Development and Psychopathology, 9 (1997), 595–631Copyright 1997 Cambridge University PressPrinted in the United States of America

Early organization of the nonlinear rightbrain and development of a predispositionto psychiatric disorders

ALLAN N. SCHOREDepartment of Psychiatry and Biobehavioral Sciences, UCLA School of Medicine

AbstractThe concepts of self-organization, state changes, and energy flow are central to dynamic systems theory. In thiswork I suggest that to apply these general principles to the study of normal and abnormal development, theseconstructs must be specifically defined in reference to current knowledge of brain development. Toward that end, Ipresent an overview of the properties of self-organizing developmental systems, and then propose a model ofattachment dynamics as synchronized energy exchanges that cocreate nonlinear changes of state, discuss the roles ofbioamines and energy-generating brain mitochondria in state regulation, and describe the energy-dependentimprinting of synaptic connectivity and neural circuitry in the infant brain. In this application of nonlinear conceptsto developmental models of both resistance against and vulnerability to mental disorders, particular emphasis isplaced upon the experience-dependent maturation of a system in the orbital prefrontal cortex that regulatespsychobiological state and organismic energy balance. This frontolimbic system is expanded in the nonlinear righthemisphere that generates stress-regulating coping strategies, and it serves as the hierarchical apex of the limbic andautonomic nervous systems. Early forming microstructural alterations and energetic limitations of this regulatorysystem are suggested to be associated with a predisposition to psychiatric disorders.

Although there is now agreement within a sciences. In particular, I will propose that cur-rent multidisciplinary knowledge regardingwide spectrum of sciences that dynamic sys-

tems theory offers powerful insights into the three systems concepts—state changes, self-organization, and the central role of energyorganizational principles of all inanimate and

animate systems, the application of its general flows—can more deeply elucidate the mecha-nisms by which early development indeliblytenets to specific problems of human psychol-

ogy and biology has presented a difficult chal- influences all later function and dysfunction.A fundamental focus of nonlinear dynamiclenge. And yet this model of the mechanism

of self-organization, of how complex systems theory is the modeling of complex patterns ofstate changes in all physical and biologicalthat undergo discontinuous changes come to

produce both emergent new forms yet retain systems. This clearly implies that the basicunit of analysis of the process of human de-continuity, clearly must be relevant to the

study of normal and abnormal human devel- velopment is not changes in behavior, cogni-tion, or even affect, but rather the ontogeneticopment. In this paper, I will suggest that to

more deeply integrate nonlinear principles appearance of more and more complex psy-chobiological states that underlie these state-into the discipline of developmental psycho-

pathology, they must not be used as just meta- dependent emergent functions (Schore, 1994).Lydic (1987, p. 14) points out that “studiesphors but rather directly incorporated in their

literal form into the core of the developmental that ignore organismic state are analogous tothe experiments of physics that ignore time”and that the ubiquity of state-dependent or-Address correspondence and reprint requests to: Allan N.

Schore, 9817 Sylvia Avenue, Northridge, CA 91324. ganismic changes “reminds us that biological

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A. N. Schore596

systems are highly dynamic and notoriously lateralized in the early developing right brain(Chiron et al., 1997), which is, more so thannonlinear.” He then concludes that the pros-

pects for future progress in our understanding the left, well connected into the limbic systemand the mechanisms of autonomic and behav-of state phenomena must include a deeper ex-

plication of the role played by the brain sys- ioral arousal, and their maturation is experi-ence-dependent. In light of the ontogenetictems that biochemically regulate all brain

and bodily state phenomena—various discrete principle that the most important informationfor the successful development of the humangroups of bioaminergic neurons of the subcor-

tical reticular formation that innervate wide brain is conveyed by the social rather than thephysical environment, I have proposed thatareas of the brain through diffuse projections.

The unique anatomical capacities of these sys- “the self-organization of the developing brainoccurs in the context of another self, anothertems to affect large areas simultaneously

allow for their central involvement in global, brain” (Schore, 1996, p. 60). This organiza-tion, like all aspects of human brain matura-state-associated brain functions.

The concept of psychobiological state lies tion, is nonlinear and shows discontinuous de-velopmental patterns.at the common boundary of the psychological

and biological sciences, and as such it can go And lastly, another cardinal feature of non-linear theory is that it assigns the sources offar to overcome the myopia of “Descarte’s er-

ror,” “the separation of the most refined oper- new adaptive forms to the self-organizingproperties of systems that use energy in orderations of mind from the structure and opera-

tion of a biological organism” (Damasio, to faciliate the cooperativity of simpler sub-system components into a hierarchically1994, p. 250). At all points of human develop-

ment, but especially in infancy, the continu- structured complex system (Thelen, 1989).This model therefore emphasizes the centralally developing mind cannot be understood

without reference to the continually maturing roles of thermodynamics, the science of en-ergy flow, and bioenergetics, the study of howbody, and their ongoing interactions become

an important interface for the organizing self. energy is used for the work of establishingbiological order, toward the understanding ofThis perspective necessitates an infusion of

recent data from developmental psychobiol- the creation of new complex structural forms.The functional activity of the brain is an en-ogy into the disciplines of developmental psy-

chology and developmental psychopathology. ergy-requiring process. One of the most strik-ing aspects of development is found in theIndeed, in a very recent text of this field, Mi-

chel and Moore (1995) declare that dynamic growing brain’s rapidly increasing capacity togenerate and sustain higher and higher levelssystem theories are “good models on which to

construct the developmental psychobiological of energy metabolism over the first 2 years oflife.approach” (p. 31).

A second core assumption of systems the- The biosynthetic processes that underliethe proliferation of synaptic connections inory is that self-organization is characterized

by the emergence and stabilization of novel the postnatally developing brain demand, inaddition to sufficient quantities of essental nu-forms from the interaction of lower-order

components and involves “the specification trients, massive amounts of energy, so muchso that the metabolic rate of the young child’sand crystallization of structure” (Lewis, 1995).

I will argue that this mechanism also de- brain is significantly greater than adults (Ken-nedy & Sokoloff, 1957). Sequential incre-scribes how hierarchical structural systems in

the developing brain self-organize. The devel- ments in metabolic rates take place in variousregions of the brain during postnatal develop-opmental neurosciences are now identifying

the “lower” autonomic and “higher” central ment, and this accounts for the finding thatthe brain matures in discontinuous discretebrain systems that organize in infancy and be-

come capable of generating and regulating stages (Martin et al., 1988). Because of therelationship between energy metabolism andpsychobiological states. These homeostatic

structures that maintain stability are primarily physiological function, this event is central to

Nonlinear right brain 597

the emergence of “higher” brain systems and theory to normal development, and then to aconceptualization of atypical development,the appearance of more complex behaviors. A

central principle of systems theory asserts that but I will address the underlying mechanismscommon to both. Within this framework, Iself-organization increases the rate of energy

transfer, and the more ordered the complexity, will propose models of the nonlinear phenom-ena of attachment dynamics, of the roles ofthe faster the energy flows (Goerner, 1995).

In light of the fact that energy systems within bioamines and mitochondria in self-oganiza-tional processes of synaptic connectivity, andthe developing brain responsible for self-or-

ganization are themselves undergoing dra- of the energy-dependent imprinting of neuralcircuitry in the infant brain. In this applicationmatic transformation, I will propose that

knowledge of the gene–environment interac- of self-organizational concepts to develop-mental models of both resistance against andtions responsible for the onset of aerobic en-

ergy metabolism in mitochondria, the preemi- vulnerability to mental disorders, I will partic-ularly focus on the experience-dependent mat-nent source of biological energy in the brain,

is relevant to an understanding of how neu- uration of a frontolimbic system that regulatespsychobiological states and organismic en-rons increase their synaptic connectivity and

how energy fluxes organize new adaptive ergy balance in a nonlinear fashion. This pre-frontal system is expanded in the right hemi-structures in development.

The energy metabolism of the brain is reg- sphere that plays a superior role in enablingthe organism to cope actively and passivelyulated and coordinated by biogenic amines

that are delivered to widely distributed re- with stress. In the final section, I will suggestthat early forming microstructural pathologygions by ascending, unmyelinated projections

from the brain stem. Ontogenetic changes in and energetic limitations of this specific sys-tem are associated with a predisposition tothese monoaminergic systems result in pro-

gressive increases in organismic energy me- later appearing psychiatric disorders. Thiswork is a continuation of recent writings intabolism. These neuromodulators, in concert

with different subtypes of their receptors that which I contend that less than optimal gene–environment interactions that occur during thedetermine whether they augment local excit-

atory or inhibitory activity, alter and synchro- critical period of growth of this system pro-duce a frontolimbic organization that is vul-nize the input–output characteristics of brain

cell populations in accord with changes in nerable to a spectrum of psychopathologies(Schore 1994, 1996).arousal. In human infancy these same bio-

agents that regulate central arousal and bodilystates play an essential ontogenetic role—they Functional Properties of Self-Organizingalso act as morphogenetic agents that induce Developmental Systemsthe growth and organization of the developingbrain. Most intriguingly, it is now evident that A fundamental property of any developing

living system is that it is open to and interac-these bioamines are regulated by the interac-tion between caregiver and infant. Neurobio- tive with its particular environment. This ap-

plies to the human infant, who actively seekslogical studies can thus offer us valuable in-formation about how social factors modulate environmental input, adjusts to the variations

of this input, transforms it with its organizingthe effects of state organization on develop-ment, that is, how early interpersonal experi- properties, and incorporates it into its devel-

oping form. In such reciprocal interchangesences induce the bioenergetic changes thatsupport the growth of brain interconnections the dynamic activity of the developing sys-

tem, in turn, produces changes in the proximaland, therefore, more complex stuctures andemergent functions. environment. As a result of these continuous

self–environment interactions the system es-This latter problem is, of course, a centralfocus of models of self-organization. To fur- tablishes dynamic equilibria both within it-

self, and between itself and its environmentther explore this question, in this paper I willpresent an application of dynamic systems (Michel & Moore, 1995). It is important to

A. N. Schore598

note that in the physical sciences dynamic jectory” that describes the time evolution ofthe system. If the system is driven away fromsystems theories imply that “the environment”

is singularly the physical environment. But in its stationary state, it will tend to return to thatstate; the time it takes to return to stationaritythe case of a living system, one that proceeds

through development to ultimately attain a is a function of the stability of the system.The stability of a system is dependent uponmature form that can pass on its genomes,

these primordial interactions are with the so- its capacity to transition between, and therebyexist within, a range of possible states, andcial environment—others of its species, and

in particular, the primary caregiver. this property is a consequence of its dynamicprocesses.A central tenet of dynamic systems theory

prescribes that in these early transactions the Self-organization, the process whereby or-der and complexity create more order anddeveloping biological system is openly ex-

changing both energy and matter with the en- complexity, proceeds hierachically, as eachlevel of self-organization builds on the levelvironment. Indeed, ongoing development re-

quires an “open” system, one which inputs that precedes it. Different levels of organiza-tion are represented in heirarchical models offree energy from the environment, uses it for

matter–energy transformations, and exports it development, and maturation in infancy isbest characterized by an alternation of rapidin degraded form. As a result of incorporating

the dissipation of energy and matter of its en- development and slower rates, even plateaus,which delimit “stages” (McGuiness, Pri-vironment into itself, the developing system

moves away from equilibrium and remains bram, & Pirnazar, 1990). Developmentalchange results from a series of states of stabil-for periods of time in a state of disequilib-

rium, one that exhibits an increase in negative ity and instability and phase transitions in theattractor landscape that irreversibly alter theentropy. In this manner the flow of energy

through the system creates conditions for trajectory of the system and allow for the or-ganization of new states of matter-dissipativestrong deviations from thermodynamic equi-

librium, and this results in the phenomenon of structures. These “points of bifurcation,”when new states can potentially evolve fromself-organization. When a system is “far-

from-equilibrium” (Prigogine & Stengers, preceding ones, occur in the context of a “mu-tually determining organism–environment in-1984) energy is continually dissipated in the

very process that binds the elements of the teraction” (Schwalbe, 1991). During these in-tervals, the open system, due to increasinglysystem together, allowing the elements to “be-

have in a sychrononous fashion, to couple with complex interconnections within its compo-nents and the creation of feedback mecha-each other through ongoing feedback, and to

act together in macroscopic entities rather than nisms, can now act not only on the output ofan environmental system with which it is in-independent entities” (Lewis, 1995, p. 79).

As the patterns of relations among the teracting, but also iteratively to amplify itsown output, and so it is sensitive to fluctua-components of a self-organizing system be-

come increasingly interconnected and well or- tions of both external and internal processes.Complex systems thus show sensitive depen-dered, it is more capable of maintaining a

coherence of organization in relation to dence on initial conditions, the state of thesystem when fluctuations first initiate change,variations in the environment. Given a partic-

ular organization and a particular environ- and small differences can be amplified intolarge effects over many cycles of iteration.mental context, the system prefers a certain

range of states. A system passes through a These fluctuations drive the system to explorenew states.succession of a finite number of states, but

it must eventually reenter a state that it has Most importantly, environmental perturba-tions that occur during points of bifurcationpreviously encountered. These cycles of con-

tiguous states represent the dynamic attractors create nonlinear breaks in organization anddiscontinuous changes in system states. Ac-of the system, and the path taken by the sys-

tem from one state to another defines a “tra- cording to Schwalbe (1991, p. 276),

Nonlinear right brain 599

Chaos . . . arises at the point of phase transitions, regulation of the organism, which maintainswhen systems are “choosing” between different internal stability and output regulation and en-process structures. What occurs at these points is ables an effective response to external stimuli,that random fluctuations in energy can be ampli- therefore depends on the formation of a dy-fied throughout the entire system so that a new namic model of the external environment.process structure is formed. Chaos in dynamical Self-organizing systems are thus systems thatsystems is thus a product of the same forces that are able capable of generating new internalcreate process structures and give rise to self-or-

representations in response to changing envi-ganization.ronmental conditions.These abstract self-organizational princi-

ples apply in a general way to all livingNonlinearity, the source of rapid change andnovel structure, is thus also the source of po- systems. The next question is, how do these

overarching principles specifically apply totential order and stability. It is now well es-tablished that nonlinearity can produce either ontogeny of the human infant, itself described

as “very nonlinear” (Thelen, 1989)? Schwalbepositive (amplifying) or negative (dampening)feedback, stability or instability, convergence (1991) portrays the human as “a nonlinear dy-

namic system,” an inherently dynamic energy(coupling or entrainment) or divergence(Goerner, 1995). Along these same lines, transformation regime that coevolves with its

environment, one that self-organizes when ex-Jackson (1991), in chaos research in the phys-ical sciences, argues that “entrainment” of a posed to an energy flux. In a scenario that re-

sembles attachment dynamics, he postulatesdynamic system is a precondition to controlof dynamic flows, and that this allows for “hi- that the infant becomes “attuned to” an exter-

nal object in its environment who consistentlyerarchical systems to adapt to environmentalchanges” (p. 4839). Shinbrot, Grebogi, Ott, responds in a stimulating manner to the in-

fant’s spontaneous impulsive energy dissipat-and Yorke (1993) report that chaotic systemsare extremely sensitive to small perturbations ing behaviors.

The concept of energy, central to dynamicand that these tiny feedback perturbationscontrol their trajectories. These researchers systems theory, is rarely used in develop-

mental psychology. In a recent article on theexperimentally demonstrate that small pertur-bations can be used both to stabilize regular self-organization of developmental paths,

Lewis (1995) asks, “What is the best analogydynamic behaviors and to direct chaotic tra-jectories rapidly to a “desired state.” They for energy in psychological systems?” He

points out that the energy flowthrough foralso show that, using only tiny perturbations,one can switch between a rich variety of dy- self-organization has been conceived of as

“information,” an idea that fits well with Har-namical behaviors as circumstances change.Referring to “the advantage of chaos,” they old’s (1986) formulation that information is a

special kind of energy required for the workconclude that “incorporating chaos deliber-ately into practical systems therefore offers of establishing biological order. He then goes

on to argue that information can be definedthe possibility of achieving greater flexibilityin their performance” (p. 411). These findings subjectively as that which is relevant to an in-

dividual’s goals or needs, an idea which ech-fit nicely with Thelen’s (1995) assertion thattimes of instability are essential to give a de- oes recent concepts of emotion as adaptive

functions that guide attention to the most rele-veloping system flexibility to select adaptivecapacities. vant aspects of the environment, and of emo-

tional appraisals that monitor and interpretDeveloping organisms “internalize” envi-ronmental forces by becoming appropriately events in order to determine their significance

to the self. Lewis concludes that there is nostructured in relation to them and by incorpo-rating an internal model of these exogenous better marker of such information than the

emotion that accompanies it, that emotionssignals they develop adaptive homeostaticregulatory mechanisms which allow for sta- amplify fluctuations to act in self-organiza-

tion, and that the processing of relevant infor-bility in the face of external variation. The

A. N. Schore600

mation in the presence of emotion may be namic system of “contingent responsivity”occurs in the context of face-to-face interac-analogous to the flowthrough of energy in a

state of disequilibrium. Stability is a property tions, and it relies heavily upon the processingof visual and auditory (prosodic) informationof interpersonal attractors that maintain their

organization by perpetuating equilibrium as emanating from the most potent source ofstimulation in the infant’s environment—thewell as resolving emotional disequilibrium.

In applying nonlinear systems concepts to mother’s face. The human face is a uniquestimulus whose features display biologicallydevelopment, Lewis emphasizes the salience

of “dyadic self-organization,” which is epito- significant information.Indeed, over the 1st year of life visual ex-mized by the creation of specific forms of

communication between the mother and in- periences play a paramount role in social andemotional development (Preisler, 1995; Wright,fant. When emotion is present in this dyadic

interaction each partner’s behavior is moni- 1991). These face-to-face dialogs create amatch between the expression of arousal-ac-tored by the other, and this results in the cou-

pling between the output of one partner’s loop celerating, positively valenced internal states.For this to happen, the mother must monitorand the input of the other’s to form a larger

feedback configuration. These transactions the infant’s state as well as her own and thenresonate not with the child’s overt behaviorrepresent a flow of interpersonal information

accompanying emotion, and critical fluctua- but with certain qualities of its internal state,such as contour, intensity, and temporal fea-tions, amplified by positive feedback, lead to

disequilibrium and self-organization. Attach- tures. In physics, a property of resonance issympathetic vibration, which is the tendencyment patterns are posited to arise through con-

solidating interpretations (working models) of of one resonance system to enlarge and aug-ment through matching the resonance fre-caretaking contingencies, and such represen-

tations take into account both emotional quency pattern of another resonance system.Dynamically fluctuating moment-to-momentresponses to caretaking fluctuations and

maternal behavioral characteristics. Core at- state sharing represents an organized dialogoccurring within milliseconds, and it acts astachment organizations stabilize with age and

branch into attachment categories, and in this an interactive matrix in which both partnersmatch states and then simultaneously adjustmanner emotional experiences with caregivers

set the course of the individual’s behavioral their social attention, stimulation, and acceler-ating arousal in response to the partner’s sig-style and emotional disposition (Lewis, 1995).nals. In this mutually synchronized attune-ment of emotionally driven facial expression,Nonlinear State Changes and prosodic vocalization, and kinesic behaviors,Organization of Attachment Dynamics the dyad coconstructs a mutual regulatory sys-tem of arousal which contains a “positivelyIn previous work I have proposed that emo-

tional transactions involving synchronized or- amplifying circuit mutually affirming bothpartners” (Wright, 1991).dered patterns of energy transmissions (di-

rected flows of energy) represent the In such facial mirroring transactions (seeFigure 1) the resonating caregiver facilitates afundamental core of the attachment dynamic

(Schore, 1994). This conception, congruent state transition, manifest in a change in pat-terns of “energetic arousal,” and a shift fromwith nonlinear dynamic models, focuses on

reciprocal affective exchanges in which the quiet alertness (point A) into an intensely pos-itive affective state (point F). Stern (1990) de-caregiver psychobiologically regulates changes

in the infant’s state. These interactions occur scribes exchanges of smiles in escalatingoverlapping waves that propel the other intoin sensitive periods of infancy, phases when

energy is high in the infant and the parent for “higher orbit.” At resonance, energy transferfrom the external agent to the resonant systemreceptivity to each other’s cues and for adapt-

ing to each other. The creation of this dy- is maximal (Katsuri, Amtey, & Beall, 1984).

Nonlinear right brain 601

Figure 1. Photographs of a “mirroring” sequence. Mother and infant are seated face to face,looking at each other. At point A, mother shows a “kiss-face,” and infant’s lips are partiallydrawn in, resulting in a tight, sober-faced expression. At point B, mother’s mouth has wid-ened into a slightly positive expression, and infant’s face has relaxed with a hint of wideningin the mouth, also a slightly positive expression. At point C, both mother and infant showa slight smile, further widened at point D. At point E, the infant breaks into a “full gapesmile.” At point F, the infant has shifted the orientation of his head further to his left, andupward, which heightens the evocativeness of the gape-smile. Total time under 3 s (Beebe &Lachmann, 1988).

In accord with complex systems theory, an ous states are experienced as affect responses,and nonlinear psychic bifurcations are mani-environmental perturbation triggers a rapid

and discontinuous change in state, one far- fest as rapid affective shifts.In light of the facts that in these inter-from-equilibrium that leads to the potential

for achieving novel states of temporal stabil- changes the infant’s and mother’s homeostaticsystems are “open” and linked together (Hofer,ity. Schwalbe (1991) posits that the nonlinear

self acts iteratively, so that minor changes, oc- 1990; Kalin, Shelton, & Lynn, 1995) and are“semipermeable to regulation from the other”curring at the right moment, can be amplified

in the system, thus launching it into a qualita- (Pipp, 1993), the transition embedded in thepsychobiological attunement of the dyad in-tively different state. The caregiver is thus

modulating changes in the child’s energetic volves an alteration in the infant’s bodilystate. These interactions increase over the 1ststate, since arousal levels are known to be as-

sociated with changes in metabolic energy. year, since the baby’s ability to adjust theamount of interaction with mother in accor-Indeed, energy shifts are the most basic and

fundamental features of emotion, discontinu- dance with internal states increases with phys-

A. N. Schore602

an intimate relationship, and that they pro-mote the development of cerebral circuits.

Central Role of Bioamines inRegulation of Energy Metabolismof Developing Brain

In her recent writings, Thelen (1995) assertsthat dynamic systems theory needs to be moreclosely tied into a theory of brain develop-ment that addresses the fundamental question,Figure 2. Channels of face-to-face communicationhow is the brain molded through experience?in protoconversation. Protoconversation is medi-Although nonlinear systems theory has beenated by eye-to-eye orientations, vocalizations, hand

gestures, and movements of the arms and head, all used to model brain functions, the problem ofacting in coordination to express interpersonal what causes the infant brain to change, of howawareness and emotions. Adapted from Trevarthen this organization is influenced by the interac-(1993).

tion of genetic programing and environmentalhistory, has not received much attention. Yet,Cicchetti and Tucker (1994) now emphasizethat the identification of the brain’s self-orga-iological and psychological maturity. An es-

sential attachment function is to promote the nizing mechanisms is a primary challenge ofscience and that indeed it may reveal the bestsynchrony or regulation of biological and be-

havioral systems on an organismic level. Da- description of development. These authorsalso point out that certain interactions be-masio (1994) concludes that primordial repre-

sentations of body states are the building tween an “open homeostatic system” and theenvironment are critical to the differentiationblocks and scaffolding of development. The

infant’s core sense of self is bodily based, and of brain tissue and that particular environmen-tal experiences during sensitive periods aresince body processes abide by the laws of

nonlinear dynamics (Goldberger, Rigney, & necessary for the induction of certain develop-mental changes that result from the matura-West, 1990), the emerging self is grounded in

biologically mediated self-organizing proper- tion of the infant brain.This leads to the fundamental questions,ties (Pipp, 1993). Even more specifically, syn-

chronized gaze transactions induce changes in what specific kinds of experiences inducebrain maturation and how does this early ex-the infant’s bodily states by maternal regula-

tion of the child’s autonomic nervous system, perience influence the “social construction”(Eisenberg, 1995) of the human brain? To-and this interactive mechanism represents a

mutual entrainment of the mother’s and in- ward that end I have proposed that attachmentexperiences essentially represent affectivefant’s brains, including a coupling of the acti-

vation of subcortical areas responsible for the transactions in which the caregiver modulateschanges in the infant’s arousal levels andsomatic components of emotion.

In support of this model, Trevarthen (1993) thereby in its energetic state. This is accom-plished by her psychobiological regulation ofargues that the epigenetic program of brain

growth requires brain–brain interaction and neurohormones and catecholaminergic neuro-modulators in the infant’s developing brainoccurs in the context of a traffic of visual and

prosodic auditory signals which induce instant (Hofer, 1990). In the context of face-to-faceinteractions the mother triggers production ofpositive emotional states in both infant and

mother (see Figure 2). The resonance of the corticotropin releasing factor (CRF) in the in-fant’s paraventricular hypothalamus that, indyad ultimately permits the intercoordination

of positive affective brain states. Trevarthen turn, raises plasma concentations of noradren-aline, activates the sympathetic nervous sys-concludes that “the affective regulations of

brain growth” are embedded in the context of tem, increases oxygen consumption and en-

Nonlinear right brain 603

ergy metabolism, and generates a state of regulation of the temporal framework of de-velopmental processes. These neuromodula-emotional excitement. CRF, which controls

endorphin and ACTH production in the ante- tors influence the ontogeny of cortical cir-cuitry and have long-lasting effects onrior pituitary, also activates the ventral teg-

mental system and augments the activity of synaptic plasticity and on biochemical pro-cesses that mediate developmental influencesthe other catecholamine, dopamine, thereby

elevating dopaminergic arousal and an elated (Foote & Morrison, 1987). Their activation ofboth glycogenolysis, a cascade of biochemicalstate in the infant.

These same catecholamines are known to reactions that trigger the release of glucose inconditions of intense activity, and the pentosebe centrally involved in the regulation of

brain metabolic energy levels, morphogene- phosphate pathway, a pathway that meditatesbiosynthetic processes, underscores their pre-sis, and the maturation of cortical areas during

different developmental stages (Berntman, eminent role in the regulation of energy sub-strate availability in the developing brain.Dahlgren, & Siesjo, 1978; Lauder & Krebs,

1986). For this reason, the energy transforma- Catecholamines modulate cerebral circula-tory systems and the blood–brain barrier thattions occurring in attachment bond formation

are vitally important for the infant’s continu- delivers and exports metabolic substrate to thebrain, thereby regulating the responsivity ofing neurobiological development. Since the

ascending bioaminergic “reticular” systems large areas of the brain to inputs in a coordi-nated manner (see Schore, 1994 for a detailedthat are responsible for various states of

arousal are in an intense state of active growth discussion). The growth and organization ofthe brain is highly dependent upon the contin-in infancy, the regulatory transactions embed-

ded in the emotional relationship are occur- ued availability of substrate, and in postnatalperiods its production of energy shifts fromring at a time when the infant’s circuitry of

the biological hardware of arousal is expand- anaerobic to aerobic oxidative metabolism,thereby enabling a significant increase in out-ing. In fact, there are specific postnatal critical

periods and developmental sequences for the put that can sustain the very large energy re-quirement of brain cells for differentiation andappearance of the biogenic amines dopamine

and noradrenaline. Central catecholaminergic the formation of connections. The brain’smain metabolic fuel is glucose, which in theneurons undergo an accelerated development

in mammalian infancy, and their proliferating presence of oxygen undergoes complete com-bustion to CO2 and H2O:axonal terminals hyperinnervate distant corti-

cal territories. In these same periods varioustypes of regional catecholaminergic receptors C6H12O6 + 6O2 → 6CO2 + 6H2O + energy. (1)are amplified, especially the D1 dopamine re-ceptor that is found throughout the prefrontal The free energy liberated in this exergonic re-

action is partially trapped as adenosine tri-cortex and limbic system associated with mem-ory, learning, and cognitive processing (Huang, phosphate (ATP), the main source of energy

in living matter, in glycolysis and oxidativeZhou, Chase, Gasella, Aronin, & DiFiglia,1992), as well as the beta noradrenergic re- phosphorylation (Erecinska & Silver, 1989).

ATP is generated both in glycolysis, a processceptor that is activated in states of emotionalexcitement (Cahill, Prins, Weber, & Mc- located in Na+,K+-ATPase activity, especially

at the plasma membrane surrounding the cellGaugh, 1994). These events are experience-dependent, and they account for the evolution and in synaptic nerve endings (Erecinska,

Nelson, & Silver, 1996), and in oxidativeof an increasing tolerance for higher levels ofarousal over the course of the 1st year. phosphorylation, the preeminent supplier of

ATP in biological systems. This latter processDuring early critical periods, biogenicamines, the same agents that regulate emotion occurs in mitochondria and reflects the activ-

ity of cytochrome oxidase, the enzyme thatand motivation throughout the life span, playan important role in the responsiveness of the supports the high aerobic energy metabolism

of the brain (Wong–Riley, 1989). The activitycortex to environmental stimulation and in the

A. N. Schore604

of these enzymes is coordinated (Hevner, mother–infant affective transactions, activatesexcitatory NMDA receptors (Knapp, Schmidt, &Duff, & Wong–Riley, 1992) and influenced

by catecholamines (Van der Krogt & Bel- Dowling, 1990) and modulates the excitabil-ity of prefrontal neurons by altering dendriticfroid, 1980), and since they act as regulators,

the effects of their action involve large ampli- spine responses to excitatory inputs (Smiley,Levey, Ciliax, & Goldman–Rakic, 1994). Ex-fication factors. The major inactivation of

biogenic amines is performed by monoamine citatory sensory input, including visual input,is required for the increases in mitochondrialoxidase, an enzyme located solely in mito-

chondria. cytochrome oxidase-driven oxidative metabo-lism in spines of growing dendrites of the de-Levels of Na+,K+-ATPase increase dramati-

cally in early development during periods of veloping cerebral cortex (Wong–Riley, 1979).Most intriguingly, catecholamines initiateneuronal arborization (Bertoni & Siegel,

1978), and cytochrome oxidase activity, regu- protein synthesis and the maturation of energytransduction in mitochondria (Houstek, Ko-lated by oxygen concentrations, increases and

peaks at the time of most rapid growth and pecky, Baudysova, Janikova, Pavelka, & Kle-ment, 1990), and infant animals exposed tomaturation (Wong–Riley, 1989). During the

critical period of a brain region, growth in early environments that allow for social expe-riences show larger mitochondrial popula-neurons occurs essentially in dendrites, and is

manifest in heightened levels of synaptogene- tions, an indicator of metabolic energy activ-ity, as well as increased dendritic volume, insis. Na+,K+-ATPase and cytochrome oxidase

are heightened in dendrites, and this accounts developing cortical areas (Sirevaag & Green-ough, 1987).for the fact that dendritic metabolism makes

the largest contribution to the metabolic activ-ity of the brain. In postnatal development mi-tochondria are associated with the presynaptic Energy-Dependent Imprinting ofand postsynaptic processes of developing syn- Neural Circuits During Criticalapses. In these same time periods catechola- Periods of Infancymines induce dynamic changes in the shapeand branching patterns of dendrites and the A central tenet of dynamic systems theory

holds that at particular critical moments, agrowth of dendritic spines. These spines havethe greatest energy requirements and density flow of energy allows the components of a

self-organizing system to become increas-of mitochondria in the brain, and they act aspotential sites of synaptic contact which mod- ingly interconnected, and in this manner or-

ganismic form is constructed in develop-ulate rapid changes in the nervous systemthroughout the course of its development. mental processes. These moments occur in

instances of imprinting, the very rapid formIt is now well established that the size andcomplexity of dendritic arbors increase in de- of learning that irreversibly stamps early ex-

perience upon the developing nervous systemvelopment and that dendritic growth and syn-aptogenesis of the postnatally developing and mediates attachment bond formation. It is

now thought that a stimulus which elicits abrain is “experience-sensitive.” Indeed, theneurodevelopmental processes of dendritic high level of catecholamine-generated arousal

facilitates the imprinting process and exertsproliferation and synaptogenesis which are re-sponsible for postnatal brain growth are criti- an enduring influence on neural development

(a perfect description of the emotionally ex-cally influenced by events at the interpersonaland intrapersonal levels. As mentioned, the pressive face of the attachment object), and

that certain types of early learning experi-events embedded in interpersonal transactionscan be very fast acting, yet structure-inducing. ences associated with new levels of arousal

lead to rapid increases in the volume of hemi-Indeed, modifications of dendritic spines oc-cur “within minutes of a stimulus train that spheric blood flow. Both imprinting and

arousal are associated with increased meta-lasts for a fraction of a second” (Lynch, 1986,p. 7). Dopamine, regulated within rapid bolic activity, and both are regulated by cate-

Nonlinear right brain 605

cholamines, agents that have pronounced ef- proposed that the onset of a critical period ofgrowth in a differentiating brain region is de-fects on cerebral oxidative energy metabolism

and cerebral blood flow. fined by a sudden switch from anaerobic toaerobic energy metabolism. A mature neuronDuring very early development, the neona-

tal cerebral metabolic rate that sustains early has greater energy-consuming demands thanan immature neuron, and this transformationcortical function is very low. But as infancy

proceeds, blood flow, known to correlate with is expressed, at the intracellular level, by areplication of the mitochondrial genome, achanges in arousal, and to be an indicator

of regional oxidative metabolism, rises to rapid multiplication of mitochondrial biogene-sis, an elevation of environmentally regulatedmaximal levels and then declines (Kennedy,

Grave, Jehle, & Sokoloff, 1972). Kennedy mitochondrial protein synthesis, and a signifi-cant increase in cytochrome oxidase levels.suggests that the peak elevation in early in-

fancy specifically reflects the increased en- These fast onset, discontinuous changes thatoccur within “the period of rapid mitochon-ergy demands associated with biosynthetic

processes essential for growth and develop- drial prolferation” (Pysh, 1970) result in anaugmentation of cellular energy metabolism,ment of differentiating cortical structures and

their emergent functions. In this period of in- since glycolysis alone only produces 2 molsof ATP per mol of glucose, while oxidativetense growth, the metabolic activity that sup-

ports this growth is heightened, so much so phosphorylation produces 36 (Erecinska &Silver, 1989).that the young child’s cerebral metabolic rate

consumes one-half of the total body oxygen The increased number and onset of aerobicmetabolism in mitochondrial populationsconsumption (Kennedy & Sokoloff, 1957).

In a similar dynamic scenario, Purves and within maturing regions of the infant’s devel-oping brain allow for the generation of signif-LaMantia (1990) demonstrate that mitochon-

drial cytochrome oxidase-rich zones in the ce- icantly higher levels of biological energy thatare available for “morphogenesis,” the gener-rebral cortex increase in number in develop-

ment, and propose that the pattern of high ation of new forms during growth and devel-opment, that is for the processing of geneticmetabolic activity in these areas demarcates

modular circuits. They further suggest that information, biosynthesis, and the transport ofbuilding blocks to their final destination (Har-novel circuits are constructed in a critical pe-

riod of postnatal life, that modular and pro- old, 1986). The transient increase in the divi-sion and production of new mitochondriacessing units are added progressively during

the period of brain growth and maturation, peaks just when the dendrites are growingout, a fact that may account for the findingand that modular circuit formation wanes in

the later stages of postnatal development. that in a developing system, postsynaptic neu-rons respond initially to excitatory inputs byThey conclude that critical periods, “epochs

in early life when the brain is particularly sen- heightening their energy metabolism (Mjaat-vedt & Wong–Riley, 1988). I suggest thatsitive to the effects of experience” represent

the normal duration of the construction of cy- during the critical period growth of a particu-lar region, the peaks of heightened energy me-tochrome oxidase-labeled circuits.

Indeed the dramatic transformations of en- tabolism described by Wong–Riley, Purvesand LaMantia, and Kennedy represent a coor-ergy production which occur in particular por-

tions of the maturing nervous system during dinated flow of energy through the compo-nents of a system that is now synapticallyspecific postnatal temporal intervals represent

the physiological basis of developmental coupling into a circuit. This directed energy iscontinually dissipated in the very process thatstage and critical period phenomena, and

these events allow for the onset of increasing binds the elements of the system together; thatis, it allows for the coordinated onset of mito-complexity of structure and efficiency and in-

tegration of function, just as described by dy- chondrial energy metabolism among the neu-rons, glia, and endothelial cells within con-namic systems theory. In recent writings

(Schore, 1994, see chapters 11 and 36) I have temporaneously differentiating cortical columns.

A. N. Schore606

Most importantly, the dramatic increase in the enzyme that degrades GABA, is located inthis organelle. Overall, these phenomena arenumber of mitochondria during a critical pe-

riod results in larger and larger flows of more accurately described by the second lawof thermodynamics, which deals with the effi-energy within more and more interconnected

elements that can be used for self-organiza- ciency with which energy is used and theamount of useful work to which the energy istional processes.

Since these bioenergetic transformations put, rather than to the first law, the conserva-tion of energy.are coordinated over long distances, they also

underlie the critical period construction of a In light of the facts that energy metabolismpeaks in a critical period of a developing brainneural circuit—a self-contained neuronal net-

work which sustains a nerve impulse by chan- region when dendrites are growing and neu-rons are attaining a new state of organization,neling it repeatedly through the same net-

work. In a discussion of the stabilization of and that dendritic spines have the greatest en-ergy requirements in the brain, I would char-excitatory Hebbian cell assemblies, Singer

(1986) suggests that pathways are formed be- acterize their local cellular environment atthis specific time as a “far-from-equilibriumtween elements that have a high probability of

being active at the same time. This selection system.” It is now held that energy-regulatingbioamines modulate ion channels in dendritesprocess serves to develop assemblies of recip-

rocally coupled neurons that allow for the or- and that excitatory events occurring in den-drites within a “narrow time window” pro-ganization of a reverberating circuit. He also

states that these experience-dependent pro- duce a “much bigger response” than outsidethis window, thereby allowing for interactionscesses rely both on cortical sensory process-

ing of information from the “outer” world and among synapses to be “highly nonlinear”(Johnston, Magee, Colbert, & Christie, 1996).on internally generated signals involving cate-

cholamines from the reticular formation Expanding upon these ideas, I suggest that al-though dendritic spines represent a unique sitewhich reflect the central state of the organism

during a postnatal period. for receiving communications from othercells, these points of interface with the localHudspeth and Pribram (1992) propose that

a maturation period has three phases: an ac- environment, especially in critical periods,also potentially expose the neuron to a statecelerating edge that reflects a changing state

in the brain region; a peak that reflects the of “oxidative stress,” thereby making the cellvulnerable to excitotoxic “apoptotic” or “pro-attainment of a new state; and a decelerating

edge, in which a stable equilibrium within the gramed cell death” (Margolis, Chuang, &Post, 1994).state is established. I deduce that the peak

phase is identical to the metabolic peak de- Apoptosis plays a crucial role in the earlydevelopment and growth regulation of livingscribed above, and that in its critical period

of maturation a particular brain region is an systems. This same mechanism may underliethe developmental process of circuit pruning,object of an energy flux which creates condi-

tions for strong deviations from thermody- the selective loss of connections and redistri-butions of inputs that allow for the appearancenamic equilibrium that result in self-organiza-

tion. The last phase may be related to the fact of an emergent function. Regressive eventssuch as cell death and the elimination of longthat in a developing system neurons initially

receive excitatory inputs that heighten energy axon collaterals and dendritic processes areessential mechanisms of brain maturation. Ametabolism followed by inhibitory inputs that

lower metabolism. This developmental shift large body of evidence supports the principlethat cortical networks are generated by a ge-from excitation to inhibition may reflect an

early overexpression of excitatory NMDA netically programed initial overabundant pro-duction of synaptic connections, which is thenglutamate receptors to later maturing inhibi-

tory GABAergic systems. Glutamate is me- followed by a process of competitive interac-tion to select those connections that are mosttabolized in mitochondria, and GABA-T, the

Nonlinear right brain 607

effectively entrained to environmental informa- Organization of Regulatory System inOrbitofrontal Cortex That Manifeststion. “Parcellation,” the activity-dependent fine

tuning of connections and winnowing of sur- Chaotic Dynamicsplus circuitry, dominates the third maturationalphase described by Hudspeth and Pribram. According to chaos theory, the stabilization of

reverberating circuits in early developmentParcellation is responsible for the selectiveloss of synapses that determines the microcir- allows for the organization of a network that

can amplify minor fluctuations over cycles ofcuitry within a cortical region, and this samemechanism of functional segregation also iteration, and thereby influences the system’s

trajectory. This reexcitational activity laun-allows the developing brain to become in-creasingly complex, a property of a self-orga- ches the system into a different state, but it

also facilitates the “persistence” of a memorynizing system. Furthermore, this process hasbeen described as analogous to natural selec- trace, an important advance, since “attractors

might be thought of as either as memoriestion. Changeux and Dehaene (1989) point outthat the “Darwinian” selective stabilization of held by the neural network or as concepts”

(Kaufmann, 1993, p. 228). As previouslysurviving synapses that have functional sig-nificance in a particular environment occurs mentioned, these attractors maintain the sys-

tem’s organization by acting as adaptive ho-in cortical areas during postnatal sensitive pe-riods. These findings imply that maternal be- meostatic regulatory mechanisms that allow

for stability in the face of external variation.havior, the preeminent source of environmen-tal information for the infant, functions as an Of particular importance to the regulation of

nonlinear emotional states are cortical–sub-agent of natural selection that shapes the tra-jectory of the infant’s emerging self. They cortical circuits, especially those that directly

link cortical areas that process current infor-may also bear upon the mechanism of “mater-nal effects” (Bernardo, 1996), the influence of mation about changes in the external social

environment with subcortical informationthe mother’s experiences on her progeny’s de-velopment and ability to adapt to its environ- about concurrent alterations in internal bodily

states.ment.Studies of the infant brain thus have direct In earliest human infancy, before most ar-

eas of the cortex are even myelinated, limbicimplications for a more precise elucidation ofdynamic systems theories. A fundamental areas of the amygdala are dominant in the

processing of emotional information. A criti-postulate of this model holds that a conditionof chaos exists when a system must move cal period for the maturation of particular rap-

idly developing temporolimbic and corticalfrom a previously ordered, yet obsolete adap-tive state to a more flexible state in order to association areas onsets in the middle of the

1st year. By the end of this year the orbitoin-be better adapted to novel aspects of a cur-rently changing environment. The term “self- sular region of the prefrontal cortex (see Fig-

ure 3), an area that contains neurons that fireorganization” can be imprecise and mislead-ing, because first, despite the implications of in response to faces, first become preemi-

nently involved in the processing of interper-the two words used to describe this process,self-organization occurs in interaction with sonal signals necessary for the initiation of so-

cial interactions and in the regulation ofanother self—it is not monadic but dyadic.And second, the organization of brain systems arousal and body states, properties that ac-

count for its central involvement in attach-does not involve a simple pattern of incre-ments but rather changes in organization. De- ment neurobiology. The orbitofrontal system

matures in the last half of the 2nd year, a wa-velopment, the process of self-assembly, thusinvolves both progressive and regressive phe- tershed time for the appearance of a number

of adaptive capacities. These advances reflectnomena, and is best characterized as a se-quence of processes of organization, disorga- the role of the frontal lobe in the development

of infant self-regulatory behavior (Dawson,nization, and reorganization.

A. N. Schore608

limbic dopamine neurons in ventral tegmentalareas of the anterior reticular formation, andto subcortical drive centers in the paraventric-ular hypothalamus that are associated with thesympathetic branch of the autonomic nervoussystem. This excitatory limbic circuit, theventral tegmental limbic forebrain–midbraincircuit, is involved with the generation of pos-itively valenced states associated with motiva-tional reward. Orbitofrontal regions also sendaxons onto subcortical targets in parasympa-thetic autonomic areas of the hypothalamus,and to noradrenergic neurons in the medullarysolitary nucleus and the vagal complex in thebrain stem caudal reticular formation, thereby

Figure 3. Boundaries of functional zones of the completing the organization of another limbichuman cerebral cortex, showing the orbital andcircuit, the lateral tegmental limbic forebrain–dorsolateral prefrontal areas (from Kolb & Whis-midbrain circuit that activates the onset of anhaw, 1990).inhibitory, negatively valenced state (seeSchore, 1994).1994) and are relevant to Cicchetti and Tuck-

er’s (1994) assertion that the homeostatic, The orbital corticolimbic system, alongwith the amygdala, insular cortex, and ante-self-regulating structures of the mind are the

major stabilities in the chaotic dynamics of rior cingulate, is a component of the “rostrallimbic system” (Devinsky, Morrell, & Vogt,psychological and neural development. Be-

cause orbital activity is essentially implicated 1995). But even more, it sits at the hierarchi-cal apex of the emotion-generating limbicin maintaining organismic homeostasis, the

operational nature of this prefrontal cortex is system, and regulates not only anterior tempo-ral and amygdala activity, but indeed all corti-best described as a nonlinear dynamic system.

The functional properties of this structural cal and subcortical components of both theexcitatory and inhibitory reverberating cir-system can only be understood in reference

to its unique neuroanatomical characteristics. cuits of the limbic system. But in addition, itacts as a major center of CNS hierarchicalThis ventromedial frontal cortex is “hidden”

in the ventral (areas 11–14 and 47) and medial control over the energy-expending sympa-thetic and energy-conserving parasympathetic(areas 24, 25, and 32) surfaces of the prefron-

tal lobe (Price, Carmichael, & Drevets, 1996). branches of the ANS, thereby regulating, re-spectively, ergotropic high arousal and tro-Because of its location at the interface of cor-

tex and subcortex (see Figure 4), the orbital photropic low arousal bodily states (Gellhorn,1970). With such autonomic connections, itprefrontal cortex acts as a “convergence zone”

and is one of the few brain regions that is plays an important cortical role in both thenonlinear mechanisms of visceral regulation“privy to signals about virtually any activity

taking place in our beings’ mind or body at (Skinner, Molnar, Vybiral, & Mitra, 1992)and the feedback from bodily systems, whatany given time” (Damasio, 1994, p. 181). In

addition to receiving input from all sensory Damasio (1994) calls “somatic markers.”These reciprocal connections with autonomicassociation areas of the posterior cortex as

well as outputs to motor areas in the anterior areas allow for an essential orbitofrontal rolein the control of emotional behavior (Price,cortex and ventral striatum, it uniquely pro-

jects extensive pathways to limbic areas in the Carmichael, & Drevets, 1996), the repesenta-tion of highly integrated information on theanterior cingulate, insula, temporal pole, cen-

tral nucleus of the amygdala, and olfactory ar- organismic state (Tucker, 1992), and the mod-ulation of energy balance (McGregor &eas, to glutamate responsive N-methyl-D-

aspartate (NMDA) receptors of mesocortico- Atrens, 1991).

Nonlinear right brain 609

Figure 4. Relationships of brain stem structures to the orbital surface of the right hemisphere(from Smith, 1981).

By being directly connected into heteromo- of life experiences are capable of influencingvirtually all, if not all, regulatory mechanismsdal areas of the cortex as well as into both

limbic circuits, the sensory perception of an in the body” (Wolf, 1995, p. 90).In such organism–environment interactionsenvironmental perturbation can be associated

with the adaptive switching of bioaminergic– there is a sensitive dependence on initial con-ditions, and these heightened affective mo-peptidergic regulated energy-expending and

energy-conserving bodily states in response to ments represent “points of bifurcation” of thepotential activation of the two limbic circuits.changes (or expected changes) in the external

environment that are appraised to be person- Marder, Hooper, and Eisen (1987) demon-strate that “a given circuit might easily ex-ally meaningful (Schore, in press-a). These

rapid acting orbitofontal appraisals of the so- press a variety of states, depending on thepresence or absence of one or more peptidescial environment are accomplished at levels

beneath awareness by a visual and auditory or amines” (p. 223). Not only the output ofeach circuit, but also the interaction betweenscanning of information emanating from an

emotionally expressive face, and they act as the circuits is influenced by one or more bioa-minergic neurotransmitters, thereby allowingnonconscious biases that guide behavior be-

fore conscious knowledge does (Bechara, Da- for an adaptive flexible control of multiplestates or output patterns. Indeed, in the orbito-masio, Tranel, & Damasio, 1997). The para-

limbic orbitofrontal cortex performs a frontal areas, dopamine excites and noradren-aline inhibits neuronal activity (Aou, Oomura,“valence tagging” function, in which percep-

tions receive a positive or negative affective Nishino, Inokuchi, & Mizuno, 1983). Mender(1994) points out that in a competitive sys-charge. The orbitofrontal system, the “admin-

istrator of the basolimbic forebrain circuitry” tem, steep gain increases in response to stimu-lus input, combined with arousal, can create(Nelson, 1994), is a central component of the

mechanism by which “forebrain circuits con- explosive bursts of neural activity and hencediscontinuous jumps between discrete aggre-cerned with the recognition and interpretation

A. N. Schore610

gate states of neuronal networks. As a result, aspects of these nonlinear phenomena isstressed by Hofer (1990, p. 74):distributed aggregates of neurons can shift

abruptly and simultaneously from one com-plex activity pattern to another in response to To accomplish various age-specific tasks, the brainthe smallest of inputs. It is interesting to note must be able to shift from one state of functionalthat dopamine neurons involved in emotional organization to another and thus form one mode ofstates show a “nonlinear” relationship be- information processing to others within an essen-tween impulse flow and dopamine release, tially modular structure. These organized states

constitute an important component of motivationaland shift from single spike to “burst firing”systems, and they can be considered to provide thein response to environmental stimuli that areneural substrates of affect—both the internal expe-associated with a quick behavioral reactionrience of affect and the communicative aspects that(Gonon, 1988), and that this effect is inducedare embedded in the form and patterning of the be-by medial prefrontal activity (Gariano &havior that is produced during these states.Groves, 1988).

Bertalanffy (1974) asserts that a smallchange in an anterior “higher” controlling The activity of this prefrontal system is re-

sponsible for the regulation of motivationalcenter “may by way of amplification mecha-nisms cause large changes in the total system. states and the adjustment or correction emo-

tional responses. It is specialized for generat-In this way a hierarchical order of parts orprocesses may be established” (p. 1104). I ing and storing cognitive interactive represen-

tations (internal working models) that containsuggest that the orbitofrontal cortex representsthis controlling center and that it is intimately information about state transitions, and for

physiologically coding that state changes as-involved in the mechanism by which affectacts as an “analog amplifier” that extends the sociated with homeostatic disruptions will be

set right. The infant’s memory representationduration of whatever activates it (Tomkins,1984). In accord with chaos theory, “Tiny dif- includes not only details of the learning cues

of events in the external environment, but alsoferences in input could quickly become over-whelming differences in output” (Gleick, of reactions in his internal state to changes in

the external environment. The dampening of1987, p. 8). These “tiny differences” refer toextremely brief events perceived at levels be- emotional discomfort and the performance of

previously rewarded actions are now thoughtlow awareness—although facially expressedemotions can be appraised within 30 ms, to be specifically stored in infant procedural

memory (Meltzoff, 1995). Regulated emo-spontaneously expressed within seconds, andcontinue to amplify within less than a half tional states represent desired attractors that

maintain self-organization by perpetuatingminute, it can take hours, or days, or evenweeks or longer for certain personalities expe- emotional equilibrium and resolving emo-

tional disequilibrium. Chaotic variability inriencing extremely intense negative emotionto get back to a “normal” state again. brain self-regulatory activity is thus necessary

for flexibility and adaptability in a changingChaotic behavior within the excitatory andinhibitory limbic circuits is thus expressed in environment. According to Ciompi (1991) un-

der certain conditions feedback processes insudden psychobiological state transitions. Or-bitofrontal activity is associated with affective “affective cognitive systems” are capable of

“provoking sudden non-linear jumps, farshifts, the alteration of behavior in responseto fluctuations in the emotional significance away from equilibrium, leading to chaotic

conditions or to the formation of new ‘dissi-of stimuli (Dias, Robbins, & Roberts, 1996).In optimal frontolimbic operations, these pative structures’” (p. 98). Very recent work

indicates that the orbitofrontal system is spe-shifts from one emotional state to another areare experienced as rhythms in feeling states cialized for “cognitive–emotional interac-

tions” (Barbas, 1995) and that neurons in theand are fluid and smooth, a flexible capacityof a coherent dynamic system. The adaptive right prefrontal cortex with balanced excit-

Nonlinear right brain 611

atory and inhibitory inputs show chaotic be- throughout the life span (Sergent, Ohta, &MacDonald, 1992).havior (van Vreeswijk & Sompolinsky, 1996).Descending projections from the prefrontal

cortex to subcortical structures are known toRight Brain as Nonlinear System mature during infancy, and the “primitive”

right hemisphere, more than the left, hasThe fact that the orbital prefrontal area is ex- dense reciprocal interconnections with limbicpanded in the right hemisphere (in contrast to and subcortical structures, and contains an in-the later maturing nonlimbic dorsolateral pre- creased emphasis on paralimbic networks.frontal area which is larger in the left—White, These reciprocal right frontal–subcortical con-Lucas, Richards, & Purves, 1994) has been nections, especially with bioaminergic andsuggested to account for the dominance of hypothalamic subcortical nuclei, account forthis hemisphere in the processing of emo- the unique contribution of the right hemi-tional information (Falk, Hildebolt, Cheverud, sphere in regulating homeostasis and modu-Vannier, Helmkamp, & Konigsberg, 1990). lating physiological state in response to inter-The early developing right cerebral cortex nal and external feedback. The representationplays an important role in the processing of of visceral and somatic states is under primaryindividual faces early in life, in the infant’s control of the right hemisphere, and the so-recognition of arousal-inducing maternal fa- matic marker mechanism, tuned by criticalcial affective expressions, and in its response learning interactions in development, is moreto the prosody of motherese. In describing the connected into the right ventromedial area.greater involvement of the right hemisphere Wittling and Pfluger (1990) conclude that thein infancy, Semrud–Clikeman and Hynd right hemisphere is dominant for “the meta-(1990, p. 198) point out that control of fundamental physiological and en-

docrinological functions whose primary con-The emotional experience of the infant develops trol centers are located in subcortical regionsthrough the sounds, images, and pictures that con- of the brain” (p. 260). This cortical asymme-stitute much of an infant’s early learning experi- try is an extension of an autonomic asymme-ence, and are disproportionately stored or pro- try—at all levels of the nervous system thecessed in the right hemisphere during the formative right side of the brain stem provides the pri-stages of brain ontogeny. mary central regulation of homeostasis and

physiological reactivity (Porges, Doussard–Roosevelt, & Maiti, 1994).Indeed, the right hemisphere is centrally in-

volved in in human bonding and attachment Expanding upon these neurophysiologicaland neuroanatomical relationships, Porges(Henry, 1993) and in the development of re-

ciprocal interactions within the mother–infant demonstrates that the right vagus is involvedin the regulation of emotion and communica-regulatory system (Schore, 1994, 1997). In

earlier work I presented a substantial body of tion. He also discusses the relationship be-tween “shifts” in emotion regulation and oxy-multidisciplinary evidence which indicates

that the high intensity affective communica- gen demands within the ANS. In his mostrecent work (1995) he presents a neuroana-tions that culminate in the development of the

attachment system are essentially right-hemi- tomical schema in which he proposes that theinput site into this right brain circuit of emo-sphere-to-right-hemisphere arousal-regulating

energy transmissions between the primary tional regulation is the nucleus of the solitarytract. This site, in turn, is fed by unnamedcaregiver and infant. Attachment dynamics

continue in ongoing development, and the higher central structures that promote eitherimmediate mobilization of energy resourcesventromedial region of the right cortex that

neurobiologically mediates these dynamics or calming. I deduce that the orbitofrontal cor-tex and the central amygdala, which both sendplays a crucial role in the processing of infor-

mation emanating from the human face axons directly into the noradrenergic neurons

A. N. Schore612

of the nucleus of the solitary tract and into the (Wittling & Schweiger, 1993). In line with theprinciple that the right cortex operates in con-hypothalamus, are these structures. Indeed,

orbitofrontal–vagal interconnections are dem- junction with a frontal system that is involvedin modulating the emotional valence of expe-onstrated in studies showing that vagal stimu-

lation induces a cortical evoked response only rience (Heller, 1993), I suggest that upon itsmaturation in the middle of the 2nd year, thein the orbitoinsular cortex, and that orbito-

frontal stimulation triggers an almost instanta- orbitofrontal area of the right hemisphere actsas an “executive control system” for the entireneous inhibition of gastrointestinal motility,

respiratory movements, and somatic locomo- right brain.These findings bear upon an ongong de-tor activity, and a dramatic precipitous fall in

blood pressure (see Schore, 1994). bate concerning hemispheric asymmetry andthe regulation of emotions. There is now gen-In other words, Porges’ right brain circuit

of emotion regulation is identical to the inhib- eral agreement that right cortical posterior as-sociation regions are centrally involved in theitory lateral tegmental noradrenergic limbic

circuit that is hierarchically dominated by the perception of all emotional information. How-ever, with regard to the production and expe-right orbitofrontal cortex. As opposed to sym-

pathetically driven “fight–flight” active cop- rience and thereby the regulation of emotion,there is a controversy as to whether the righting strategies, parasympathetically mediated

passive coping mechanisms expressed in im- hemisphere regulates all emotions or the rightis specialized for negative and the left for pos-mobility and withdrawal allow for conserva-

tion-withdrawal, the capacity that improves itive emotions. In general, studies examininghemispheric lateralization for emotional non-survival efficiency through inactive disen-

gagement and unresponsiveness to environ- verbal stimuli (e.g., faces) have provided sup-port for the right hemispheric model of emo-mental input in order “to conserve resources.”

In contrast to “problem focused coping,” tional lateralization (Ali & Cimino, 1997), afinding that fits with the conception that thewhich entails direct action on the self or on

the environment to remove the source of right hemisphere contains a “nonverbal affectlexicon,” a vocabulary for nonverbal affectivestress, this “emotion focused coping” is di-

rected toward the reduction of the emotional signals such as facial expressions, gestures,and prosody (Bowers, Bauer, & Heilman,impact of stress through psychological pro-

cesses (Folkman & Lazarus, 1980). 1993). Conditioned autonomic responses aftersubliminal presentations of facial expressionsWith regard to the other ventral tegmental

dopaminergic limbic circuit, psychopharma- only occur when faces are presented to theright hemisphere (Johnsen & Hugdahl, 1991),cological research shows that emotionally

stressful experiences result in greater dopa- clearly implying that future studies should usetachistoscopic facial stimuli. Furthermore, theminergic activation of the right over the left

prefrontal cortex (Fitzgerald, Kewller, Glick, & majority of these studies have been done withadults, but recent infant studies (e.g., Nass &Carlson, 1989). In a recent study of the meso-

cortical dopaminergic system, the authors Koch, 1991) report that the right hemisphereplays a crucial role in mediating emotionalconclude that the right cortex is at the top of

a hierarchy for the processing of prolonged expression from a very early point in develop-ment (note in earlier Figure 1, at point F, inemotionally stressful inputs, and that endoge-

nous dopaminergic modulation facilitates the high arousal elated state, the infant turnsthe head to the left, indicating right hemi-adaptive responses (Sullivan & Szechtman,

1995). Furthermore, they posit that under in- spheric activation), and that infants with rightposterior brain damage show a persistent defi-tense inputs, a left to right shift occurs in in-

trinsic neural activity. These ideas correspond cit in the expression of positive affect (Reilly,Stiles, Larsen, & Trauner, 1995). These latterwith the assertion that this “nondominant”

hemisphere plays a central role in the control researchers conclude that the development ofinfant emotions represent “primitives” of af-of vital functions supporting survival and en-

abling the organism to cope with stressors fective communication.

Nonlinear right brain 613

It is important to note that emotions have, left hemipsheric-driven counterparts, anxiety,interest, enjoyment, and guilt.in addition to a valence (hedonic) dimension,

an intensity or arousal (energetic) dimension. The right cortex is also specialized forglobally directed attention, holistic analysis,Many of the “primary” emotions are ergotrop-

ic-dominant, energy-expending high arousal, or and the processing of novel information. Asopposed to the left hemisphere’s “linear” con-trophotropic-dominant, energy-conserving low

arousal affects, and these “primitive” affects secutive analysis of information (Tucker,1981), the processing style of the right hemi-appear early in development, arise automati-

cally, are expressed in facial movements, and sphere has been described as “nonlinear”based on multiple converging determinantsare correlated with differentiable ANS activ-

ity. Due to the lateralization of catecholamin- rather than on a single causal chain (Galin,1974). I conclude that the orbitofrontal cortex,ergic systems in the right hemisphere, it is

dominant in the regulation of arousal and is especially in the right brain, is particularlysuited to amplify appraisals of short-acting,more closely associated with regulation of

heart rate than the left. This hemisphere is small fluctuations of initial conditions intolarger effects, and that it is primarily activatedspecialized for processing the autonomic cor-

relates of emotional arousal (Spence, Sha- in “far-from-equilibrium” states of heightenedergotropic and/or trophotropic emotional arous-piro, & Zaidel, 1996), and activation of the

right orbitofrontal area occurs during classical al that create a potential for achieving novelstates and a new stability.conditioning of an emotional response, the

learning of the relationship between eventsthat allows the organism to represent its envi-ronment (Hugdahl et al., 1995). The structural Critical Period Gene–Environmentand functional qualities of the right cortex, Interactions and the Development of awhich has a higher metabolic rate than the Vulnerability to Psychopathologyleft, thus account for its essential role inhighly arousing emotional processes. The development, in the first 2 years of life,

of a right hemispheric dynamic system thatThe developmental approach presentedhere is compatible with a model in which the adaptively regulates psychobiological states is

a product of the interaction of genetic systemsearly maturing right hemisphere modulates allnonverbal “primary” emotions, regardless of and early experience. Recent transactional

models view the organization of brain systemsvalence, while the later maturing left (whichdoes not begin it growth spurt until the last as an outcome of interaction between geneti-

cally coded programs for the formation ofhalf of the 2nd year) modulates verbal “so-cial” emotions and enhances positive and in- structures and connections among structures

and environmental influence (Fox, Calkins, &hibits negative emotional behavior (Ross,Hohman, & Buck, 1994). It also supports the Bell, 1994). The onset and offset of sensitive

periods, “unique windows of organism–envir-views that the right hemisphere mediates plea-sure and pain and the more intrinsically primi- onment interaction,” are now attributed to the

activation and expression of families of pro-tive emotions, and that although the left cor-tex acts to inhibit emotional expression gramed genes which synchronously turn on

and off during infancy, thereby controlling thegenerated in the limbic areas of the right halfof the brain, the right brain contains a circuit transient enhanced expression of enzymes of

biosynthetic pathways which allow for growthof emotion regulation that is involved in themodulation of “primary” emotions and “in- in particular brain regions. In light of the es-

tablished principles that early postnatal devel-tense emotional-homeostatic processes” (Porges,1995). Thus, the experience and regulation of opment represents an experiential shaping of

genetic potential (Kendler & Eaves, 1986)affects mediated by extremes of arousal, bothhigh, such as terror, excitement, and elation, and that visual experience regulates gene ex-

pression in the developing cortex (Neve &or low, such as shame, would involve moreright hemispheric activity, in contrast to their Bear, 1989), I suggest that gene–environment

A. N. Schore614

mechanisms are embedded within face-to-face defect in psychiatric disorders is in the heredi-tary systems involved in the synthesis and ca-visuoaffective interactions.

These socioemotional interactions thus di- tabolism of biogenic amines which trophicallyregulate maturation in subcortical and corticalrectly impact the growth of limbic regions.

The right cerebral cortex, densely intercon- information processing centers, and that suchmutations lead to a disruption of normal syn-nected into limbic structures, is specifically

impacted by early social experiences, is pri- aptogenesis and circuit formation. The genesthat encode the production of bioamines andmarily involved in attachment experiences,

and is more vulnerable to early negative envi- their receptors continue to be activated post-natally, causing a dramatic expansion of theseronmental influences than the left. Bowlby

(1969) points out that the development of a systems over the stages of human infancy.Aminergic neuromodulators regulate both thelate-maturing control system associated with

attachment is influenced by the particular en- responsiveness of the developing cortex to en-vironmental stimulation, and the organizationvironment in which development occurs. This

implies that during sensitive periods of right of cortical circuitry, and because their activityis highly heritable (Clarke et al., 1995), al-hemispheric growth less than optimal early

environments in interaction with genetic fac- tered genetic systems that program the keyenzymes in their biosynthesis are now consid-tors are important forces in compromised

brain organization and the pathogenesis of ered to represent potential contributors to highrisk scenarios (Mallet, 1996). Indeed, thedisorders of affect regulation.

The brain growth spurt spans from the end genes for tyrosine hydroxylase, the rate-limit-ing enzyme in both dopamine and noradrena-of prenatal life through the end of infancy, a

time period when the right hemisphere is rap- line production, are essential to both fetal de-velopment and postnatal survival (Zhou,idly expanding. During this exact interval the

total amount of DNA in the cerebral cortex Quaife, & Palmiter, 1995). Alterations in thegenetic systems that program bioamines andincreases dramatically and then levels off

(Winick, Rosso, & Waterlow, 1970). It is in their receptors, agents that directly influencemorphogenesis, would thus negatively affectthis period that timed gene action systems

which program the structural growth and con- the critical period organization and function-ing of ventral tegmental dopaminergic andnections of the higher structures of the limbic

system are activated. Although it is estab- lateral tegmental noradrenergic neurons thatregulate the metabolic capacities of their cor-lished that these hereditary expressions re-

quire transactions with the environment, the ticolimbic terminal fields.As previously mentioned, the constructionquestion arises as to what mechanism embed-

ded in the early caregiver–infant relationship of modular circuits in critical periods is asso-ciated with linkages between areas of high ac-could act to experientially shape genetic po-

tential? Hofer’s (1990) research shows that tivity of the energy generating enzyme cyto-chrome oxidase. This implies that earlythe mother acts as a “hidden” regulator of not

only infant brain catecholamines, agents that mitochondrial pathology would underlie de-fective brain circuitry. Nuclear and mitochon-activate the pentose phosphate pathway and

ribonucleic acid synthesis (Cummins, Lor- drial genes that encode cytochrome oxidase(Hevner & Wong–Riley, 1993), especially ineck, & McCandless, 1985), but also of orni-

thine decarboxylase, a key enzyme in the bioaminergic (and hypothalamic neuroendo-crine) systems and their receptors, may turncontrol of nucleic acid synthesis in the devel-

oping brain (Morris, Seidler, & Slotkin, out to be an important locus for the develop-ment of “faulty” circuit wirings that mediate1983). These events influence not only cate-

cholaminergic-driven maturation of the amyg- a predisposition to later forming psychiatricdisorders. In fact brain mitochondrial abnor-dala, but later maturing paralimbic areas in

the temporal pole and then orbitofrontal cor- malities are now implicated in the etiology ofa childhood neurological disorder of the righttices.

There is now an increasing amount of evi- frontal lobe (Rett Syndrome) that shows so-cialization deficits at 9 months and onset ofdence indicating that the underlying genetic

Nonlinear right brain 615

autisitic-appearing regression of interpersonal to the environmental signals provided by theexternal body of the mother. The brain growthinteraction at 18 months (Cornford et al.,

1994). Alterations of oxidative metabolism spurt, from the last trimester of pregnancythrough the 2nd year, spans both of these peri-due to mutations of genes that encode iso-

forms of cytochrome oxidase are now being ods, emphasizing the principle that the genesthat program its regional organization are ex-explored in the pathogenesis of the schizo-

phrenic brain (Marchbanks, Mulcrone, & pressed in two very different environments,first a totally anaerobic and then an increas-Whatley, 1995).

Mitochondrial gene expression is involved ingly aerobic cellular environment. Gene ex-pression is regulated by oxygen levels in thein “the mechanisms by which mammalian

cells adapt to the changing energetic demands cell as well as by neurohormones and bio-aminergic neuromodulators.in response to functional, developmental and

pathological factors” (Attardi, Chomyn, King, During critical periods of regional matura-tion, prolonged perturbations in the social en-Kruse, Polosa, & Murdter, 1990, p. 509). The

genetic system encoded in mitochondrial vironment lead to dysregulated levels ofstress-responsive catecholamines, thereby al-DNA is maternally inherited, is governed by

non-Mendelian mechanisms, and has a muta- tering gene–environment interactions andproviding for potential sites of pathomorpho-genicity rate 10 times that of nuclear DNA. A

mutation of these genes may occur in utero, genesis. Dopamine, acting at excitatory gluta-matergic NMDA and D1 receptors, triggersbut the amplification of mitochondrial DNA

(which occurs from infancy onward; Simo- c-fos immediate early genes (Berretta, Robert-son, & Graybiel, 1992) that turn on othernetti, Chen, DiMauro, & Schon, 1992) during

a critical period of rapid mitochondrial prolif- genes within the cell, ultimately leading tolong-term structural changes associated witheration in actively growing brain regions rep-

resents a mechanism by which the number of early imprinting experiences. But dopamineincreases under stress (Bertolucci–D’Angio,local genetic mutations could increase. It is

now thought that once the mutant mitochon- Serrano, Driscoll, & Scatton, 1990), and caninduce neurotoxic inhibition of mitochondrialdrial DNAs reach a critical level, cellular phe-

notype changes rapidly from normal to abnor- respiration and defective energy metabolism(Ben–Shachar, Zuk, & Glinka, 1994) andmal, and the resultant impairment of oxidative

phosphorylation and ATP production leads to DNA mutations in brain tissue (Spencer et al.,1994). An early stressful environment thusdisease expression. Shoffner (1996) states

“disease expression seems to be influenced by detrimentally and irreversibly impacts the ge-netic systems of catecholaminergic neuronspoorly understood genetic and environmental

interactions” (p. 1284). and their receptors (including receptors on as-troglial and endothelial cells, near dendriticCurrent models of the genetic analysis of

complex diseases prescribe an interaction be- spines) that trophically regulate the criticalperiod growth and metabolism of widespreadtween a susceptibility gene with a predispos-

ing environmental agent. In these studies, “en- corticolimbic areas.Indeed, animal studies show that earlyvironmental” usually refers to factors in the

physical environment, but I propose that in postnatal stress, such as maternal deprivation,produces permanent changes in dopamine re-the case of the transmission of psychiatric dis-

eases stressors in the social environment inter- ceptor function (Lewis, Gluck, Beauchamp,Keresztury, & Mailman, 1990), especially inact with genetic mechanisms to amplify a ge-

netic predisposition and create a vulnerability cortical areas, as well as a significant reduc-tion in the number of dopaminergic neuronsto later forming mental illness. I further sug-

gest that these interactions occur between the in the ventral tegmental area, long-lasting ef-fects that result in “abnormalities of socialdeveloping organism and the “nonshared”

(Plomin, Rende, & Rutter, 1991) environment and affective function” (Martin, Spicer,Lewis, Gluck, & Cork, 1991) and a reducedwith which it interacts, responding first to the

environmental signals provided by the inter- capacity to respond to aversive experiencesin adulthood (Cabib, Puglisi–Allegra, &nal body of the mother, and then after birth,

A. N. Schore616

D’Amato, 1993). It is now well established states, a pathological system lacks variabilityin the face of environmental challenge. Whatthat postnatally maturing dopaminergic pro-

jections are potential sites of developmental early factors could produce such an organiza-tion? According to the classical diathesis–defects. In light of the principle that “develop-

ing mesencephalic dopamine neurons may stress model, psychiatric disorders are causedby the interaction of genetic–constitutionaldisplay varying subpopulation specific vulner-

ability to outside pathological influences over vulnerability and environmental psychosocialstressors. The interface of nature and nurturethe course of postnatal ontogeny” (Wang &

Pitts, 1994, p. 27), genetic systems, both nu- is now thought to occur in the psychobiologi-cal interaction between mother and infant,clear and mitochondrial DNA, of the dopa-

mine neurons within the ventral tegmental “the first encounter between heredity and thepsychological environment” (Lehtonen, 1994,area, particularly the medial, rostral linear nu-

cleus (as opposed to other mesencephalic do- p. 28). In such transactions the primary care-giver is providing experiences which shapepaminergic subnuclei that innervate mesolim-

bic areas), would be particularly important, genetic potential by acting as a psychobiologi-cal regulator (or dysregulator) of hormonessince these project collaterals to the cortex,

including the ventral prefrontal areas (see that directly influence gene transcription. Thismechanism mediates a process by which psy-Schore, 1994).

In addition, early social experiences also choneuroendocrinological changes duringcritical periods initiate permanent effects atplay a significant role in the development of

the other catecholamine, noradrenaline. At- the genomic level. The final developmentaloutcome of early endocrine–gene interactionstachment stress induces alterations in mam-

malian infant noradrenaline levels (Clarke, is expressed in the imprinting of evolvingbrain circuitry.Hedecker, Ebert, Schmidt, McKinney, &

Kraemer, 1996) that become permanent (Hig- Of particular importance to the creation ofa brain system which is “invulnerable” orley, Suomi, & Linnoila, 1991). The enduring

changes in noradrenergic system function that “vulnerable” to future psychopathology aresteroid hormones associated with stress re-result from disturbed mother–infant relations

represent a biological substrate or “risk fac- sponses. These bioagents regulate gene ex-pression, and, depending upon the cell type,tor” for a vulnerability to despair in later life

(Kraemer, 1992) and a susceptibility to affec- induce or repress sets of genes, and in thismanner they act as an essential link betweentive and anxiety disorders (Rosenblum,

Coplan, Friedman, Basoff, Gorman, & An- “nature and nurture.” Levels of corticosteroidsin the infant’s brain are directly influenced bydrews, 1994). In human studies, Rogeness and

McClure (1996) report lowered noradrenaline the mother–infant interaction. In beneficialexperiences the infant’s glucocorticoid stresslevels in children exposed to neglect, and sug-

gest that this psychosocial stress modifies response is modulated by the psychobiologi-cally attuned mother, thereby inhibiting thethe genetic expression of the noradrenaline

system. These authors conclude that early ex- infant’s pituitary–adrenal response to stress.As a result of these experiences, the infant, inperience has long-lasting effects on neuro-

modulator functioning, and that genetic–envi- the face of a subsequent novel stimulus,shows a lesser corticoid output and a moreronmental factors, especially during early

critical periods of development, are important rapid return of corticosterone to baseline lev-els, characteristics of a resilient coping mech-in psychopathogenesis.anism. These critical period experiences alsohave long-term structural consequences—theyExcessive Developmental Parcellation permanently enhance glucocorticoid receptorand the Pathomorphogenesis of concentrations in neurons in the frontal cortexFrontolimbic Circuits that are involved in terminating the adreno-cortical stress response.As opposed to an adaptive stable dynamic

system that can flexibly transition between On the other hand, stressful dyadic interac-

Nonlinear right brain 617

tions that generate enduring states of painful of growth are exposed for extended periods oftime to heightened levels of circulating corti-negative affect are associated with elevated

levels of corticosteroids in the infant brain. costeroids and catecholamines. This toxicbrain chemistry induces synapse destructionDeprivation of early maternal stress modula-

tion is known to trigger an exaggerated re- and death in “affective centers” in the matur-ing limbic system and therefore permanentlease of corticosteroids upon exposure to

novel experiences which, in adulthood, per- functional impairments of the directing ofemotion into adaptive channels. More specifi-sists for a longer period of time. Elevated lev-

els of this stress hormone in prenatal and cally, I suggest that the postnatal developmentof the affect regulating orbitofrontal cortex,postnatal periods inhibit dendritic branching,

reduce brain nucleic acid synthesis, and per- the corticolimbic system which directly con-nects into the hypothalamus and influencesmanently decrease brain corticosteroid recep-

tors. Critical periods are times of heightened corticosteroid levels (Hall & Marr, 1975), isspecifically and permanently negatively im-energy production, and these neurohormones

specifically inhibit brain energy metabolism pacted by high levels of circulating corticoste-roids that accompany stressful socioemotional(Bryan, 1990), a condition that enhances the

toxicity of excitatory neurotransmitters (No- environmental interactions.In support of this, there is evidence tovelli, Reilly, Lysko, & Henneberry, 1988) and

produces alterations in mitochondrial struc- show that that stress-induced increases of glu-cocorticoids in postnatal periods induce an ab-ture and function (Kimberg, Loud, & Weiner,

1968). Glucocorticoids within the high physi- normal intrinsic circuitry within the cortico-limbic system. Benes (1994) suggests that theological range impact both DNA and energy

systems, and profoundly affect areas of the neurotoxic effects of glucocorticoids are asso-ciated with simultaneous hyperactivation ofbrain that are organizing in infancy.

As I have noted in other works, the devel- the excitotoxic NMDA-sensitive glutamate re-ceptor, a critical site of synapse eliminationoping brain of an infant who experiences

frequent intense attachment disruptions is and neurotoxicity during early development.It is now known that not only glucocorticoidschronically exposed to states of impaired au-

tonomic homeostasis which he/she shifts into (Wyllie, 1980) but also glutamate (Ankar-crona et al., 1995) and dopamine (Offen, Ziv,to maintain basic metabolic processes for sur-

vival. These disturbances in limbic activity Sternia, Melamed, & Hochman, 1996) can in-duce apoptotic cell death. Dopamine activatesand hypothalamic dysfunction are accompa-

nied by increased levels of “stress proteins” NMDA receptors, and excessive NMDA re-ceptor stimulation generates the superoxidein the developing brain (see Schore, 1994). In

addition to an extensive history of misat- free radicals associated with oxidative stress(Lafon–Cazal, Pietri, Culcas, & Bockaert,tunement in the 1st year, stressful socializa-

tion experiences in the 2nd that elicit shame 1993). Both Na+,K+-ATPase (Jamme, Petit,Divoux, Gerbi, Maixent, & Nouvelet, 1995)represent a traumatic interruption of interper-

sonal synchronizing processes, a rupture of at- and mitochondria (Vercesi & Hoffmann,1993) can sustain damage from the potentiallytachment dynamics that triggers a state transi-

tion from energy-mobilizing sympathetic to toxic effects of the extremely reactive freeradicals, especially hydroxyl radicals that de-energy-conserving parasympathetic dominant

ANS activity, a sudden switch from ergo- stroy cell membranes and induce mutations inmitochondrial DNA (Giulivi, Boveris, & Ca-tropic to trophotropic arousal that is accompa-

nied by elevated levels of cortisol (see Schore, denas, 1995). Defective mitochondrial bio-genesis and energetic activity are early events1991, in press-b). Both catecholamines are re-

leased in response to stressful disruptions of in apoptosis (Vayssiere, Petit, Risler, & Mig-notte, 1994; Zamzimi et al., 1995). Impairedthe attachment bond. If the caregiver does not

participate in reparative functions that reduce mitochondrial function would result in re-duced ATP synthesis levels, which in turn isstress and reestablish psychobiological equi-

librium, limbic connections in a critical stage associated with synaptic transmission failure

A. N. Schore618

(Lipton & Whittingham, 1982). These events, axons that project to different subcortical bio-aminergic or hypothalamic nuclei, would haveoccurring during a critical period, could pro-

duce a permanently diminished local metabolic long-enduring negative effects.These interactive experiences are embed-capacity and therefore reduced functional ac-

tivity within and between particular brain re- ded in different types of dyadic attachmenttransactions, and if they are less than optimalgions, especially under challenging conditions

that require sustained energy levels. they can induce an excessive apoptotic parcel-lation (e.g., elimination of long axon collater-In fact, this same interaction between corti-

costeroids and excitatory transmitters is now als, cell death, dendritic regression) of thecomponents of either one or both of the dualthought to mediate programed cell death and

to represent a primary etiological mechanism limbic circuits (Schore, 1994, 1996). Fronto-limbic parcellation is mediated by the samefor the pathophysiology of neuropsychiatric

disorders (Margolis et al., 1994). Although mechanism described above—excitotoxinshave been shown to destroy orbitofrontal neu-the critical period overproduction of synapses

is genetically driven, the pruning and mainte- rons (Dias et al., 1996), and this would pro-duce modifications in the microstructural or-nance of synaptic connections is environmen-

tally driven. This clearly implies that the de- ganization and thereby metabolic limitationsof areas that hierarchically dominate the twovelopmental overpruning of a corticolimbic

system that contains a genetically encoded un- limbic circuits. Different amounts and typesof connectional degenerations of the maturingderproduction of synapses represents a sce-

nario for high risk conditions. Carlson, Earls, orbitofrontal cortex, an area intimately in-volved in attachment dynamics, would ac-and Todd (1988) emphasize the importance of

“psychological” factors in the “pruning” or count for the different patterns in biobehav-ioral organizations of securely and insecurely“sculpting” of neural networks in specifically

the postnatal frontal, limbic, and temporal attached infants (Spangler & Grossmann,1993).cortices. Excessive pruning is thought to a be

primary mechanism in such “neurodevelop- More specifically, infants with a history of“disorganized–disoriented” insecure attach-mental” disorders as autism and schizophrenia

(Keshavan, Anderson, & Pettegrew, 1994), ments show a high rate of exposure to abuseexperiences (Main & Solomon, 1986). Perry,where large reductions in frontal connectivity

are associated with the emergence of circuit Pollard, Blakley, Baker, and Vigilante (1995)assert that the abused infant responds to thispathology that mediates dysfunctional symp-

toms (Hoffman & Dobscha, 1989). threatening interpersonal environment withboth states of hyperarousal that induce long-In most models of psychiatric disorders the

concept of “pruning in parallel circuits” lasting elevations of sympathetic catechol-aminergic activty, and of parasympathetic va-(Mender, 1994) has been applied to circuits

within the cortex, but it is the pruning of hier- gal-associated dissociation associated withhypoarousal and increased cortisol produc-archical cortical–subcortical circuits that is

central to the psychoneurodevelopmental ori- tion, and that these states are internalized asa sensitized neurobiology. The latter effect isgins of the corticolimbic defects that underlie

a vulnerability to psychopathology. Of special revealed in the finding that this group of tod-dlers exhibits higher cortisol levels than allimportance to the emergence of adaptive af-

fect regulation are the reciprocal connections other attachment classifications (Hertsgaard,Gunnar, Erickson, Farrell, & Nachmias, 1995).between the orbitoinsular cortex and not only

all sensory areas of the cortex, but with sub- These dysregulating environmental eventstrigger extreme and rapid alterations of ergo-cortical dopamine neurons in the ventral teg-

mental area, noradrenaline neurons in the me- tropic and trophotropic arousal that createchaotic biochemical alterations in the infantdulla, and various neuroendocrine neurons in

the hypothalamus. Critical period interactive brain, a condition conducive to extensive oxi-dative stress and apoptotic destruction of de-experiences that lead to excessive pruning of

catecholaminergic axonal terminals that inner- veloping synaptic connections within bothlimbic circuits. This psychoneurobiologicalvate cortical areas or of cortical cholinergic

Nonlinear right brain 619

mechanism may mediate the effects by which In contrast, different attachment historiesindelibly influence the dual limbic compo-exposure of an infant to emotional trauma re-

sults in a sensory-affecto-motor “emotional– nents of the “organized” forms of insecure at-tachments. An insecure–resistant (ambivalent)instinctual recordings” of the experience that

are inscribed in the neurotransmitter patterns attachment organization reflects an experi-ence-dependent expansion of the excitatoryin the limbic system (Weil, 1992).

Early abuse experiences of neglect and/or ventral tegmental circuit and an extensive par-cellation of the inhibitory lateral tegmentaltrauma thus create abnormal critical period

microenvironments for the development of circuit. The final wiring of this type of orbito-frontal system is sympathetically biased to-corticolimbic areas. Critical period cell death

of orbitofrontal and/or temporal cortical neu- wards states of ergotropic high arousal andheightened emotionality, but it lacks in “vagalrons that respond to emotional facial displays

would lead to permanent deficits in reading restraint” and therefore has a reduced func-tional capacity of, under stress, stimulatingthe facially expressed emotional states of oth-

ers. Deficits in emotion decoding ability are the parasympathetic and inhibiting the sympa-thetic components of limbic function. Thisseen in abused children (Camras, Grow, & Ri-

bordy, 1983). Since the orbitofrontal areas are system manifests a susceptibility to the under-regulation disturbances that underlie external-tied into both limbic circuits and both branches

of the autonomic nervous system, an exten- izing psychopathologies. Such personalitiesshow difficulty in repressing negative affectssive developmental parcellation of both cir-

cuits would result in a poorly evolved fronto- and easy access to negative memories, and aninability to inhibit emotional spreading (Mi-limbic cortex, one in which sympathetic and

parasympathetic components could not oper- kulincer & Orbach, 1995). On the other hand,insecure–avoidant attachment histories expe-ate reciprocally (Berntson, Cacioppo, & Quig-

ley, 1991). This organization of autonomic rientially shape an expansion of the inhibitorylateral tegmental and excessive parcellation ofcontrol prevents the integration of lower more

primitive autonomic states that allows for the the excitatory ventral tegmental limbic cir-cuits. In the middle of the 2nd year, a pointelaboration of new higher states. Because of

its fragile regulatory capacities, under even of orbitofrontal maturation, insecure–avoidantinfants of depressed mothers, during separa-moderate stress, it is vulnerable to disorgani-

zation and to affect shifts that are extremely tion stress, exhibit reduced right frontal EEGactivity (Dawson, 1994). This type of fronto-discontinuous and labile.

It is now established that structural alter- limbic system is biased towards parasympa-thetic states of trophotropic low arousal andations of the developing hypothalamic–pituit-

ary–adrenal system are responsible for a vul- reduced overt emotionality, but under stress itis inefficient in regulating high arousal states,nerability to pathology in later life and that

chronically elevated levels of corticosteroids and is vulnerable to overregulation disturb-ances and internalizing psychopathologies.are associated with psychiatric disturbance.

Exposure of the right hemisphere to extensive These personalities show defensiveness andlow accessibility to negative memories, asand long-enduring traumatic alterations of

arousal during its critical period of organiza- well as high levels of “deactivating strategies”(Dozier & Kobak, 1992). A recent finding oftion may predispose the disorganized–dis-

oriented infant to a vulnerability to posttrau- gender differences in orbital functions that areestablished in the 2nd year but thought to per-matic stress disorders (Rauch et al., 1996).

This hemisphere is dominant for the regula- sist across the life span (Overman, Bacheva-lier, Schuhmann, & Ryan, 1996) suggests dif-tion of the secretion of cortisol (Wittling &

Pfluger, 1990) and shows heightened activity ferences in wiring of the limbic systembetween the sexes, and may be relevant to thein overwhelming and uncontrollable panic

states marked by terror and intense somatic well-known susceptibility of males to exter-nalizing and females to internalizing disor-symptoms (Heller, Etienne, & Miller, 1995)

and during recall of traumatic memories ders.Frontal functions have long been known to(Schiffer, Teicher, & Papanicolaou, 1995).

A. N. Schore620

be associated with personality functioning. ing system and its environment. These pat-terned energy fluctuations, associated withAn important emphasis of the chaotic systems

approach is a shift away from the study of nonlinear changes in state, allow for morecomplex interconnections between the sys-traditional group-oriented procedures toward

a new emphasis on individual differences of tem’s components, and therefore constitute asalutary primordial matrix for self-organiza-personality. In the latest neuroscience litera-

ture, authors are proclaiming that rather than tion and the emergence of a hierarchical struc-tural system that is capable of dynamicallyconcentrating on a singular “average” neuro-

anatomic design, attention should now be fo- transitioning between a range of possiblestates and exploring new states. This allowscused on the large range of variation that

“normal” stuctures can exhibit, and that the for the operation of a stable and resilient sys-tem, one that can adaptively change in re-variability in the morphology of the frontal

lobe may underlie individual differences in sponse to environmental perturbations yet re-tain continuity. I then applied this generalfunctional capacities. These principles equally

apply to the ontogenesis of “abnormal” organ- model to the developmental organization ofthe orbitofrontal cortex and its subcortical andizations, and particularly to the experience-de-

pendent evolution of frontal and limbic mi- cortical connections, a homeostatic systemthat dynamically regulates organismic energycroarchitectures and metabolic limitations that

are associated with emotional dysfunction balance and transitions between psychobio-logical states in response to internal and exter-and a vulnerability to psychiatric disorders.

According to Rutter (1995) environmental nal alterations. This hierachical regulatorystructure acts as an executive control systemstresses impinge most on those who have al-

ready exhibited psychological vulnerability for the nonlinear right brain.As opposed to growth-promoting environ-and accentuate preexisting psychological

characteristics. ments, growth-inhibiting environments nega-tively influence the ontogeny of homeostaticThe question is, which specific structural

systems exhibit this vulnerability? I am sug- self-regulatory and attachment systems. Non-optimal environments do not supply sufficientgesting that the orbital frontolimbic system,

the “executive control system” for the entire quantities of nutritive matter and modulatedlevels of energy to the growing brain, andright cortex, the primary cortical hemisphere

involved in attachment functions, the process- these circumstances, especially in interactionwith a genetically encoded lowered limbicing of socioemotional information, and the

regulation of psychobiological states, is sensi- threshold and hyperreactivity to novel envi-ronmental events, give rise to a developingtive to prolonged aversive experiences during

its critical period of growth, and that different system that is poorly equipped to enter into adyadic open homeostatic system with the hu-types of alterations of its organization account

for its adaptive limitations and dysfunctional man environment. This precludes exposure toa variety of socioemotional experiences thatoperations. This formulation is congruent with

Main’s (1996) assertion that “disorganized” are required for experience-dependent brainmaturation, and therefore negatively influ-and “organized” forms of insecure attachment

are primary risk factors for the development ences the stabilization of interconnectionswithin subcortical and cortical areas of the in-of mental disorders.fant’s brain that are in a critical period ofgrowth. Furthermore, the infant’s transactionsEarly Forming Structural Pathology of with an emotionally unresponsive or misat-Nonlinear Right Hemisphere and Origins tuned environment that provides poor interac-of Predisposition to Psychiatric Disorders tive repair are stored in the infant’s develop-ing corticolimbic circuitries as imagistic,At the beginning of this work, I presented a

general model of self-organization, one that visceral, and nonverbal procedural memories.As opposed to a secure interactive representa-emphasizes the central role of synchronized

energy exchanges between a developing liv- tion of an regulated-self-in-interaction-with-

Nonlinear right brain 621

an-attuning-other, these “pathological” work- nia, bipolar disorder, unipolar depression,posttraumatic stress disorder, drug addiction,ing models of attachment encode an enduring

prototypical cognitive–affective schema of a alcoholism, and psychopathic, borderline, andnarcissistic personality disorders (see Schore,dysregulated-self-in-interaction-with-a-misat-

tuning-other (see Schore, 1994, 1997). 1994, 1996 for references).A fundamental postulate of clinical psychi-Early attachment experiences represent

psychobiological transactions between the atry holds that the major source of stress pre-cipitating psychiatric disorders involves themother’s and infant’s right hemispheres. The

child’s growing brain imprints the output of affective response to a rupture or loss of asignificant relationship. It is now thought thatthe mother’s right cortex which contains the

mechanism for the maternal capacity to com- an environmental event, appraised to be emo-tionally meaningful, may be the direct causefort the infant (Horton, 1995). Structural limi-

tations in the mother’s emotion processing of a neurochemical change that then becomesthe psychopathogenic mechanism of the ill-right brain are reflected in a poor ability to

comfort and regulate the infant’s negative af- ness (Gabbard, 1994). Because of the “pat-terning of the nervous system” psychiatric pa-fective states, and these experiences are

stamped into the infant’s right orbitofrontal tients show an inability to adapt internally tostress, and this is symptomatically expressedsystem and its cortical and subcortical con-

nections. Exposure to such conditions through- in a continuing activation or inhibition of or-gan systems in a manner inappropriate to theout a critical period of corticolimbic martura-

tion results in inefficient coping systems that immediate environmental situation. In up-dated neuropsychiatric models, defectivecannot adaptively switch internal states in re-

sponse to stressful external environmental modulators are viewed as causal agents formental abnormalities that are characterized bychallenges. The functional indicators of this

intergenerationally transmitted adaptive limi- a disturbance in the continuity of successivestable memory states (Mender, 1994). Ac-tation are specifically manifest in recovery

deficits of internal reparative coping mecha- cording to dynamic systems theory a stableyet resilient dynamic open system can returnnisms, a poor capacity for the state regulation

involved in self-comforting in times of stress. to a previous stationary state within an ap-propriate time period (Thelen, 1989), but aSuch deficits are most obvious under

highly emotional and challenging conditions dysfunctional system shows poor capacity torecover after stressful departures from homeo-that call for behavioral flexibility and affect

regulation. The adaptive limitation of all psy- static equilibrium. Systems that exhibit goodprimitive organization become more complexchopathologies is manifest in more intense

and longer lasting emotional responses and (Schwalbe, 1991), but those with a compro-mised early ontogeny are inefficient at statethe amplification of negative states. This char-

acterization describes the dysfunction of a regulation and therefore exhibit an abnormal-ity in the dimensionality of state transitions,structurally impaired frontal ventromedial

system that results in “emotional response specifically an overreliance on an oversimpli-fied set of transition paths among attractorsperseveration” (Morgan & LeDoux, 1995),

that is, an inefficiency in the temporal organi- which constrains the individual’s flexibility toadapt to challenging situations with new strat-zation of behavior (Fuster, 1985) and in the

adjustment and correction of emotional states egies.Recent research in biological psychiatry is(Rolls, 1986). Recent neurobiological studies

indicate that due to its unique neurobiological focusing on the relationships between the dis-turbed emotions and cognitions of psycho-characteristics, the orbital cortex shows a

“preferential vulnerability” to a spectrum of pathological states and neurotransmitter dys-functions (Maas & Katz, 1992) and ispsychiatric disorders (Barbas, 1995). In previ-

ous work I have begun to chronicle a growing emphasizing the functional role of monoami-nergic neuromodulators in psychiatric disor-number of studies that implicate orbitofrontal

metabolic dysfunction in autism, schizophre- ders (Dolan & Grasby, 1994). Indeed, the lim-

A. N. Schore622

bic receptors of these bioamines are the This clearly implies that various patternsof alterations of right brain bioamine activityprimary target of the psychopharmacological

agents that are currently being used by clini- should be exhibited in the high risk infant. In-deed, there is now current interest in identify-cal psychiatry. Contemporary psychiatry is

also now delving more deeply into the role of ing the critical involvement of dopamine indevelopment, before signs and symptoms areright hemispheric dysfunction in psychiatric

disorders (Cutting, 1992), such as schizophre- expessed (Winn, 1994). Psychobiological re-search indicates that prenatally stressed de-nia (Cutting, 1994), autism (Ozonoff &

Miller, 1996), depression (Liotti & Tucker, veloping systems show, soon after birth, analteration of dopamine levels in the right1992), mania (Starkstein, Federoff, Berth-

ier, & Robinson, 1991), and posttraumatic hemisphere and alterations of emotionality(Friede & Weinstock, 1988). Children diag-stress disorder (Rauch et al., 1996). This

hemisphere is deeply connected into the two nosed as high risk for schizophrenia exhibitearly neurointegrative deficits, reflecting dys-forebrain–midbrain limbic circuits, the norad-

renergic vagal brain circuit of emotion regula- regulation of hypothalamic and reticular acti-vating systems (Fish, Marcus, Hans, Auer-tion and the mesocortical dopaminergic sys-

tem that processes emotionally stressful bach, & Perdue, 1992). Under challenge,these infants show left-sided postural andinputs. The dysfunction of these limbic cir-

cuits is central to the affect regulatory deficits movement abnormalities, reflecting overacti-vity of ascending dopaminergic systems in theof all psychiatric disorders.

A major contribution of the discipline of right hemisphere (Walker, 1994). This devel-opmental syndrome may reflect an early inef-developmental psychopathology to the study

of psychiatric disorders is its emphasis on the ficient orbitocortical modulation of ascendingexcitatory influences which results in an over-elucidation of the early ontogenetic factors

that predispose high risk individuals to later activity of right brain ascending dopaminergicsystems and enhanced responsiveness of sub-psychopathologies. In consonance with dy-

namic systems theory, this developmental per- cortical mesolimbic dopaminergic systems tostress (Deutch, 1992). High risk offspring ofspective underscores the fact that a more de-

tailed knowledge of the self-organization of schizophrenic parents show EEG abnormali-ties in the right rather than left hemispherethe developing brain is essential to a deeper

understanding of specifically how genetic and (Itil, Hsu, Saletu, & Mednick, 1974), and dis-turbances in facial expressions of emotion areenvironmental factors interact to generate an

enduring vulnerability to stress-induced disor- seen in preschizophrenic infants in the firstyear of life (Walker, Grimes, Davis, & Smith,ganizations of adaptive functions. Develop-

mental neurobiological studies indicate that 1993). These early events may play a criticalrole in the “developmental disconnection ofthe right brain system, which more than the

left is deeply interconnected into the limbic temporolimbic prefrontal cortices” seen in thehypometabolic prefrontal areas of the schizo-system and is fundamentally involved in re-

sponding to and coping with stress, is in a phrenic brain (Weinberger & Lipska, 1995)and in the genesis of the negative symptomsgrowth spurt in early infancy. The limbic ar-

eas of the cortex are in an intense state of my- of the disorder.This model of early right brain deficits iselination from the middle of the first through

the middle of the 2nd year (Kinney, Brody, also supported in another high risk popula-tion. Three- to 6-month-old infants of de-Kloman, & Gilles, 1988) and show an ana-

tomical maturation at the end of this period. pressed mothers show a right frontal EEGasymmetry (Field, Fox, Pickens, & Nawrocki,Most importantly, the biogenic aminergic sys-

tems that regulate the growth and activity of 1995) which has been interpreted as reflectinga subcortical asymmetry in the amygdalathe limbic system are in an active state of ex-

perience-dependent growth in these same (Calkins & Fox, 1994). At 10 months, infantswho express more intense distress to maternalstages of human infancy.

Nonlinear right brain 623

separation display a greater right than left cial perception, chronic emotional difficulties,inability to display affect, and impairment infrontal activation (Davidson & Fox, 1989),

and this asymmetry has been related to emo- visuospatial representation (Weintraub &Mesulam, 1983).tional reactivity and vulnerability to psycho-

pathology in both infants and adults (David- These deficits endure into adulthood, sincelongitudinal studies are now showing that un-son, Ekman, Saron, Senulis, & Friesen, 1990).

Individuals with extreme right frontal activa- dercontrolled and inhibited disturbances inearly childhood predict adult psychiatric dis-tion are thought to exhibit a negative affective

response to a very low intensity negative af- orders (Caspi, Moffitt, Newman, & Silva,1996). In adults “greater right hemisphericity”fect elicitor, and to be impaired in the ability

to terminate a negative emotion once it has is associated with a history of more frequentnegative affect and lower self-esteem (Per-begun (Wheeler, Davidson, & Tomarken,

1993). In very recent work, Fox, Schmidt, singer & Makarec, 1991), that is, chronic dif-ficulties in affect regulation. Functional limi-Calkins, Rubin, and Coplan (1996) report that

young children with internalizing and exter- tations of affect regulation reflect structuraland metabolic impairments in right frontolim-nalizing problems show greater right than left

frontal EEG activation, and suggest that this bic distributed systems that contain connec-tions between cortical and subcortical areas,pattern reflects difficulties with affect regula-

tion, whether the affect arousal is extremely and these prefrontal organizations representprimary sites of psychopathogenesis. This isnegative or positive. These findings fit nicely

with the model of right hemispheric regulation because early relational environments that in-hibit the organization of this control systemof intense emotional states presented earlier.

There is now convincing evidence that the generate an unstable right cortical capacity toevaluate and guide behavior, a metabolicallydeficits of an early compromised right cortex

persist as the individual passes into early inefficient one that under stress is easily dis-placed by an inflexible subcortical mecha-childhood. A loss of interconnections (exten-

sive parcellation) within the infant’s early de- nism. The uncoupling of the two right brainlimbic circuits would occur in response toveloping right hemisphere is associated with

an impairment of social perception (i.e., diffi- high levels of interactive stress in episodes of“expressed emotion,” intense levels of humili-culty in evaluating facial expression, gestures,

or prosody). These children are at high risk ation, criticism, hostility, and emotional over-involvement within a close relationshipfor the nonverbal learning disabilities (Sem-

rud–Clikeman & Hynd, 1990) associated with (Vaughn & Leff, 1976). This uniquely potentpsychobiological stressor for the induction ofa “developmental right hemisphere syn-

drome” (Gross–Tsur et al., 1995). The latter all classes of psychiatric disorders triggers ex-tremely high levels of sympathetic ergotropicauthors enumerate specific emotional and in-

terpersonal problems that are present early in and parasympathetic trophotropic arousal thatare beyond the individual’s regulatory capaci-development but frequently not recognized

until the child begins school. These include ties. The resultant “transient frontolimbic im-balance” elicits subcortical limbic kindling,maladaptation to new situations, difficulties in

maintaining friendships, withdrawn and ex- subjectively experienced as a sudden transi-tion into rapidly shifting and intensely affec-cessively shy behaviors, and avoidance of eye

contact. A “developmental social–emotional tive states, that is, “emotional chaos” (Grot-stein, 1990).processing disorder” associated with electro-

physiological abnormalities of the right hemi- The right hemisphere, which is preferen-tially activated in stress, is specialized to pro-sphere has been reported by Manoach, Sand-

son, Mesulam, Price, and Weintraub (1993). cess intensely negative states (Otto, Yeo, &Dougher, 1987). PET imaging studies thatIn a previous study these authors concluded

that early right hemisphere dysfunction is ex- measure energy metabolism are now reveal-ing the preeminent role of right hemisphericpressed in later life as introversion, poor so-

A. N. Schore624

paralimbic activity as traumatic emotional negative affective states, to develop a theoryof mind of the intentions of others, and to bememories are activated (Rauch et al., 1996),

and are documenting the changes in orbito- psychobiologically attuned and thereby em-pathic to the internal states of an other selffrontal metabolic activity during the evocation

of a phobic state (Frederikson, Wik, Annas, are fundamental prerequisites of an adaptivecapacity to enter into satisfying interactionsEricson, & Stone–Elander, 1995). The impor-

tance of these studies is that they can do more with other humans. Affect regulating interac-tions are essential to the development of thethan simply “localize” psychiatric impair-

ments in the brain. Rather, they offer informa- infant’s coping skills, but at later points in thelife span they continue to be necessary for thetion regarding the temporal organization of

dysregulated dynamic systems, and can there- continued growth of the brain and the expand-ing capacity to experience more complex psy-fore elucidate a deeper understanding of the

state changes that underlie the various forms chobiological states.The nonlinear right hemisphere, the sub-of emotional dysregulation manifest in differ-

ent classes of psychiatric disorders. The fact strate of early attachment processes, ends itsgrowth phase in the 2nd year, when the linearthat a broad spectrum of psychiatric disorders

show disturbances of the right hemisphere, left hemisphere begins one, but it cycles backinto growth phases at later periods of the lifethe hemisphere that is centrally influenced by

attachment experiences, accounts for the prin- cycle (Thatcher, 1994). This allows for thecontinuity of attachment mechanisms in sub-ciple that all early forming psychopathology

constitutes disorders of attachment and mani- sequent functioning, and yet also for the po-tential continuing reorganization of the emo-fests itself as failures of interactional and/or

self-regulation. tion-processing right brain throughout life.The orbitofrontal regions, centrally involvedin the regulation of psychobiological state andDynamic Systems Theory and Ongoing energy balance, are unique in that they retainRight Hemispheric Development the neuroanatomic and biochemical featuresof early development, and for this reason theyAttachment is “the apex of dyadic emotional

regulation, a culmination of all development are the most plastic areas of the cortex (Bar-bas, 1995). If, however, an infant, especiallyin the first year and a harbinger of the self-

regulation that is to come” (Sroufe, 1996, p. one born with a genetically encoded alteredneurophysiologic reactivity, does not have ad-172). The attachment dynamic continues

throughout the life span as an unconscious equate experiences of being part of an opendynamic system with an emotionally respon-mechanism that mediates the interpersonal

and intrapsychic events of all relationships, sive adult human, its corticolimbic organiza-tion will be poorly capable of coping with theespecially intimate relationships. By the 2nd

year, the infant can construct accurate repre- stressful chaotic dynamics that are inherent inall human relationships. Such a system tendssentations of events that endure and are acces-

sible over time (Bauer, 1996), and these expe- to become static and closed, and invested indefensive structures to guard against antici-riences are imprinted into right hemispheric

networks that store autobiographical memory pated interactive assaults that potentially trig-ger disorganizing and emotionally painful(Fink et al., 1996). In this manner, “disposi-

tional characteristics that appear to be linked psychobiological states. Because of its avoid-ance of novel situations and diminished ca-to right hemisphere activity are a product of a

developmental process involving cognitive pacity to cope with challenging situations, itdoes not expose itself to new socioemotionaland memory structures” (Heller, 1993, p.

484). The ability to access an internal work- learning experiences that are required for thecontinuing experience-dependent growth ofing model of relationships that encodes strate-

gies of affect regulation and expectations of the right brain. This structural limitation, inturn, negatively impacts the future trajectoryfuture interactions, to interact with a meaning-

ful other to share positive affect and reduce of self-organization.

Nonlinear right brain 625

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