Development and Psychopathology, 8 (1996), 43-58 Copyright 1996 Cambridge University Press Printed in the United States of America
Abstract
The model presented identifies the importance of neural regulation of autonomic state as an antecedent substrate for emotional, cognitive, and behavioral regulation. It is proposed that individual differences in neural regulation of autonomic state are related to normal and abnormal development. Establishing nervous system regulation of autonomic state is the infant's initial task of self-regulation. Survival for the high-risk infant is based primarily on physiological self-regulation. Although the methods described focus on the high-risk neonate, the model provides insight into normal development and may be generalized to the study of older children and adults with behavioral and psychological problems. Moreover, the model may contribute to assessment and intervention strategies for normal and abnormal development.
Birth is the greatest challenge to human survival. When an infant is born, the supportive environment of the womb is gone. Parturition functionally disrupts the fetus's dependency on maternal physiology and expels the fetus from this secure environment. Thus, birth marks a transition as the management of autonomic regulation shifts from the maternal placental-fetal system to the newborn. In this demanding environment, the newborn must have skills to regulate autonomic processes (e.g., breathe, feed, digest, thermoregulate, etc.) and to communicate autonomic state needs to caregivers (e.g., cry). Within minutes of birth, these skills are challenged. Difficulties in expressing physiological competence are life threatening. Even with healthy fullterm newborns, there is great concern by healthcare professionals and parents about an infant's physiological regulation competency in negotiating this complex transition. Postpartum adaptation is more difficult for the high-risk infants who experience a variety of risk factors including prematurity and delivery complications. These high-risk infants, often limited by a less mature or a damaged nervous system, are compromised in performing these self-regulatory tasks.
The study of the high-risk neonate provides a real-life laboratory to evaluate the unique contribution of autonomic regulation to development. Research can evaluate the relation between specific physiological vulnerabilities and subsequent developmental problems in behavioral organization, social behavior, and cognitive function.
A model of neural regulation of autonomic processes that focuses on the high-risk neonate might address two research questions. First, is it possible to assess the relative risk that an individual newborn faces following the birth process; and second, how do we help the high-risk newborn negotiate the transition from a physiological dependency on maternal systems to the physiological self-regulation required in the extrauterine world?
Successful adaptation of the newborn to the extrauterine environment requires a dynamic and complex repertoire of responses. These responses occur on several levels. Although self-regulatory physiological strategies require complex neurophysiological systems, involving feedback between the brain and peripheral physiology, several systems may be monitored by careful visual surveillance of the newborn. For example, the Apgar scale (Apgar, 1953) codifies the status of physiological self-regulation via a standard observational scale. Similarly, neurological examinations during the newborn period assess neural function through the systematic elicitation of observable reflexes.
In the day-to-day care of the high-risk infant, clinical management attempts to compensate for the immature or compromised nervous system and its limited abilities to regulate physiological homeostasis. For example, radiant heaters use the neonate's core temperature in a feedback loop to compensate for an inability to thermoregulate; ventilators are used to ensure sufficient oxygen when the respiratory system is either too premature or depressed; and orogastric or nasogastric (i.e., tube) feeding is used to compensate for the neonate's inability to actively suck and to coordinate sucking, swallowing, and breathing.
The attentiveness of staff in the neonatal intensive care unit (NICU) emphasizes the importance of observable physiological systems such as body movements, breathing, thermoregulation, and sucking to detect shifts in clinical status. Thus, although technology has contributed to the evaluation of physiological self-regulation through specialized biomedical monitoring equipment (e.g., computerized oxygen saturation, blood pressure, temperature, and heart rate monitors), the primary clinical indicators of autonomic regulation that promote homeostasis are still obtained through clinical observations.
Before the infant can master complex behavioral interactions with the environment, the infant must competently regulate autonomic processes. A goal of mammalian development is to become independent of the caregiver. There are several constraints on the development of self-regulatory skills including the status of neurons, neurophysiological systems, motor behavior control, and the availability and contingency of socioenvironmental stimulation. Although assessments of self-regulatory skills usually focus on global levels of motor and social behavior, these abilities are dependent upon physiological systems. In turn, physiological systems are dependent upon a neuronal substrate, which provides the boundary conditions. If there is damage to neural tissue, the ability to regulate both motor and visceral processes is limited. Neurons can be damaged by hypoxia, fever, trauma, and other insults such as drugs. Although neurons cannot be measured noninvasively in the infant, the functional output of populations of interconnecting neurons produce physiological responses such as sucking, breathing, and heart rate, which are easily monitored.
Self-Regulation and the Nervous System
Implicit in the evaluation of clinical status in the newborn is the assumption that the assessment reflects the quality of nervous system function. Although many assessments do not require detailed physiological monitoring, the systems observed (e.g., regularity of respiration, body movements, sucking responses, coloration of skin, etc.) provide insight into the competence of the nervous system and its ability to orchestrate complex self-regulatory physiological processes. Thus, underlying most assessment strategies is the assumption that the nervous system provides the management skills necessary to regulate internal physiological systems and plays a pivotal role in determining the newborn's success in navigating through the changing environment.
Self-regulation characterizes physiological systems. Weiner (1948) proposed a model of nervous system self-regulation to explain homeostasis. According to Weiner, homeostasis is an emergent property of a system that, via bidirectional communication, monitors and regulates the status of an organ to maintain an output level within a specific functional range. As illustrated in Figure 1, the system would include a central regulator that would determine the motor output to an organ after interpreting the information from the sensor (e.g., afferent feedback) that monitors the status of the organ.
To maintain physiological homeostasis, sensory pathways originating in peripheral organs (e.g., chemoreceptors and baroreceptors in the carotid sinus) convey information regarding physiological status and motor pathways (e.g., vagal and sympathetic pathways to the heart) change the output of peripheral organs. The sensory pathways from visceral organs originate in the periphery and usually terminate in the brainstem; however, many of the motor pathways originate in the brainstem and terminate in the periphery.
Physiological systems could be described as being composed of sensors that input information about the external (outside the body) and internal (within the body) environments, motor systems that control behavioral and visceral activity, and an integrative mechanism that evaluates the input from the sensors and determines the specifics of the motor output.
The study of normal psychological and behavioral development emphasizes the importance of the external environment. For example, individual differences in development are often associated with socioeconomic status, family function, nutrition, and stress factors. In contrast, partially because psychopathology can be observed in "healthy" environments, the study of psychopathological development emphasizes the importance of the internal environment (e.g., the brain and neural regulation of physiological systems). For example, pathological development is often associated with problems in brain development and dysfunctional physiological systems. This interest in organismic variation promotes research questions evaluating mechanisms through which feedback from visceral organs contributes to the organization and development of emotional, cognitive, and behavioral processes.
Self-regulation: A negative feedback system
Physiological systems regulating visceral state (e.g., heart rate, temperature, blood pressure) are self-regulatory. Self-regulatory systems adjust output to the changing input through a process known as feedback. When the feedback opposes the state of the system, it is known as negative feedback. When the feedback augments the state of the system, it is known as positive feedback. The room thermostat provides a functional metaphor for a negative feedback system. The room thermostat contributes to the temperature regulation by evaluating sensors to determine when the room temperature deviates from a predetermined range (i.e., homeostasis). If the room temperature drifts outside this range, the thermostat will trigger "motor" mechanisms to heat or cool the room to obtain a temperature within the previously defined "homeostatic" range.
The regulation of blood pressure represents a physiological feedback system with an objective to maintain levels within healthy limits. Because brain function requires a continuous supply of oxygenated blood, any drop in blood pressure is critical to survival and requires a rapid and appropriate physiological adjustment. In the healthy individual, drops in blood pressure are instantaneously detected by baroreceptors in the blood vessels. The baroreceptors send information to the brainstem and the brainstem sends a motor command to the heart to increase heart rate rapidly. As soon as blood pressure returns to normal limits, neural feedback slows heart rate. However, there are individuals who have defective feedback. For example, in the elderly or individuals using specific medications, the blood pressure feedback system may be depressed. For these individuals, when the blood pressure drops because of a posture shift, they may experience severe dizziness or even syncope. This experience is common in the elderly and frequently contributes to falls and severe injuries.
In contrast to the negative feedback systems, which characterize self-regulatory processes, there are also positive feedback systems. A malfunctioning room thermostat providing positive feedback would continue to augment the temperature until the system ceased functioning due to extreme heat or extreme cold. Thus, prolonged positive feedback is destructive to systems. For example, rage, severe anger, or panic might be viewed as a behavioral consequence of physiological positive feedback that promotes increased metabolic output. Consistent with the feedback model, the physiological cost of prolonged periods of positive feedback might compromise the health of the individual.
The characteristics of physiological feedback may change as a function of physiological, emotional, cognitive, or behavioral demands. For example, during periods requiring massive metabolic output, such as exercise, the feedback system must be vigilant and efficient to support the changing oxygen needs of the cardiovascular system. During less motorically demanding conditions, such as periods of drowsiness and sleep, the pattern of neural feedback may change and go through periods of dissociation. Additionally, it is possible that the ability to express emotional sensitivity or behavioral contingency might be related to the "gain" or "amplification" of the feedback from the viscera. Therapeutic drugs, such as clonidine, used for panic disorders, may alter the neural feedback system by dampening the impact of the afferent feedback from visceral organs. Thus, the study of abnormal development and psychopathology may prompt attention to the study of the development of normal feedback systems and the relation between physiological systems and emotional, cognitive, and behavioral development (cf, Cicchetti, 1993).
Homeostasis: Signs and signals of competent neural self-regulation
For the newborn, maintaining physiological homeostasis is crucial for survival. Homeostasis is not a passive process in which physiological systems remain constant. Rather, homeostasis is an active, neurally modulated process in which physiological systems vary within viable ranges.
The quality of homeostasis provides measurable variables that are related to clinical status. When the output of a system is above the functional level, output is decreased until the level drops into the functional range. The output level progressively decreases through the functional range. When the output drops below the functional level, the output is progressively increased to reach and pass through the functional range. This process of waxing and waning of output reflects the negative feedback property of our nervous system. Thus, healthy physiological systems have a characteristic rhythm that provides an important observable window of the status of the nervous system. For example, respiration, blood pressure, heart rate, and temperature exhibit rhythms that provide important clinical information.
The rhythms provide indicators of the quality of feedback characterizing the system as it attempts to maintain homeostasis. The physiological rhythms produced by central-autonomic feedback loops have two dynamic characteristics: (a) a period or time constant reflecting the temporal latency of the system to adjust or respond, and (b) a magnitude dimension reflecting the degree to which the system can deviate from a specific state. Both dimensions are modulated by higher brain structures and limited by neurochemical processes. Thus, by the nature of brain-autonomic regulation, autonomic response systems are time series, characterized by oscillations, with a period determined by the duration of the feedback loop, and an amplitude determined by central regulatory control.
Measures of heart rate oscillations, such as respiratory sinus arrhythmia (often used to assess cardiac vagal tone), dynamically reflect the bidirectional communication between the peripheral cardiovascular system and the brain. Under specific demand situations requiring shifts in metabolic output (e.g., stress- or survival-motivated responses, attention or social engagement, activity, fever, disease) the characteristics of the feedback, magnitude, valence and period may change. Thus, the interest in monitoring cardiac vagal tone during demand situations, and as a marker of physiological self-regulation, is justified.
There are times when the nervous system is compromised and the neural feedback regulating cardiopulmonary and thermoregulatory processes is deficient. The occurrence of apnea and bradycardia signal dysfunction in the neural regulation of cardiopulmonary function. Similarly, difficulties in maintaining body temperature when ambient temperatures are changing reflect difficulties in thermoregulation.
The care of the high-risk infant often requires interventions to regulate physiological processes that are no longer under appropriate neural control (i.e., efficient negative feedback). Following apnea and bradycardia, interventions such as physical movement of the infant, serve as potent stimuli to re-engage neural regulation of cardiopulmonary processes. When an infant has difficulty thermoregulating, rather than relying on neural feedback to vascular and cardiac processes, technology may use feedback from sensors that monitor body temperature to regulate ambient temperature. The common use in the NICU of heating units controlled by the newborn's body temperature is a functional example of a negative feedback system that compensates for defective self-thermoregulation.
The well-managed diabetic provides another example of external manipulation of a deficient internal feedback system. The diabetic has a defective feedback system that does not adequately regulate blood sugar through the endogenous release of insulin. To compensate for this problem, the diabetic must supplement the endogenous feedback system. To provide afferent feedback, blood is sampled and the amount of sugar in the blood is assessed. The individual's brain and associated cognitions interpret the afferent feedback and determine the appropriate amount of insulin required to regulate blood sugar within a functional level. To complete the feedback loop, motor systems are recruited to administer the insulin.
The human nervous system functions as a collection of several interacting self-regulatory negative feedback systems, each with a specific role. Sensors or receptors are located on the surface of the body to assess environmental changes and within the body to assess internal conditions. Motor systems control body movements and visceral organs. The feedback from internal sensors is interpreted by brainstem structures that contribute to the regulation of autonomic state (e.g., nucleus tractus solitarius, dorsal motor nucleus of the vague, nucleus ambiguus). The nervous system provides the infrastructure for all levels of self-regulation. Self-regulatory processes characterize various domains ranging from the overt behavioral strategies of the infant demanding caregiver attention, to subtle physiological shifts related to changes in thermoregulation, digestion, or cardiopulmonary function.
Self-regulation of physiological systems: Primary survival agenda
In the proposed model, the effectiveness of an assessment is dependent upon its sensitivity to measure the status of the nervous system. The success of an intervention is dependent upon the functional enhancement of the nervous system. Although developmental follow-up studies of high-risk infants focus on the complex regulation of motor, social, and cognitive behaviors, survival of the high-risk infant in the NICU is based upon successful regulation of the physiological systems that support growth and restorative processes. Initially, this regulation may involve extraneural feedback provided by external monitoring of critical care variables (e.g., temperature, heart rate, respiration, oxygen saturation). Then, based upon the monitored condition, clinical interventions (e.g., ventilation, ambient temperature, medication) are administered to aid physiological regulation. If these interventions were successful, the clinical course would reflect a shift from a dependence on extraneural regulation to neural self-regulation. Thus, assessment should be directed at evaluating the nervous system structures and functions that promote physiological states fostering growth and restorative processes. Moreover, when methods are developed to accurately monitor these systems, interventions could be developed that specifically enhance neural feedback and improve the function of these systems.
The vagal system: An indicator of survival-related self-regulation
The proposed model for assessment and intervention focuses on the vagal system, a physiological system uniquely important for the survival of the high-risk infant. The vagal system contributes to the regulation and coordination of survival processes including breathing, sucking, swallowing, heart rate, and vocalization. Dysfunction in these processes places the infant at survival risk and produces clinical indicators of risk such as apnea, bradycardia, difficulties in sucking and swallowing, and weak high-pitched cries.
Although the clinical indicators listed above appear to reflect divergent processes, they share an important neuroanatomical and neurophysiological substrate. The following four points highlight our knowledge and understanding of this substrate and justify why knowledge of this system may contribute to the development of psychophysiological assessment and clinical intervention strategies (a detailed and documented review of the physiological substrate of this system is reported by Porges, 1995b).
First, from a neuroanatomical level, sucking, swallowing, vocalizations, heart rate, and bronchial constriction are regulated by a common brainstem area. The regulation of these processes is dependent upon motor fibers emerging from a medullary nucleus known as the nucleus ambiguus. These myelinated motor fibers originate in the nucleus ambiguus and travel through the tenth cranial nerve, the vagus.
Second, the vagus contributes sensory and additional motor fibers to the self-regulation of physiological systems. The vagus contains sensory fibers that provide feedback and motor fibers originating in the dorsal motor nucleus of the vagus. Sensory fibers compose over 80% of vagal fibers. The vagal sensory fibers originate in several visceral organs (e.g., heart, lungs, stomach, pancreas, liver, intestines) and terminate in a brainstem area known as nucleus tractus solitarius. The vagal motor fibers originating in the dorsal motor nucleus of the vagus, unlike the myelinated motor fibers originating in the nucleus ambiguus, are unmyelinated and provide the primary motor control of the digestive system. However, the dorsal motor nucleus also projects to the bronchi and heart.
Third, nucleus tractus solitarius integrates sensory information from visceral organs and communicates, via interneurons, with the primary source nuclei of the vagus (i.e., nucleus ambiguus and dorsal motor nucleus). As illustrated in Figure 2, this feedback system regulates digestive and cardiopulmonary processes to foster growth and restoration. The afferent and efferent pathways conveying the bidirectional communication between the peripheral organs and the brainstem travel through the vagus. Note that the model describes potential feedback modulation (changing the magnitude or direction of the feedback) by other brain structures.
Fourth, neurophysiological research suggests that respiration rate is determined by a brainstem system that also outputs the respiratory rhythm to the heart and the bronchi. This neurophysiological drive to breathe is, in part, dependent upon the emergent properties of interneuronal communication between the nucleus ambiguus and the nucleus tractus solitarius. According to Richter and Spyer (1990) the interneuronal communication between the nucleus ambiguus and the nucleus tractus solitarius is the source of a rhythmic generator producing a cardiopulmonary rhythm that results in oscillations in bronchial constriction and heart rate at a frequency similar to spontaneous breathing. The rhythmic concordance among these processes may functionally enhance diffusion of oxygen, and coordinate breathing and heart rate with other processes dependent upon nucleus ambiguus motor fibers such as sucking, swallowing, and vocalization.
The above overview of the vagal system emphasizes the importance of vagal fibers in self-regulatory processes. The neuroanatomical descriptions and neurophysiological information regarding vagal function have been organized in the Polyvagal Theory (Porges, 1995b). The Polyvagal Theory provides a theoretical basis for specific clinical assessments and interventions in the NICU. Based upon the Polyvagal Theory, interventions may be developed that will not jeopardize the clinical status of the vulnerable infant. In contrast, the Polyvagal Theory also explains how stimulation of specific sensory systems may elicit life-threatening vagal reflexes. For example, oral-esophageal stimulation, commonly occurring during suction or during the insertion of the orogastric tube for gavage feeding, may elicit potent bradycardia.
Polyvagal Theory. The Polyvagal Theory emphasizes the functional difference between vagal fibers originating in two areas of the brainstem, the nucleus ambiguus and the dorsal motor nucleus of the vagus. The two types of pathways have different embryological origins, promote different response strategies, and provide the neurophysiological justification for new definitions and explanations of stress, distress, and distress vulnerability. The Polyvagal Theory explains the stress and distress experienced by the high-risk infant within the context of the evolution of the mammalian autonomic nervous system. Because of the evolutionary pressures associated with obtaining and maintaining oxygen resources and transporting oxygenated blood to the brain, a neomammalian vagal system developed from fibers originating in or migrating to the nucleus ambiguus. The neomammalian vagal system provides the neural control of the muscles that evolved from the primitive gill arches. The gill arches throughout evolution have been associated with the extraction of oxygen from the environment. Somatomotor pathways from the neomammalian vagal system innervate the larynx, pharynx, and esophagus and coordinate vocalizations, breathing, and sucking. Additionally, visceromotor pathways from this vagal system regulate bronchial constriction and heart rate. Thus, this system is involved still in obtaining oxygen from the environment, in diffusing oxygen in the blood, and in maintaining cerebral blood flow by regulating blood pressure. The evolutionarily older, reptilian vagal system, involves fibers originating in the dorsal motor nucleus.
The Polyvagal Theory emphasizes that the two vagal systems (neomammalian and reptilian) respond differently to a stressor. For healthy mammals, the initial response is mediated by the neomammalian vagus and is characterized by a rapid withdrawal of vagal tone. This functionally removes the potent vagal brake from the heart and facilitates an instantaneous increase in metabolic output (i.e., increased heart rate) to mobilize energy resources for the classic flight or fight response. Removal of the vagal brake increases strength and speed to deal with stress and to aid in obtaining oxygen resources. However, withdrawal of the vagal brake functionally degrades (i.e., reduces control in) the motor systems involving the nucleus ambiguus. Thus, stress would not only be associated with faster heart rate, but also with higher pitch vocalizations (e.g., cries) and difficulties in coordinating sucking, swallowing, and breathing. This, of course, is commonly observed in physiologically stressed or compromised infants.
The removal of the vagal brake is the neomammalian vagal response to stress. According to this model, stress characterized by removal of the vagal brake is not necessarily detrimental to the survival of the individual. Removing the vagal brake occurs often as an adaptive response to increase metabolic output to mobilize and react to survival-related demands. For example, the vagal brake will be removed during exercise, pain, attention, and even during the appetitive phases of eating. Successful postpartum adaptation is related to the infant's skill and neurophysiological capacity to regulate the vagal brake to differentially engage and disengage with the environment. Therefore, the high-risk infant who exhibits a systematic regulation of the vagal brake to environmental demands should have more positive social and cognitive outcomes (e.g., Doussard-Roosevelt, Porges, Scanlon, Alemi, & Scanlon, unpublished; Hofheimer, Wood, Porges, Pearson, & Lawson, 1995).
Removal of the "vagal brake" places the mammalian nervous system in a vulnerable state because: (a) it compromises homeostatic functions including those associated with blood pressure regulation, thermoregulation, food intake, and digestion; and (b) it places the nervous system at risk for reptilian vagal reactions. When the neomammalian vagus is in control, the heart and bronchi are protected from the reptilian vagus, and blood is appropriately oxygenated and transported to the brain. In the healthy infant, transitory behavioral states such as crying are characterized by a disengagement and self-soothing as a reengagement of the vagal brake. Infants with greater neomammalian vagal tone tend to be more reactive to the environment (DeGangi, DiPietro, Greenspan, & Porges, 1991; Porges, Doussard-Roosevelt, Portales, & Suess, 1994; Porter, Porges, & Marshall, 1988; Stifter & Fox, 1990) and more able to self-soothe and calm (Fox, 1989). Moreover, high-risk newborns with greater neomammalian vagal tone have fewer risk factors (Porges, 1992; Porges, 1995a) and have more optimal cognitive outcomes (Fox & Porges, 1985).
In contrast to the self-regulatory characteristics of the neomammalian vagus and the function of the vagal brake in staging responses as a function of environmental demands, the reptilian vagus responds with massive increases in vagal tone that slow the heart and constrict the bronchi. By reducing metabolic output, the reptilian vagus contributes to the conservation of available oxygen and promotes adaptive responses such as submerging and diving in aquatic environments or behaviorally freezing (i.e., feigning death) in terrestrial environments. Unfortunately, these response strategies, which are adaptive for reptiles, are potentially fatal for mammals. In mammals, this maladaptive strategy is observed in clinical settings as potentially lethal bradycardia and apnea. Based on the Polyvagal Theory, it has been proposed (Porges, 1995b) that fetal distress and sudden death, including sudden infant death syndrome, due to their neurogenic origins, are potential examples of the noxious impact of the reptilian vagal surge.
In a clinical setting it may be possible to evaluate the status of the neomammalian vagus to indicate stress and distress vulnerability. Vagal fibers to the heart from the nucleus ambiguus produce a respiratory rhythm, known as respiratory sinus arrhythmia. By applying time-series statistics to the beat-to-beat heart rate pattern (Porges, 1985), it is possible to extract a measure of respiratory sinus arrhythmia that accurately represents vagal influences from the nucleus ambiguus. In our research we are currently designating this component of cardiac vagal tone as Vna.
In the absence of nucleus ambiguus stimulation to the heart, the heart is vulnerable to surges in vagal tone from the dorsal motor nucleus that produce bradycardia. Data from my laboratory support this conclusion. We have observed that bradycardia in the fetus and newborn occur during periods of depressed respiratory sinus arrhythmia, the measure of vagal tone from the nucleus ambiguus. Moreover, the observed meconium in the amniotic fluid of fetuses who have suffered from hypoxia (i.e., fetal distress) provides additional support for this model, because vagal stimulation via the dorsal motor nucleus of the vagus to the lower digestive track produces meconium (Behrman & Vaughan, 1987). Thus, during fetal distress, when we know respiratory sinus arrhythmia is depressed, the fetuses exhibit dorsal motor nucleus vagal surges as evidenced by the expression of meconium.
In support of these conclusions, neuroanatomical research suggests that sudden infant death syndrome may be related to a delayed maturation of the myelinated fibers of the vagus (Becker, Zhang, & Pereyra, 1993). The neomammalian vagal motor fibers are myelinated, as are many of the vagal sensory fibers. Hypoxia or other neurophysiological insults that may impede vagal myelination or contribute to demyelination would result in defects in the negative feedback system regulating the neomammalian vagus. The engagement and disengagement of the vagal brake would be unreliable. Defects in this system are critical to survival, because the nucleus ambiguus is involved in the generation of respiratory rhythms and the coordination of sucking, swallowing, and breathing. Thus, evaluation of nucleus ambiguus function may map into a continuum of deficits in self-regulation processes.
Hierarchical model of self-regulation
Self-regulation processes observed in mammals may be organized into a hierarchical model with four levels (Porges, 1983). The hierarchical model emphasizes the dependence of higher order behavioral systems on more primary physiological systems. The model assumes that behaviors such as the organized motor activity associated with feeding, or the appropriate emotional regulation during social interaction, are dependent upon a more primary physiological substrate related to the systematic regulation of autonomic state. The model has four levels and is hierarchical, because each level requires successful functioning on the preceding level of organization (see Table 1).
Table 1. Hierarchical model of self-regulation
Level 1: Neurophysiological processes characterized by bidirectional communication between the brainstem and peripheral organs to maintain physiological homeostasis.
Level II: Physiological processes reflecting the input of higher nervous system influences on the brainstem regulation of homeostasis. These processes are associated with modulating metabolic output and energy resources to support adaptive responses to environmental demands.
Level III: Measurable and often observable motor processes including body movements and facial expressions. These processes can be evaluated in terms of quantity, quality, and appropriateness.
Level IV: Processes that reflect the coordination of motor behavior, emotional tone, and bodily state to successfully negotiate social interactions. Unlike those of Level III, these processes are contingent with prioritized cues and feedback from the external environment.
Level I is characteristic of homeostatic processes of physiological systems regulating the internal organs. Homeostatic regulation requires bidirectional processes of monitoring and regulating the internal organ via sensory and motor pathways between the brain and the internal organ. Level II processes require cortical, conscious, and often motivated influences on the brainstem regulation of homeostasis. Level III processes are observable behaviors that can be evaluated by the quantity, quality, and appropriateness of motor behavior. Level IV reflects the coordination of behavior, emotional tone, and bodily state to successfully coordinate social interactions.
Unique to this model is the assumption that complex behaviors, including social interactions, depend on physiology and how appropriately the nervous system regulates autonomic state. Thus, the regulation of autonomic state, via bidirectional communication between the brain and visceral organs, becomes the linchpin of physical, psychological, and social development. This article elaborates only on Level I and Level II processes, because these processes provide a developmentally antecedent substrate of emotional, cognitive, and behavioral regulation and must be mastered by all infants to ensure survival and successful adaption in the postpartum environment.
Level I processes: Physiological homeostasis
Level I processes represent the successful regulation of internal bodily processes via neural negative feedback systems composed of interceptors or sensory receptors monitoring internal bodily state, and their respective neural pathways. To maintain homeostasis, interoceptors originating in the body cavity (e.g., gastric, hepatic, enteric, cardiac, vascular, and pulmonary systems) transmit information via neural pathways to brainstem structures. The brainstem structures interpret the sensory information and regulate the visceral state by triggering motor pathways that either directly manipulate various organs via neural pathways (e.g., increase or decrease heart rate, constrict or dilate blood vessels, inhibit or facilitate peristaltic activity) or trigger the release of specific hormones or peptides (e.g., adrenalin, insulin, oxytocin, vasopressin, gastrin, somatostatin). Level I is associated with the organization and neural feedback mechanisms that characterize the maintenance of homeostasis.
Level II processes: Cost of doing business
The autonomic nervous system deals both with servicing the needs of the internal viscera and with responding to external challenges. Competence in the ability to trade off between internal and external needs may be used in developing definitions of adaptive behavioral strategies and homeostasis. Based upon this model, response strategies to environmental demands and homeostasis are interdependent. When there are no environmental demands, the autonomic nervous system services the needs of the internal viscera (e.g., internal organs such as the heart, lungs, and gut) to enhance growth and restoration. However, in response to environmental demands, homeostatic processes are compromised and the autonomic nervous system supports increased metabolic output, by down-regulating "growth and restoration" functions to deal with these external challenges. The central nervous system mediates the distribution of resources to deal with internal and external demands. This trade off between internal and external needs is monitored and regulated by the central nervous system.
Survival tasks of the high-risk newborn: In the NICU and post-NICU
Survival in the NICU is dependent upon achievement of Level I and Level II self-regulatory processes. Competence in regulating these processes enables the newborn to maintain and regulate homeostatic processes such as temperature, breathing, feeding, blood pressure, and sleeping. All other systems, including neurophysiological systems associated with cortical function, sensory integration, and motor control of observable behavior are dependent upon successful regulation of these more primary homeostatic functions. A similar argument can be made regarding the importance of brainstem control systems (e.g., nucleus ambiguus, nucleus tractus solitarius, dorsal motor nucleus of the vagus) as an infrastructure for emotional regulation, social behavior, and cognitive development. Thus, clinical care of the high-risk newborn should include assessments to evaluate, and intervention strategies to foster, development of nucleus ambiguus function.
Discharge from the NICU is directly related to competent self-regulation of Level I and Level II processes. In contrast, survival post-NICU is dependent upon processes attributed to Level III and Level IV. Successful adaption post-NICU, not only requires competent Level I and Level II processes, but is dependent upon the Level III and Level IV processes that require the regulation of motor behavior, emotional expression, cognitive processes, and social interactions.
The concept that early difficulties in self-regulation lead to problems in emotional and social development evolves from the clinical and theoretical work of Greenspan (1992). Greenspan has described a sequence of developmental milestones that may be equated with the hierarchical levels presented above. Although his work focuses on Level IV processes, he acknowledges the importance of more primary physiological systems related to sensory feedback and motor control. Greenspan has proposed that difficulties in these primary neurophysiologically dependent systems contribute to problems in impulse control, attention, concentration, creative thinking, affect integration, and social interactions. The current detailed descriptions of Level I and Level II processes and their dependence on the nucleus ambiguus, provide a neurophysiological model that complements these clinical observations.
Global assessment strategy. With the view that nucleus ambiguus function is critical to the survival risk of the newborn and our knowledge of how to monitor this function via respiratory sinus arrhythmia, we have the tools for a global neurophysiological assessment. A noninvasive assessment strategy might use a baseline or sleep measure of respiratory sinus arrhythmia to assess a Level I process and a feeding test to challenge the system to evaluate a Level II process. In older children, the autonomic substrate (i.e., Level I and Level II) might be evaluated during baseline and tasks associated with higher order processes. Baseline measures followed by tasks requiring Level III and Level IV processes, such as manipulating motor (e.g., activity level), cognitive (e.g., attentional), or social demands might be used to evaluate the child's autonomic tone (i.e., Level I) and ability to regulate autonomic state (i.e., Level II) to support higher level processes.
Level I assessments. To assess Level I, we have measured cardiac vagal tone (Vna) during periods of minimal environmental demand (e.g., sleep or quiet states) in the neonatal nursery. Research with this assessment procedure has reliably distinguished between high-risk and full-term newborns (Porges, 1992) and between risk groups of preterm newborns matched for gestational age (Porges, 1995b). Consistent with the hierarchical model, research has demonstrated that the respiratory sinus arrhythmia measure of vagal function in the NICU is related to cognitive outcome at 3 years of age (Doussard-Roosevelt, Porges, Scanlon, Alemi, & Scanlon, unpublished). Similarly, preterm newborns with greater respiratory sinus arrhythmia exhibited more social behavior and attention in the NICU (Hofheimer, Wood, Porges, Pearson, & Lawson, 1995).
Level II assessments. To assess Level II, we have measured changes in cardiac vagal tone (Vna) during periods of well-defined environmental demands (e.g., feeding) in the neonatal nursery. Two studies have been conducted to evaluate the effect of a feeding challenge on the pattern of Vna. In one study, an apparatus provided water or sucrose in solution when a newborn sucked (Porges & Lipsitt, 1993). In response to increased sweetness, the heart rate increased, the amplitude of respiratory sinus arrhythmia decreased (lower nucleus ambiguus vagal tone), and the sucking frequency increased. In a second study, Vna was evaluated during bottle feeding in a sample of NICU newborns (Portales, Porges, Abedin, Lopez, Young, Beeram, & Baker, unpublished). During the bottle feeding, Vna was depressed and heart rate increased. Following feeding, the levels returned to prefeeding baseline levels. Outcomes studies are being conducted using the feeding paradigm to challenge vagal control mediated by the nucleus ambiguus. In these studies, the pattern of vagal reactivity to the feeding challenge and recovery following feeding are used as Level II Assessment indices. These assessments will be evaluated to determine whether they are related to clinical risk factors and developmental outcome.
General intervention strategy
Measurement of respiratory sinus arrhythmia provides the capability to assess individual differences in neural regulation of homeostatic function in terms of nucleus ambiguus control. It is now possible to answer two questions: (a) whether individual differences in neural regulation are related to intervention effectiveness, and (b) whether interventions are beneficial or detrimental to survival-related physiological regulation. Thus, our knowledge regarding neurophysiological function may be useful in designing intervention strategies to promote increased nucleus ambiguus function.
Beneficial intervention strategies would stimulate specific visceral sensors to increase the function of the neomammalian vagus. The intervention would stimulate motor outflow and enhance the regulation and coordination of heart rate, respiration, vocalization, sucking, and swallowing. Positive developmental outcomes (e.g., weight gain, improved state regulation, longer periods of alertness, improved neurological development) would be the product of the improved regulation and coordination.
In contrast, detrimental intervention strategies would stimulate sensors that would increase the function of the reptilian vagus. Under conditions during which the dorsal motor nucleus vagus becomes dominant, the intervention might result in bradycardia, apnea, and digestive problems and produce compromised outcomes.
The sensory components of the trigeminal nerve (cranial nerve V) and the facial nerve (cranial nerve VII) provide the primary sensory input to the nucleus ambiguus. Therefore, interventions that provide sucking opportunities, oral stimulation, and facial movement would provide regulation challenges to the nucleus ambiguus vagal system and may be beneficial. In contrast, interventions that may trigger dorsal motor activity may be potentially dangerous. For example, shifting the posture of an infant will elicit baroreceptor responses including a heart rate change mediated via the vagus to regulate blood pressure. In the low-risk infant, this intervention exercises a negative feedback system that maintains cerebral blood pressure and contributes to the regulation of behavioral state. The system includes motor control of the cardiovascular system from the dorsal motor nucleus and the nucleus ambiguus. In the high-risk infant, with depressed nucleus ambiguus function, posture shifts may result in a massive bradycardia and loss of consciousness similar to the vaso-vagal syncopes observed in older adults with low nucleus ambiguus vagal tone.
Similarly, abdominal massage or pelvic manipulations may be detrimental to the high-risk infant. These interventions, similar to the posture shifts, may stimulate sensory pathways that stimulate both nucleus ambiguus and dorsal motor nucleus. Thus, in the presence of low nucleus ambiguus tone (a characteristic of the high-risk infant), these interventions also might elicit massive bradycardia and loss of consciousness.
Caution. It is extremely important to emphasize that many high-risk infants are in a compromised physiological state, defined by low nucleus ambiguus vagal tone. Interventions applied to these infants such as abdominal pressure during massage, baroreceptor stimulation by posture shifts, or lower esophageal stimulation during either suction or orogastric feeding might trigger massive dorsal motor nucleus reflexes, and in turn, bradycardia, apnea, and even loss of consciousness.
Conclusion
Although the methods described have focused on the high-risk infant during the neonatal period, the model may be generalized to study older children and even adults with behavioral and psychological problems. Associated with various psychological and psychiatric disorders are symptoms related to difficulties in state regulation. For example, hyperactivity or forms of attentional problems are associated with an inability to regulate the physiological substrate to support appropriate attentive and social behaviors. Similarly, individuals with inappropriate expressions of panic, terror, or rage, with their defining massive physiological responses, provide examples of an inability to self-regulate physiological state to self-soothe or to be contingent with social gestures being expressed by others to help calm them.
In support of the above generalizations, several studies have investigated Level I and Level II processes in clinical populations with the vagal tone measure (Vna). Level I assessments have been used to determine whether individual differences in tonic state of the vagal system measured via respiratory sinus arrhythmia (e.g., assessed during sleep or quiescent periods) are related to clinical risk factors. Level I methodology also has been used in specific experimental manipulations to evaluate potential mechanisms that may mediate psychopathology, such as panic disorders, or to evaluate the autonomic impact of the pharmacological treatments commonly used for psychiatric disorders. Level II assessments, involving the quantification of the pattern of vagal tone regulation in response to a clearly defined challenge, also have been used in clinical research.
Examples of Level I assessments
In an attempt to understand the mechanisms of how the nervous system regulates autonomic state during panic, George, Nutt, Walker, Porges, Adinoff, and Linnoila (1989) evaluated Vna (i.e., respiratory sinus arrhythmia) during hyperventilation and sodium lactate infusion, manipulations known to elicit panic. They reported that both manipulations produced a massive decrease in the vagal tone measure. Based upon the assessment model, these data reflect a severe deficit in Level I processes. Thus, consistent with the clinical observations of elicited panic and severe anxiety, the assessment would predict that self-regulatory physiological and behavioral functions would be compromised.
Other research has attempted to evaluate how psychotropic medication influences Level I processes. Based upon the assessment model, the degree that medication depresses Vna would affect behavioral and psychological outcome. For example, it would be predicted that if medication depressed Vna, it would compromise higher level processes, and behavior would not improve. Alternatively, it would be predicted that if medication increased or did not decrease Vna, the psychotropic effect on behavior would be optimized. McLeod, Hoehn-Saric, Porges, and Zimmerli (1992) demonstrated that the effectiveness of imipramine on general anxiety disorders (i.e., measured by the Hamilton Scale), was directly related to the influence imipramine had on Vna. If imipramine, due to its known anti-cholinergic effects, reduced Vna, then imipramine did not have beneficial effects. In contrast, if the patient did not exhibit depressed Vna in response to imipramine, behavioral outcome was optimized. Thus, if medication disrupted Level I processes, the higher level processes also were compromised.
The focus of this article has been on clinical applications of the proposed psychophysiological assessment model. There have been several investigations that demonstrate the utility of Level I assessments in clinical settings. Porges (1992) demonstrated that high-risk neonates had significantly lower Vna. Moreover, individual differences in Vna within the high-risk sample were related to clinical condition (Porges, 1995a) and predicted cognitive outcome (Doussard-Roosevelt, Porges, Scanlon, Alemi, & Scanlon, unpublished). Consistent with these findings Donchin, Constantini, Byrne, and Porges (1992) reported that in adults preneurosurgical levels of Vna predicted clinical course (i.e., neurological and cognitive outcomes).
Examples of Level II assessments
Level II assessments have been designed to evaluate the individual's ability to regulate the component of the vagal tone system originating in the nucleus ambiguus. Level II assessments assume that the regulation of Vna is mediated by higher central mechanisms that influence brainstem feedback to promote either immediate mobilization of energy resources or calming. Level II assessments are important in dealing with populations that appear to exhibit normal Level I activity. For example, we have reported that, independent of resting levels of Vna, children who do not systematically depress Vna during attention-demanding tasks are more likely to have behavioral regulation problems (DeGangi, DiPietro, Greenspan, & Porges, 1991). In a second sample we observed that this inability to regulate Vna at 9 months of age predicted behavioral problems at 3 years (Portales, Doussard-Roosevelt, Lee, & Porges, 1992). Consistent with the hierarchical model, both studies demonstrate that measures of Vna regulation are predictive, when baseline Vna, an indicator of Level I processes, does not predict outcome. Other research has evaluated the acute and tonic influences of alcohol and narcotics on the ability to regulate vagal reflexes. For example, Hickey, Suess, Newlin, Spurgeon, and Porges (1995) demonstrated that children exposed to opiates in utero, characterized by attentional problems, also exhibited difficulties in regulating vagal tone during sustained attention.
Research with Level II processes has been conducted to investigate the parallel between autonomic state regulation and affective regulation in infants. To evaluate individual differences in the dynamic covariation of affect tone and Vna, Bazhenova (1995) challenged Level II processes by eliciting various affective states. The Bazhenova study demonstrated that infants who exhibited a systematic parallel between shifts in affect tone and Vna exhibited more optimum social behavior and state regulation.
Research in my laboratory with newborn infants has focused on evaluating the feeding challenge as a Level II assessment. Preliminary research with feeding challenges demonstrates individual differences in Vna regulation while bottle feeding (Portales et al., unpublished), sucking (Porges & Lipsitt, 1993), or during orogastric feeding (DiPietro & Porges, 1991). We are currently developing a standardized Level II assessment for newborn infants that evaluates Vna regulation during feeding. The assessment procedure will evaluate Level I processes from a baseline recording of Vna during sleep and Level II processes from the Vna regulation in response to the feeding challenge. We are also testing the generality of the assessment model to evaluate Vna regulation (Level II processes) in older children in a variety of challenges related to sustained attention, emotion regulation, and social interactions.
Summary
The methods for assessment and intervention described in this article focus on a specific physiological system originating in the nucleus ambiguus. The nucleus ambiguus is a brainstem nucleus that coordinates sucking, swallowing, vocalizing, and breathing via vagal pathways. Moreover, vagal pathways from nucleus ambiguus provide the primary neural control of heart rate. Thus, nucleus ambiguus regulation of the heart is the neurophysiological substrate for all behaviors requiring a regulation of metabolic output to engage, disengage, and re-engage dimensions of the environment. By monitoring a rhythmic heart rate pattern (i.e., respiratory sinus arrhythmia) mediated by the nucleus ambiguus, it is possible to assess shifts in the competence of neural regulation in the infant, child, or adult. The methodology for assessing nucleus ambiguus function is available and can be generalized to older children and adults by devising tasks that require the individual to regulate nucleus ambiguus output to mobilize and cope with transitory environmental demands. Therefore, this technology may be used to noninvasively monitor nucleus ambiguus function in high-risk infants or other clinical populations, to assess relative risk, and to evaluate the effectiveness of specific interventions. Although this article has emphasized assessment, there is a great need to develop appropriate interventions. Research needs to be directed at designing age-specific interventions that will efficiently enhance the neural feedback critical to the function and regulation of the vagal system.
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