be able to regulateher own arousal state. The capacity ofthe infant to experience increasinglevels of positive arousal states is am-

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plified and externally regulated bythe primary caregiver and dependson her capacity to engage in an inter-active communication of emotionsthat generates feelings in herself andher child. Maternal sensitivity, there-fore, acts as an external organizer ofthe infant’s biobehavioral regulation.

Research also shows frequent mo-ments of misattunement in the dyador ruptures of the attachment bond.In early development, an adult pro-vides much of the modulation of in-fant states, especially after a state dis-ruption or a transition betweenstates, and this intervention allowsfor the development of self-regulation. The key to this beneficialinteraction is the caregiver’s capacityto monitor and regulate her own (es-pecially negative) affect. In this es-sential regulatory pattern of “ruptureand repair,” the attuned “good-enough” caregiver who induces astress response in her infant througha misattunement remedies the situa-tion and helps her infant regulate hisor her negative affect via her partici-pation in “interactive repair.” Theprocess of re-experiencing positiveaffect following negative experienceallows the child to learn that negativeaffect can be tolerated and that rela-tional stress can be regulated. Infantresilience emerges from an interac-tive context in which the child andparent together make the transitionfrom positive to negative and back topositive affect. The adaptive regula-tory capacity of resilience in the faceof stress is an ultimate indicator ofsecure attachment and optimal men-tal health.

Affect synchrony that createsstates of positive arousal and interac-tive repair that modulates states ofnegative arousal are the fundamentalbuilding blocks of attachment and itsassociated emotions. These arousal-regulating transactions, which con-tinue throughout the first year,

underlie the formation of an attach-ment bond of emotion regulationbetween the infant and primary care-giver. Indeed, psychobiological at-tunement and the interactive mutualentrainment of physiologic rhythmsare fundamental processes that medi-ate attachment. Thus, throughoutthe life span, attachment is a primarymechanism for the regulation of bio-logic synchronicity within and be-tween organisms.

These data clearly suggest that af-fect regulation is not just the reduc-tion of affective intensity or thedampening of negative emotion. Af-fect regulation involves an intensifi-cation of positive emotion, a condi-tion necessary for more complex self-organization. The attuned mother ofthe securely attached child not onlyminimizes the infant’s negative statesthrough comforting transactions butalso maximizes his positive affectivestates in interactive play. Regulatedaffective interactions with a familiar,predictable primary caregiver create asense of safety and a curiosity thatfuels the child’s exploration of novelsocioemotional and physical environ-ments. This ability is a marker ofadaptive infant mental health.

Interpersonal Neurobiology ofRight Brain-to-Right BrainAttachment CommunicationsLearning how to communicate emo-tional states is an essential develop-mental process. Because these com-munications are nonverbal andsubjective, it was believed that theirunderlying mechanisms were un-available to experimental analysis.However, studies in developmentalpsychobiology have offered impor-tant contributions to this problem,revealing that during optimal mo-ments of bodily based affective com-munications, the adult’s and infant’sindividual homeostatic systems arelinked in a superordinate organiza-

tion that allows for mutual regula-tion of vital endocrine, autonomic,and central nervous systems of bothmother and infant by elements oftheir interaction with each other.

Basic developmental neurobio-logical research findings are conso-nant with the psychological modelsof early mother-infant communica-tion described in the preceding sec-tion. Coordinated visual eye-to-eyemessages, auditory vocalizations, andtactile and body gestures serve aschannels of communicative signalsthat induce instant emotional effects:the positive feelings of excitementand pleasure build within the inter-subjective field created by the dyad.According to Trevarthen, (16) theintrinsic regulators of a child’s braingrowth are adapted specifically forcoupling, by emotional communica-tion, to the regulators of adult brains.

Attachment communications,therefore, are “built into the ner-vous system,” inducing substantialchanges in the developing brain.Which parts of the brain are affectedby the interactive regulation embed-ded within various types of visual,auditory, and tactile communica-tions? Keeping in mind that the brainactually represents two unique hemi-spheric processing systems, a sub-stantial body of research indicatesthat the right hemisphere begins acritical period of maturation beforethe left. This hemisphere is more ad-vanced than the left in surface fea-tures from about the 25th gestationalweek until the beginning of the sec-ond postnatal year, when the lefthemisphere undergoes a growthspurt. (17) Neuroimaging studiesdemonstrate that brain mass in-creases rapidly during the first 2 yearsafter birth, normal adult appearanceis seen at 2 years, and all major fibertracts can be identified by age 3 years.Infants younger than 2 years of age

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show higher right than left hemi-spheric volumes. (18)

Several studies support the princi-ple that “the emotional experience ofthe infant develops through thesounds, images, and pictures thatconstitute much of an infant’s earlylearning experience, and are dispro-portionately stored or processed inthe right hemisphere during the for-mative stages of brain ontogeny.”(19) The neurobiology of attach-ment, therefore, is an interpersonalneurobiology of right brain-to-rightbrain communications. Although thelater developing left hemisphere me-diates most language functions, theearly developing right hemisphere ismore important to the broader as-pects of communication through allstages of life.

In support of this right brain-to-right brain communication model,research indicates that at about8 weeks (onset of intense face-to-facecommunications), a critical period isinitiated in the occipital cortex dur-ing which synaptic connections aremodified by visual experience. (20)Infants as young as 2 months of ageshow right hemispheric activation onpositive emission tomography whenexposed to a woman’s face, and par-ticular areas of the right hemisphereare timed to be in a plastic and recep-tive state at the very time when sen-sory information that emanates fromfaces is being attended to most in-tensely by the infant. (21) Duringsynchronized face-to-face transac-tions, patterns of information ema-nating from the caregiver’s face, es-pecially of low visual and auditoryfrequencies, are processed by the in-fant’s right hemisphere. Studiesdemonstrate that the development ofthe capacity to process informationfrom faces efficiently requires visualinput to the right (and not left)hemisphere during infancy. (22)

Over the first year, emotional

communications embedded withinmutual gazing are etched into devel-oping right lateralized networks thatare specialized for assessing familiarfaces and gaze direction and for pro-cessing visual and auditory emotionalsignals. The right cerebral cortex isdominant for the infant’s processingof individual faces, recognition ofmaternal facial expressions, and re-sponse to the mother’s voice. Simi-larly, the mother’s mature righthemisphere is faster than the left inappraising emotional facial expres-sions; responding to the positive as-pects of facial expressions, visualstimuli, touch, and smell; and as-sessing visual or auditory emotionalsignals.

Other studies reveal that the re-sponse to an infant’s cry, a funda-mental attachment behavior, is ac-companied an activation of themother’s right brain. These data sup-port the idea that engrams related toemotional voices are imprinted morestrongly on the infant’s early matur-ing, more active right hemisphere.(23) With respect to tactile commu-nications, most women tend to cra-dle infants on the left side of thebody. This left-cradling tendency fa-cilitates the flow of maternal affectivesignals into the infant’s left ear andeye and processing in the developingright hemisphere, and the ensuinginfant’s auditory and visual commu-nications are fed back to the center ofemotional decoding in the mother’sright hemisphere. (24) Researchersconclude that this left-cradling con-text allows for maximal somatoaffec-tive feedback within the dyad andthat “the role of the right hemisphereis crucial in relation to the most pre-cious needs of mothers and infants.”(25)

From a neurobiological perspec-tive, “When the child is held andhugged, brain networks are activatedand strengthened and firing spreads

to associated networks; when thechild is sung to, still other networksare strengthened to receive soundsand interpret them as song. The re-peated appearance of the motherprovides a fixation object as in im-printing.” (26) The cortical and sub-cortical systems of the infant’s rightbrain become tuned to dynamic self-organization upon perceiving certainpatterns of exteroceptive social infor-mation, namely, the visual, auditory,and tactile stimuli emanating fromthe smiling, joyful, soothing, andcalming face as well as the expressivebody of a loving mother.

These imprinting experiences are“affectively burnt in” (27) develop-ing limbic circuits in the infant’s rightbrain, which are known to undergoextensive myelination in the first 18postnatal months. Thus, at a funda-mental level, the mother functions asa regulator of the infant’s socioemo-tional environment, and her regula-tory interactions play a critical roleduring the establishment and main-tenance of developing emotion-processing limbic circuits. The spon-taneous emotional communicationthat occurs within the attachment re-lationship has been described as “aconversation between limbic sys-tems.” Because the early maturingright hemisphere, which is deeplyconnected into the limbic system, isin a growth spurt at this time, attach-ment experiences specifically affectdeveloping limbic and cortical areasof the right brain networks that arecritical to self-regulation.

This research indicates that themother functions in the short term asa regulator of the child’s homeostaticalterations and in the long term influ-ences the child’s capacity to copeadaptively with the social-emotionalenvironment. (28) Although themother initially provides an externalregulating mechanism for the in-fant’s immature neurobiological pro-

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cesses, by the end of the first postna-tal year, the infant becomes self-regulating through the maturation ofinternal regulatory mechanisms en-trained to the mother’s stimuli. Cur-rent psychobiological models refer torepresentations of the infant’s affec-tive dialogue with the mother, whichcan be accessed to regulate its affec-tive state. Studies are detailing howeven subtle affect-regulating transac-tions alter activity levels permanentlyin the child’s maturing brain. Duringthe last 10 years, many studies havedocumented the enduring impact ofmaternal visual, vocal, and tactileemotional stimuli on the infant’sbrain development and on resultingemotional, social, cognitive, and reg-ulatory capacities in later life. (11)(A detailed discussion of the relevantanatomy and physiology of the brainis presented in the appendix to thisarticle.)

Secure Attachment, OptimalRight Brain Maturation, andthe PsychoneurobiologicalOrigins of Mental HealthIn optimal interpersonal environ-ments, coregulated emotional com-munications between the securely at-tached infant and the primaryattachment object facilitate the self-organization and increased complex-ity of the infant’s right brain. Follow-ing the child’s attachment to themother in the first year, the childforms another attachment in the sec-ond year to the father, allowing thechild to have affect-attuning andarousal-regulating experiences withtwo different types of caregivers. As aresult of this interaction with care-givers, the infant forms internalworking models of attachment thatare stored in right-lateralized non-verbal implicit-procedural memory.Security of attachment relates to aphysiologic coding of an expectationthat during times of stress, homeo-

static disruptions will be set right.These interactive representations en-code strategies of affect regulationand contain coping mechanisms formaintaining basic regulation andpositive affect in the face of environ-mental challenge. The infant’s abilityto develop more complex self-regulatory coping capacities, to reg-ulate stressful alterations of psycho-biological state either interactively orautonomously, emerges out of its ex-periences with the social environ-ment.

In all later interpersonal function-ing, this right hemispheric represen-tation of a working model of theattachment relationship, acting atlevels beneath conscious awareness,is accessed to appraise, interpret, andregulate socioemotional informationand guide future action in both fa-miliar and novel interpersonal envi-ronments. For the rest of the lifespan, the right hemisphere that hasbeen imprinted and organized byearly relational experiences is domi-nant for the nonconscious reception,expression, communication, and reg-ulation of emotion, essential func-tions for creating and maintainingsocial relationships, especially inti-mate ones. (29)(30)(31)(32) Studiessuggest that attachment psychobiol-ogy and right brain neuropsychologyrepresent the substrate of three othercapacities that are critical to humaninteractions: trust, empathy, andmoral development. (33)(34)(35)

Indeed, the right brain is domi-nant for the regulation of funda-mental physiologic, endocrinologic,immunologic, and cardiovascularfunctions, thereby controlling vitalfunctions that support survival andenable the organism to cope activelyand passively with stress. A growingbody of data underscores a strongassociation between alterations inmaternal-infant interactions, earlyprogramming of the hypothalamic-

pituitary-adrenal axis, pre- and post-natal critical periods of brain devel-opment, and adult health and disease.(36) This work is paralleled by studieslinking attachment, stress, and child-hood attachment (37)(38) with adultcortisol and cardiovascular function(39) and research showing that theright hemisphere plays a unique rolefor pain sensitivity and negative affect.(40) Assets or limitations of rightbrain survival functions, thus, affectnot just “psychological” but also es-sential “psychobiological” capacitiesof coping with both emotional dis-turbance and physical disease. Theseregulatory capacities, significantly in-fluenced by optimal attachment ex-periences, are critical indices of adap-tive physical and mental health.

In addition to self-regulation, theright hemisphere is specialized forgenerating self-awareness and self-recognition and for the processingof “self-related material.” (41)(42)Devinsky (9) posits an evolutionaryrole of the right hemisphere in thefollowing adaptive functions: main-taining a coherent, continuous, andunified sense of self; identifying acorporeal image of self and its rela-tion to the environment; distinguish-ing self from nonself; recognizing fa-miliar members of a species as well asother familiar organisms, items, andplaces; recalling autobiographical in-formation; appraising environmentalreality; and emotionally understand-ing and reacting to bodily and envi-ronment stimuli. All of these criticaladaptive functions are present by thesecond postnatal year (the end of theright brain growth spurt), and all areessential components of the earliestmanifestation of mental health.

According to the unpublishedmanuscript of the Infant MentalHealth Task Force of Zero to Three,National Center for Infant, Toddlersand Families, “Infant mental healthis the developing capacity of the child

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from birth to three years to experi-ence, regulate, and express emotions;form close interpersonal relation-ships; and explore the environmentand learn. . . Infant mental health issynonymous with healthy social andemotional development.” The earli-est expression of mental health re-flects the adaptive or maladaptivefunctioning of the right brain, theneurobiological locus of the emo-tional self. (43)(44)

Although the right brain reorga-nizes later in life and retains plastic-ity, conditions affecting its initialstages of evolution have an enor-mous impact on its subsequent de-velopment. The postnatal matura-tion of limbic-autonomic circuits isinfluenced significantly by the pri-mary caregiver’s provision andregulation of social-emotional expe-riences within the attachment rela-tionship. Neuroscience now revealsthat at the most fundamental level,regulated attachment experiences fa-cilitate the brain’s major regulatorysystems, located in the right brain.However, studies also show that un-repaired and chronic stressful dys-regulating interactions within theearly social environment lay thegroundwork for an insecure attach-ment, right brain dysfunction,limbic-autonomic deficits, and thedevelopment of a predisposition tolater psychiatric and psychosomaticdisorders.

The principle that early disruptionof the mother-infant attachment re-lationship has a negative impact onbrain plasticity and predisposes tolater psychopathology is well es-tablished. (10)(45)(46)(47)(48)(49)(50) Helmeke and associates (51)concluded, “Positive (formation ofemotional attachment) or negative(eg, maternal separation or loss)emotional experience may carve apermanent trace into a still develop-ing neuronal network of immature

synaptic connections, and therebycan extend or limit the functionalcapacity of the brain during laterstages of life.” (See Affect Dysregula-tion and Disorders of the Self (11) foran extensive discussion of the neuro-biology of psychopathogenesis).

The increasing appreciation of theprofound and indelible impact ofearly interpersonal relationships onthe psychological, physiologic, andneurobiological trajectory of the selfover all stages of life substantially al-ters our view of human infancy. Inthe middle of the last century, thepediatrician-psychoanalyst DonaldWinnicott asserted that there is noinfant without the mother. (52) Thisdevelopmental psychological con-ception is mirrored in the previouslymentioned developmental neurobio-logical principle that “the self-organization of the developing brainoccurs in the context of a relationshipwith another self, another brain.” (7)This other brain is the right brain ofthe primary caregiver, the mother.Although controversies have existedin the past, a large and consistentbody of developmental neuroscienceresearch across both human and ani-mal species confirms the central roleof the early relationship with themother in the neurobehavioral devel-opment and, therefore, future social-emotional and stress-regulation ca-pacities of the developing individual.(25)(28)(45)(46)(53)(54)(55)(56)(57)(58)(59)

There is an intense interest in neu-roscience in the enduring impact ofearly “enriched experience” on braindevelopment in the first 18 postnatalmonths and in the applications of thisknowledge to child development.These studies indicate that enrichedexperiences “are especially effectiveearly in life and they set the basis forlater use and maintenance of thebrain and of ability.” (60) In the past,an “enriched environment” has been

defined narrowly as a complex phys-ical environment, and the reputedimpact of early exposure was on cog-nitive development. It now is clearthat for optimal brain development,the infant also needs to interact withan enriched social environment. Thespectrum of regulated affective trans-actions within a psychobiologicallyattuned mother-infant attachmentrelationship defines an enriched envi-ronment more correctly—one thathas a long-term impact on emotionaldevelopment and the essential capac-ity of self-regulation.

In accord with these conceptual-izations, a very recent National Insti-tute of Child and Human Develop-ment study on the mother-childrelationship and affect dysregulationconcluded, “Self-regulation in in-fancy is best conceptualized as a qual-ity of the infant-caregiver relation-ship, rather than a characteristic ofthe infant alone.” (61) The authorscited a large body of data that “em-phasize the importance of the child’srelationship with the primary care-giver as central to understanding thedevelopmental processes leadingfrom early affective arousal and atten-tion control to later functioning. . .Children’s inability to control nega-tive affect in early interactions withtheir caregivers may forecast con-tinuing difficulties with affective reg-ulation across multiple contexts.”

Psychobiological markers that as-sess attachment relationships, regula-tion of affect, the right brain, andinfant mental health need to be in-cluded in the diagnostic armamen-tarium of the practicing pediatrician.This information allows the clinicianto understand the system of nonver-bal communication and interactiveregulation that lies at the core of themother-infant relationship. To assessthe social and emotional capacitiesof the nonverbal infant and the statusof the nonverbal communications

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within the attachment dyad, the pe-diatrician must use clinical skills thatinvolve her or his subjective rightbrain as well as objective left brain.The principles of regulation theorythat apply to the mother-infant rela-tionship also apply to the clinician-patient relationship. (10)(12) Ac-cording to Adler, (62) the art of thedoctor-patient relationship, whichinvolves the physician’s empathy andthe capacity for responsive listening,“entails establishing the same kind ofperson-to-person attunement that isessential to the development of thenewborn (Shore, 1994).” Psycho-biological markers that assess attach-ment relationships, regulation ofaffect, the right brain, and infantmental health need to be included inthe diagnostic armamentarium of thepracticing pediatrician. (See the Ta-ble for a schematic of clinical obser-vations of affect regulation and rightbrain development.)

SummaryRecent interdisciplinary data on at-tachment, affect regulation, and theright brain can be applied directly toclinically relevant models of the ear-liest manifestations of normal andabnormal social and emotional de-velopment. Adaptive infant mentalhealth, an outcome of optimal at-tachment experiences, can be definedas the earliest expression of efficientand resilient right brain strategies forregulating both negative and positiveaffective states and for coping withnovelty and stress, especially inter-personal stress. (43) The formationof an increasingly complex rightbrain system for communicatingemotion allows the developing indi-vidual to switch internal, bodilybased affective states in response toperceived changes in the external so-cial environment via autoregulationor interactive regulation, thus main-taining a cohesive sense of self in

both autonomous or interconnectedcontexts.

On the other hand, maladaptiveinfant mental health is manifest in apoor right brain capacity to enterinto emotional communications withothers, prolonged frequent and in-tense episodes of affect dysregula-tion, a fragile self system, and an in-ability to adapt to demands of thedynamically changing social environ-ment in a timely manner. (48) Theformer is a resilience factor for cop-ing with the psychobiological stres-sors inherent in social interactions;the latter is a risk factor for interrup-tions of developmental processes anda vulnerability to the coping deficitsthat define a predisposition to later-forming psychopathology. Theseconceptions directly relate to whatthe American Academy of Pediatricsterms “the attainment of optimalphysical, mental, and social health forall infants” and thereby the primor-dial expression of health in “children,adolescents, and young adults.”

References1. Gluckman PD, Adler HM. Living withthe past: evolution, development, and pat-terns of disease. Science. 2004;305:1733–17362. Suomi SJ. How gene-environment inter-actions can influence emotional developmentin Rhesus monkeys. In: Bearer CEL, LernerRM, eds. Nature and Nurture: The ComplexInterplay of Genetic and Environmental Influ-ences on Human Behaviour and Development.Mahwah, NJ: Erlbaum; 2004:35–513. Crabbe JC, Phillips TJ. Mother naturemeets mother nurture. Nature Neurosci.2003;6:440–4424. Cicchetti D, Tucker D. Developmentand self-regulatory structures of the mind.Develop Psychopathol. 1994;6:533–5495. Bowlby J. Attachment and Loss. Vol. 1:Attachment. New York, NY: Basic Books;19696. Paus T, Collins AC, Leonard B, Zijden-bos A. Maturation of white matter in thehuman brain: a review of magnetic reso-nance studies. Brain Res Bull. 2001;54:255–266

7. Schore AN. The experience-dependentmaturation of a regulatory system in theorbital prefrontal cortex and the origin ofdevelopmental psychopathology. DevelopPsychopathol. 1996;8:59–878. Chiron C, Jambaque I, Nabbout R,Lounes R, Syrota A, Dulac O. The rightbrain hemisphere is dominant in human in-fants. Brain. 1997;120:1057–10659. Devinsky O. Right cerebral hemispheredominance for a sense of corporeal andemotional self. Epilep Behavior. 2000;1:60–7310. Schore AN. Affect Regulation and theOrigin of the Self: The Neurobiology of Emo-tional Development. Mahwah, NJ: Erlbaum;199411. Schore AN. Affect Dysregulation andDisorders of the Self. New York, NY: WWNorton; 200312. Schore AN. Affect Regulation and theRepair of the Self. New York, NY: WW Nor-ton; 200313. Van Toller S, Kendal-Reed M. A possi-ble protocognitive role for odor in humaninfant development. Brain Cognition.1995;29:275–29314. Weller A, Feldman R. Emotion regula-tion and touch in infants: the role of chole-cystokinin and opioids. Peptides. 2003;24:779–78815. Lester BM, Hoffman J, Brazelton TB.The rhythmic structure of mother-infant in-teraction in term and preterm infants. ChildDevelop. 1985;56:15–2716. Trevarthen C. The self born in inter-subjectivity: the psychology of an infantcommunicating. In: Neisser U, ed. The Per-ceived Self: Ecological and InterpersonalSources of Self-Knowledge. New York, NY:Cambridge University Press;1993:121–17317. Trevarthen C. Lateral asymmetries ininfancy: implications for the development ofthe hemispheres. Neurosci Biobehav Rev.1996;20:571–58618. Matsuzawa J, Matsui M, Konishi T, etal. Age-related changes of brain gray andwhite matter in healthy infants and children.Cerebral Cortex. 2001;11:335–34219. Semrud-Clikeman M, Hynd GW.Right hemisphere dysfunction in nonverballearning disabilities: social, academic, andadaptive functioning in adults and children.Psychol Bull. 1990;107:196–20920. Yamada H, Sadato N, Konishi Y, et al.A milestone for normal development of theinfantile brain detected by functional MRI.Neurology. 2000;55:218–22321. Tzourio-Mazoyer N, De Schonen S,Crivello F, Reutter B, Aujard Y, Mazoyer B.Neural correlates of woman face processing

back to basics


by 2-month-old infants. NeuroImage.2002;15:454–46122. Le Grand R, Mondloch C, Maurer D,Brent HP. Expert face processing requires vi-sual input to the right hemisphere during in-fancy. Nature Neurosci. 2003;6:1108–111223. Lorberbaum JP, Newman JD, HorwitzAR, et al. A potential role for thalamocingu-late circuitry in human maternal behavior.Biol Psychiatr. 2002;51:431–44524. Manning JT, Trivers RL, Thornhill R,et al. Ear asymmetry and left-side cradling.Evol Human Behavior. 1997;18:327–34025. Sieratzki JS, Woll B. Why do motherscradle babies on their left? Lancet. 1996;347:1746–174826. Epstein HT. An outline of the role ofbrain in human cognitive development.Brain Cognition. 2001;45:44–5127. Stuss DT, Alexander MP. Affectivelyburnt in: one role of the right frontal lobe?In: Tulving E, ed. Memory, Consciousness, andthe Brain: The Talin Conference. Philadelphia,Pa: Psychology Press; 1999:215–22728. Ovtscharoff W Jr, Braun K. Maternalseparation and social isolation modulate thepostnatal development of synaptic composi-tion in the infralimbic cortex of octodon de-gus. Neuroscience. 2001;104:33–4029. Borod J, Cicero BA, Obler LK, et al.Right hemisphere emotional perception: ev-idence across multiple channels. Neuropsy-chology. 1998;12:446–45830. Blonder LX, Bowers D, Heilman KM.The role of the right hemisphere in emo-tional communication. Brain. 1991;114:1115–112731. Dimberg U, Petterson M. Facial reac-tions to happy and angry facial expressions:evidence for right hemisphere dominance.Psychophysiol. 2000;37:693–69632. George MS, Parekh PI, Rosinsky N, etal. Understanding emotional prosody acti-vates right hemispheric regions. Arch Neu-rol. 1996;53:665–67033. Perry RJ, Rosen HR, Kramer JH, BeerJS, Levenson RL, Miller BL. Hemisphericdominance for emotions, empathy, and so-cial behavior: evidence from right and lefthanders with frontotemporal dementia.Neurocase. 2001;7:145–16034. Shamay-Tsoory SG, Tomer R, BergerBD, Aharon-Peretz J. Characterization ofempathy deficits following prefrontal braindamage: the role of the right ventromedialprefrontal cortex. J Cog Neurosci. 2003;15:324–33735. Winston JS, Strange BA, O’DohertyJO, Dolan RJ. Automatic and intentionalbrain responses during evaluation of trust-

worthiness of faces. Nature Neurosci. 2002;5:277–28336. Matthews SG. Early programming of thehypothalamo-pituitary-adrenal axis. TrendsEndocrinol Metab. 2002;13:373–38037. Maunder RG, Hunter JJ. Attachmentand psychosomatic medicine: developmen-tal contributions to stress and disease. Psy-chosomat Med. 2001;63:556–56738. Schmidt S, Nachtigall C, Wuethrich-Martone O, Strauss B. Attachment and cop-ing with chronic disease. J Psychosomat Res.2002;53:763–77339. Luecken LJ. Childhood attachmentand loss experiences affect adult cardiovas-cular and cortisol function. PsychosomatMed. 1998;60:765–77240. Pauli P, Wiedemann G, Nickola M.Pain sensitivity, cerebral laterality, and neg-ative affect. Pain. 1999;80:359–36441. Decety J, Chaminade T. When the selfrepresents the other: a new cognitive neuro-science view on psychological identification.Conscious Cognition. 2003;12:577–59642. Keenan JP, Nelson A, O’Connor M,Pascual-Leone A. Self-recognition and theright hemisphere. Nature. 2001;409:30543. Schore AN. The effects of a secure at-tachment relationship on right brain devel-opment, affect regulation, and infant mentalhealth. Infant Mental Health J. 2001;22:7–6644. Schore AN. Plenary address: parent-infant communications and the neurobiol-ogy of emotional development. In: Proceed-ings of Head Start’s Fifth National ResearchConference, Developmental and ContextualTransitions of Children and Families. Impli-cations for Research, Policy, and Practice.Washington, DC: Department of Healthand Human Services; 2000:49–7345. Caldji C, Tannenbaum B, Sharma S,Francis D, Plotsky PM, Meaney MJ. Mater-nal care during infancy regulates the devel-opment of neural systems mediating the ex-pression of fearfulness in the rat. Proc NatlAcad Sci USA. 1998;95:5335–534046. Cirulli F, Berry A, Alleva E. Early dis-ruption of the mother-infant relationship:effects on brain plasticity and implicationsfor psychopathology. Neurosci BiobehavRev. 2002;27:73–8247. Graham YP, Heim C, Goodman SH,Miller AH, Nemeroff CB. The effects ofneonatal stress on brain development: im-plications for psychopathology. Develop Psy-chopathol. 1999;11:545–56548. Schore AN. The effects of relationaltrauma on right brain development, affectregulation, and infant mental health. InfantMental Health J. 2001;22:201–269

49. Schore AN. Dysregulation of the rightbrain: a fundamental mechanism of trau-matic attachment and the psychopathogen-esis of posttraumatic stress disorder. AustralNew Zeal J Psychiatr. 2002;36:9–3050. Siegel DJ. The Developing Mind: To-ward a Neurobiology of Interpersonal Experi-ence. New York, NY: Guilford Press; 199951. Helmeke C, Ovtscharoff W Jr, PoeggelG, Braun K. Juvenile emotional experiencealters synaptic inputs on pyramidal neuronsin the anterior cingulate cortex. CerebralCortex. 2001;11:717–72752. Winnicott DW. The theory ofparent–infant relationship. In: The Matura-tional Processes and the Facilitating Environ-ment. New York, NY: International Univer-sities Press; 196053. Carter CS. Neuroendocrine perspec-tives on social attachment and love. Psycho-neuroendocrinol. 1998;23:779–81854. Fleming AS, O’Day DH, Kraemer GW.Neurobiology of mother-infant reactions:experience and central nervous system plas-ticity across development and generations.Neurosci Biobehav Rev. 1999;23:673–68555. Gunnar MR, Donzella B. Social regu-lation of the cortisol levels in early humandevelopment. Psychoneuroendocrinol. 2002;27:199–22056. Meaney MJ. Maternal care, gene expres-sion, and the transmission of individual differ-ences in stress reactivity across generations.Annu Rev Neurosci. 2001;24:1161–119257. Menard JL, Champagne DL, MeaneyMJP. Variations of maternal care differen-tially influence “fear” reactivity in responseto the shock-probe burying test. Neuro-science. 2004;129:297–30858. Nitschke JB, Nelson EE, Rusch BD,Fox AS, Oakes TR, Davidson RJ. Orbito-frontal cortex tracks positive mood in moth-ers viewing pictures of their newborn in-fants. NeuroImage. 2004;21:583–59259. Weaver ICG, Cervoni N, ChampagneFA, et al. Epigenetic programming by ma-ternal behavior. Nature Neurosci. 2004;7:847–85460. Rosenzweig MR, Bennett EL. Psycho-biology of plasticity: effects of training andexperience on brain and behavior. BehavBrain Res. 1996;78:57–6561. NICHD Early Child Care ResearchNetwork. Affect dysregulation in themother-child relationship in the toddleryears: antecedents and consequences. De-velop Psychopathol. 2004;16:43–6862. Adler HM. The sociophysiology of car-ing in the doctor-patient relationship. J GenIntern Med. 2002;17:883–890

back to basics


Tab

le.Sc

hore

’sM

odel

ofAf

fect

Regu

latio

nan

dRi

ght

Brai

nDe

velo

pmen

t

Infa

ntCo

ntex

tM

othe

rCo

ntex

tIn

tera

ctiv

eCo

ntex

tRi

ght

Brai

nto

Righ

tBr

ain

RIGH

TBR

AIN

COM

MUN

ICAT

ION

PROC

ESSE

SVI

SUAL

/FAC

IAL

Regu

late

dRe

spon

se!

Orie

nts,

expl

ores

,gaz

esat

face

ofm

othe

ran

dot

hers

,see

ksey

eco

ntac

t.!

Disp

lays

brig

ht,w

ide-

eyed

faci

alex

pres

sions

.!

Uses

aw

ide

rang

eof

affe

ctiv

eex

pres

sions

.!

Rest

ing

quie

t-al

ert

stat

eof

plea

sant

faci

alex

pres

sions

.

!Re

spon

ds(a

ttun

es)

toin

fant

’scu

esw

ithva

riety

ofaf

fect

ivel

yex

pres

sive

faci

alex

pres

sions

(eye

cont

act,

smili

ng,p

leas

ant

faci

alex

pres

sions

).

!Dy

adic

visu

al-a

ffec

tive

arou

salr

egul

atio

n.!

Each

mem

ber

ofdy

adfo

cuse

sga

zeup

onth

eot

her,

enga

ging

inm

utua

leye

cont

act,

smili

ng,b

right

faci

alex

pres

sions

.!

Inte

rper

sona

lres

onan

ceam

plifi

espo

sitiv

est

ates

inbo

th.

Stre

ssRe

spon

se!

Durin

gre

latio

nals

tres

s,tr

ansie

ntly

avoi

dsor

ient

ing,

expl

orin

g,or

gazi

ngat

mot

her’s

face

oren

gagi

ngin

eye

cont

act.

!Fl

at,a

bsen

t,fe

ar-i

nduc

ing,

orin

cong

ruen

tfa

cial

expr

essio

ns(la

ughi

ngw

hen

infa

ntis

dist

ress

ed).

!On

ebr

eaks

off

mut

ualg

aze

and/

orey

eco

ntac

t.!

Dyad

tran

sient

lyou

tof

sync

(misa

ttun

ed);

acut

edy

adic

stre

ss.

!Ab

senc

eor

avoi

danc

eof

eye

cont

act

byei

ther

mot

her

orin

fant

may

bea

signi

fican

tin

dica

tor

requ

iring

furt

her

inve

stig

atio

n.VO

CAL

TON

EAN

DRH

YTHM

Regu

late

dRe

spon

se!

Turn

sto

war

dsm

othe

r’svo

ice.

!Us

esin

vitin

g/pl

ayfu

lton

ein

resp

onse

(coo

ing,

babb

ling)

.

!Vo

caliz

esso

othi

ngre

spon

ses

with

varie

dto

nes

and

rhyt

hms.

!M

odul

ates

tone

san

drh

ythm

sof

voic

eto

infa

nt’s

psyc

hobi

olog

ical

stat

e.

!Dy

adic

audi

tory

-aff

ectiv

ear

ousa

lreg

ulat

ion.

!M

atch

esor

imita

tes

each

othe

r’svo

calt

ones

and

rhyt

hms.

Stre

ssRe

spon

se!

Durin

gre

latio

nals

tres

s,tr

ansie

ntly

turn

saw

ayfr

omm

othe

r’svo

ice.

!Us

esdi

stre

ssed

tone

(cry

ing)

inre

spon

seor

isno

nres

pons

ive.

!Us

esdi

scor

dant

,har

sh,l

oud,

orun

mod

ulat

edto

nean

drh

ythm

ofvo

ice

ordo

esno

tus

evo

caliz

atio

nsin

resp

onse

toin

fant

’sem

otio

nal

com

mun

icat

ion.

!Do

esno

tvo

caliz

eor

mirr

or(m

atch

)in

fant

’svo

caliz

atio

ns.

!On

eus

esdi

scor

dant

tone

whi

leth

eot

her

issil

ent

orbo

thar

eus

ing

dist

ress

edor

disc

orda

ntto

nes.

!No

nres

pons

ivity

ortu

rnin

gaw

ayfr

omm

othe

r’svo

ice

may

bea

signi

fican

tin

dica

tor

requ

iring

furt

her

inve

stig

atio

n.

GEST

URAL

/POS

TURA

LRe

gula

ted

Resp

onse

!M

oves

limbs

and

body

even

lyan

dflu

idly

,rel

axed

post

ure,

reac

hes

and

turn

sto

war

dot

her

orno

vel

soci

alst

imul

us.

!Ap

proa

ches

toso

othe

,man

ipul

ate,

orm

aneu

ver

infa

ntge

ntly

and

caut

ious

ly.

!Re

spon

dsto

and

inte

rpre

tsso

cial

bodi

lyba

sed

gest

ures

.

!In

intim

ate

phys

ical

cont

ext,

dyad

’srh

ythm

icm

atch

ing

allo

ws

bodi

esto

crad

le/m

old

into

othe

r.!

Inso

cial

refe

renc

ing

late

infir

stye

ar,g

estu

res

beco

me

purp

osef

ulan

dsy

nchr

oniz

ed,p

rom

otin

gin

ters

ubje

ctiv

een

gage

men

t.(c

ontin

ued)

back to basics


Tab

le.Sc

hore

’sM

odel

ofAf

fect

Regu

latio

nan

dRi

ght

Brai

nDe

velo

pmen

t(c

ontin

ued)

Infa

ntCo

ntex

tM

othe

rCo

ntex

tIn

tera

ctiv

eCo

ntex

tRi

ght

Brai

nto

Righ

tBr

ain

Stre

ssRe

spon

se!

Inso

cial

lyst

ress

edco

ntex

ts,

mov

eslim

bsun

even

lyan

d/or

fran

tical

ly.

!Fa

ilsto

reac

hou

t,av

erts

head

,tu

rns

body

away

,stif

fens

orar

ches

body

tom

othe

r’sto

uch.

!Ap

proa

ches

infa

ntto

oqu

ickl

yor

resp

onds

toin

fant

inth

reat

enin

gor

fear

fulm

anne

r.!

Hand

les

awkw

ardl

yor

roug

hly.

!M

isint

erpr

ets

infa

nt’s

gest

ures

ordo

esno

tat

tem

ptto

soot

he,

resp

ond,

orin

terp

ret

gest

ures

and

body

mov

emen

ts.

!In

fant

cont

inue

sor

incr

ease

sdi

stre

ssed

gest

ures

and

post

ures

and

isun

resp

onsiv

eto

mot

her’s

effo

rts.

!M

othe

rin

crea

ses

roug

h/aw

kwar

dge

stur

es/p

ostu

res.

!M

othe

rco

ntin

ues

tom

isint

erpr

etin

fant

’sge

stur

es/

body

mov

emen

ts.

!Dy

adbe

com

esfr

ustr

ated

orce

ases

/fai

lsto

atte

mpt

toso

othe

and

com

fort

inte

ract

ivel

y.RI

GHT

BRAI

NAF

FECT

PROC

ESSI

NG

POSI

TIVE

AFFE

CTPR

OCES

SIN

GRe

gula

ted

Resp

onse

!Hi

gh,p

ositi

vear

ousa

l.!

Enjo

ymen

t-jo

y,in

tere

st-

exci

tem

ent.

!Vi

talit

yex

pres

sed

free

ly.

!Ha

ppy

dem

eano

r;re

spon

sive

to,

supp

ortiv

eof

,and

mat

chin

gof

infa

nt’s

affe

ctan

dpo

sitiv

ear

ousa

l.

!M

utua

ldel

ight

.!

Mot

her

orin

fant

lead

saf

fect

ive

inte

ract

ion

whi

leot

her

follo

ws.

!N

on-o

verw

helm

ing

and

turn

-tak

ing

beha

vior

s.!

Dyad

icam

plifi

catio

nof

posit

ive

arou

sali

nre

latio

nalp

lay.

Stre

ssRe

spon

se!

Hype

raro

used

/ove

rstim

ulat

edor

hypo

arou

sed/

unde

rstim

ulat

ed.

!In

cong

ruen

tha

ppy

dem

eano

rto

infa

nt’s

dist

ress

edcu

esor

sad

dem

eano

rto

infa

nt’s

posit

ive

cues

.!

Cont

inue

sto

fail

tocr

eate

regu

late

d,po

sitiv

ear

ousa

lstim

uli

for

infa

nt.

!Lo

wfr

eque

ncy

ofpl

aybe

havi

or.

!M

ismat

ched

(misa

ttun

ed)

arou

sals

tate

s.!

One

orbo

thhy

pera

rous

ed/o

vers

timul

ated

oron

eis

inpo

sitiv

ear

ousa

lsta

tew

hile

the

othe

ris

hypo

arou

sed/

unde

rstim

ulat

edor

hype

raro

used

/ov

erst

imul

ated

.!

Over

whe

lmed

dyad

.

NEG

ATIV

EAF

FECT

PROC

ESSI

NG

Regu

late

dRe

spon

se!

Fuss

y,m

oody

affe

ctex

pres

sed

free

ly.

!Re

silie

nce.

!Ab

leto

tole

rate

and

expr

ess

sadn

ess,

ange

r,fe

arin

self

and

infa

ntw

hile

seek

ing

toin

tera

ctap

prop

riate

ly.

!Pa

rtic

ipat

esin

inte

ract

ive

repa

ir.

!M

utua

latt

unin

gto

disq

uiet

ing

stim

ulio

rco

nditi

on.

Stre

ssRe

spon

se!

With

draw

sor

isno

nres

pons

ive

orbe

com

esag

itate

d,fr

ustr

ated

,or

fear

fulw

hen

expe

rienc

ing

sens

atio

nsof

dist

ress

(dys

regu

late

dst

ates

).!

Incr

easin

gin

tens

ityan

ddu

ratio

nof

eith

erst

ate

prec

lude

sin

fant

’squ

ick

resp

onse

toso

othi

ngat

tem

pts

and

retu

rnto

regu

late

dst

ate.

!Un

able

toto

lera

teow

nne

gativ

efe

elin

gsan

dre

spon

dsin

appr

opria

tely

(exp

ress

esan

ger,

irrita

tion,

orfr

ustr

atio

nor

with

draw

san

dis

nonr

espo

nsiv

eto

war

din

fant

).!

Poor

capa

city

for

inte

ract

ive

repa

ir.

!M

utua

lfru

stra

tion.

!M

othe

rca

nnot

ordo

esno

tso

othe

infa

ntan

dre

pair

nega

tive

affe

ct:d

yad

rem

ains

indi

stre

ssed

stat

e.

back to basics


Infa

ntCo

ntex

tM

othe

rCo

ntex

tIn

tera

ctiv

eCo

ntex

tRi

ght

Brai

nto

Righ

tBr

ain

RIGH

TBR

AIN

REGU

LATI

ONIN

TERA

CTIV

ERE

GULA

TION

!Ex

pres

ses

and

reco

gniz

esaf

fect

ive

faci

alex

pres

sions

,vo

caliz

atio

ns,a

ndge

stur

es.

!In

fant

seek

sou

tm

othe

rto

core

gula

tein

ner

stat

eof

bein

g.

!Re

spon

dsw

ithar

ousa

l/reg

ulat

ing

faci

alex

pres

sions

,voc

aliz

atio

ns,

and

gest

ures

.!

Mot

her

seek

sto

affe

ctin

fant

’sin

ner

stat

eof

bein

g.

!Ea

chm

embe

rof

dyad

cont

inge

ntly

resp

onds

toot

her’s

faci

alex

pres

sions

,voc

aliz

atio

ns,a

ndge

stur

es(r

ight

brai

nto

right

brai

n)!

Mot

her

and

infa

ntin

tera

ctiv

ely

seek

attu

nem

ent.

!Fr

eque

ntep

isode

sof

inte

ract

ive

play

.AU

TORE

GULA

TION

!Se

lf-so

othi

ngbe

havi

ors

(suc

ksfin

ger/

paci

fier,

rock

sbo

dy,h

olds

soft

obje

ct).

!Se

lf-cr

eate

dso

lutio

nsfo

rre

gula

ting

inne

rst

ate

ofbe

ing.

!Se

lf-ca

lmin

gbe

havi

ors

(dee

pbr

eath

s,se

lf-ta

lk).

!M

othe

rle

tsin

fant

stru

ggle

with

dist

ress

brie

flyan

dth

enre

gula

tes

(ass

ists

inau

tore

gula

tion)

.

!Ea

chm

embe

rof

dyad

rem

ains

calm

inpr

esen

ceof

othe

r.!

Each

regu

late

sow

nst

ate

ofbe

ing

auto

nom

ously

.

RIGH

TBR

AIN

DYSR

EGUL

ATIO

NIN

TERA

CTIV

EDY

SREG

ULAT

ION

!Av

erts

gaze

,bec

omes

agita

ted

byso

unds

and

gest

ures

.!

Star

tles

topa

rent

.!

Habi

tual

lydi

scon

nect

sfr

omm

othe

r’sat

tem

pts

toco

regu

late

whi

lein

ner

stat

ees

cala

tes.

!Se

nse

ofsa

fety

thre

aten

edby

inte

ract

ion.

!Fr

eque

ntan

gry,

host

ilefa

cial

expr

essio

ns,h

arsh

tone

and

unev

enrh

ythm

s,th

reat

enin

gge

stur

es.

!Do

esno

tlo

okat

the

infa

ntor

unre

spon

sive

“dea

dfa

ce.”

!Re

peat

edly

fails

tore

spon

dto

infa

nt’s

affe

ctiv

est

rugg

lede

spite

infa

nt’s

esca

latin

gin

ner

dist

ress

.

!M

utua

laro

usal

dysr

egul

atio

n.!

Indi

vidu

ally

ordy

adic

ally

igno

res

cues

ofot

her;

dyad

fails

toco

llabo

rate

inre

gula

ting

infa

nt’s

inne

rne

edst

ate.

!In

cons

olab

lein

fant

may

lead

tom

othe

r’sne

gativ

efe

elin

gsto

war

dhi

m/h

eran

ddi

min

ishm

othe

r’sco

nfide

nce

inhe

rbe

ing

a“g

ood

enou

gh”

mot

her.

AUTO

DYSR

EGUL

ATIO

N!

Cryi

ng,a

rchi

ng,fl

ailin

g,an

dvo

miti

ng;o

rbl

ank

star

e,lim

p,m

otio

nles

s.!

Infa

ntre

peat

edly

fails

tose

lf-re

gula

tein

ner

stat

e,be

com

ing

over

whe

lmed

,eve

ntua

llyex

haus

ted

and

with

draw

n.!

Diss

ocia

tes

tom

ater

nals

timul

i.!

Chro

nic

sens

eof

thre

ator

lack

ofse

nse

ofsa

fety

.

!Irr

itabl

e,th

reat

enin

g,in

trus

ive,

and

roug

hor

flat

affe

ct,u

nres

pons

ive.

!Di

sreg

ards

infa

nt’s

abili

tyto

auto

-re

gula

teby

quie

ting

orst

imul

atin

gse

lf.!

Diss

ocia

tes

toin

fant

’sst

imul

i.

!Ag

itate

dor

with

draw

nin

pres

ence

ofot

her.

!Bo

thfa

ilto

allo

win

fant

toen

larg

ehi

s/he

rca

paci

tyto

self-

regu

late

affe

ct.

!N

ore

latio

nalo

rin

ters

ubje

ctiv

eco

ntex

t.

back to basics


Appendix. Anatomy andPhysiology of Attachmentand Affect RegulationIn his initial outline of attachmenttheory, Bowlby hypothesized that asuccession of increasingly complexregulatory systems involving the lim-bic system and brain arousal areasmediates attachment processes. Theneuroscience literature now refers tothe “rostral limbic system,” a hierar-chical sequence of interconnectedlimbic areas in the amygdala, anteriorcingulate, insula, and orbital cortex,and a “circuit of emotion regulation”consisting of the amygdala, anteriorcingulate, and orbital frontal cortex.Based on the principle of caudal-to-rostral brain development, I have of-fered a model of the early experience-dependent maturation of the limbicsystem and proposed a sequence ofregulatory systems that are imprintedby more complex attachment com-munications and evolve over the first2 years of human infancy. (1)(2) Theoptimal formation of these brain ar-eas essential to the child’s emotionaldevelopment depends on theinteractive regulation embeddedwithin the attachment communica-tions of the mother-infant relationship.

At birth, only the amygdala, aprimitive subcortical limbic regula-tory system that appraises crude in-formation about external stimuli andmodulates autonomic and arousalsystems, is online. The right amyg-dala processes olfactory stimuliwithin the mother-perinatal infantrelationship and mediates the infant’srecognition of the mother’s scent aswell as the mother’s recognition ofthe neonate through olfactory cues.At 8 weeks, a critical period for thedevelopment of the anterior cingu-late commences, allowing this systemto regulate play and separation be-haviors, laughing and crying vocal-izations, face representations, andthe modulation of autonomic activ-

ity. The first year also is a criticalperiod of experience-dependent mat-uration of the right insula, a structurewithin the temporal lobes that is in-volved essentially in the subjectiveawareness of inner body feelings andemotionality, and the right parietalcortex, a posterior cortical area in-volved in the representation of thephysical self and the ability to distin-guish self from others.

By the last quarter of the firstpostnatal year, the orbital (ventro-medial) areas of the frontal lobes en-ter a critical period of growth thatcontinues through the middle of thesecond year. The orbitofrontal cor-tex, the hierarchical apex of the lim-bic system, acts at the highest level ofcontrol of behavior, especially in re-lation to emotion, and is identical toBowlby’s control system of attach-ment. I have suggested that in mu-tual gaze transactions, the mother isdownloading programs from herlimbic system into the child’s devel-oping limbic system. A very recentfMRI study by Nitschke and col-leagues of mothers viewing a photo-graph of their own infants showedmaximal brain activation in themother’s orbitofrontal cortex, espe-cially on the right side. (3) Theseauthors concluded that this cortexplays a critical role in the representa-tion of attachment-related positiveaffect, as described by Bowlby, that itlinearly tracks the intensity of posi-tive emotions underlying maternalattachment, and that individual vari-ations in orbitofrontal activation toinfant stimuli reflect an important di-mension of maternal attachment.

Other studies demonstrate thatthe right prefrontolimbic areas play aprimary role in the appraisal of bio-logically meaningful exteroceptiveand interoceptive self-related infor-mation and in the integration of in-ternal physiologic states with salientenvironmental cues, processes cen-

tral to the attachment mechanism.This right cerebral hemisphere is crit-ically involved in regulating thehypothalamic-pituitary-adrenal (HPA)axis and in activating physiologic stressresponses. (4) More than any other areaof the human prefrontal lobes, the rightorbitofrontal cortex, which plays an ex-ecutive control function for the entireright brain, is linked most directly to thebrain’s stress regulatory system. (5)Recall, the regulation of stressors in so-cial relationships, modifies prefrontalmaturation, and in this manner a secureattachment facilitates the transfer of reg-ulatory capacities from caregiver to in-fant. Lyons and colleagues state, “Theo-ries of human development suggest thatstressful experiences in social relation-ships modify prefrontal maturation(Schore, 1996)” and demonstrate thatconditions that affect early maternal vari-ability in infancy produce “significantdifferences in right but not left adultprefrontal volumes, with experience-dependent asymmetric variation mostclearly expressed in ventral medial cortexmeasured in vivo by magnetic resonanceimaging.” (6) Thus, on a fundamentallevel, the attachment relationship be-tween the child and primary caregiver isformative because it promotes the devel-opment of the brain’s major self-regulatory mechanisms.

More specifically, the attachmentrelationship mediates the dyadic reg-ulation of both positive and negativeemotion via the maternal interactiveregulation of the infant’s postnatallydeveloping autonomic nervous sys-tem (ANS). Optimally regulatedcommunications embedded in se-cure attachment experiences imprintthe connections between the postna-tally maturing central nervous systemlimbic system that processes and reg-ulates social-emotional stimuli andthe ANS that generates the somaticaspects of emotion. A growing bodyof work reveals that the right hemi-sphere is deeply connected into the

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ANS and that it, more so than theleft, controls both sympathetic andparasympathetic responses. (7) Thehypothalamus, the head ganglion ofthe ANS, is right lateralized, and thehypothalamic nuclei are considerablylarger on the right side of the humanbrain. This hemisphere is dominantfor the production of corticotropin-releasing factor and the glucocorti-coid cortisol, the neurohormonesthat mediate stress coping responses.Convincing evidence shows that theinfant’s relationship with the motherregulates the development of theHPA axis, (8) that neonatal socialbehavior associated with the HPAaxis increases right hemisphere dom-inance, (9) and that perinatal distressleads to a blunting of the stress re-sponse in the right (and not left)

prefrontal cortex that is manifest inadulthood. (10)

References1. Schore AN. The effects of a secure at-tachment relationship on right brain devel-opment, affect regulation, and infant mentalhealth. Infant Mental Health J. 2001;22:7–662. Schore AN. Affect Dysregulation andDisorders of the Self. New York, NY: WWNorton; 20033. Nitschke JB, Nelson EE, Rusch BD, FoxAS, Oakes TR, Davidson RJ. Orbitofrontalcortex tracks positive mood in mothersviewing pictures of their newborn infants.NeuroImage. 2004;21:583–5924. Wittling W. The right hemisphere andthe human stress response. Acta PhysiolScand. 1997;640(suppl):55–595. Sullivan RM, Gratton A. Prefrontalcortical regulation of hypothalamic-pituitary-adrenal function in the rat and

implications for psychopathology: sidematters. Psychoneuroendocrinol. 2002;27:99–1146. Lyons DM, Afarian H, Schatzberg AF,Sawyer-Glover A, Moseley ME. Experience-dependent asymmetric maturation in pri-mate prefrontal morphology. Exp BrainRes. 2002;136:51–597. Spence S, Shapiro D, Zaidel E. The roleof the right hemisphere in the physiologicaland cognitive components of emotionalprocessing. Psychophysiol. 1996;33:112–1228. Gunnar MR, Donzella B. Social regula-tion of the cortisol levels in early humandevelopment. Psychoneuroendocrinol. 2002;27:199–2209. Tang AC, Reeb BC, Romeo RD, Mc-Ewen BS. Modification of social memory,hypothalamic-pituitary-adrenal axis, andbrain asymmetry by neonatal novelty expo-sure. J Neurosci. 2003;23:8254–826010. Brake WG, Sullivan RM, Gratton A.Perinatal distress leads to lateralized medialprefrontal cortical dopamine hypofunction inadult rats. J Neurosci. 2000;20:5538–5543

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Documents

Schore Pediatrics in Review (2011) Attachment & Emotion