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15
A Neurovisceral Integration Model of Health Disparities in Aging

Julian F. Thayer and Bruce H. Friedman


Significant ethnic disparities exist in the health of elderly Americans that cover a broad range of disorders, from the psychological to the physiological, and that are manifested in both morbidity and mortality differences. The life expectancies of minority groups in the United States and other industrialized countries are often dramatically reduced (see Chapter 2, this volume; Williams, 1997). Moreover, morbidity is often greater in ethnic minorities. For example, hypertension rates in African Americans are among the highest in the world, with the age-adjusted rate being more than 50 percent higher than for white Americans. African Americans also develop hypertension earlier and have much higher average blood pressures and higher rates of stage 3 hypertension than whites. These factors combine to produce higher rates of stroke mortality (80 percent higher), heart disease mortality (50 percent higher), and hypertension-related end-stage renal disease (320 percent higher) than whites (National High Blood Pressure Education Program, 1997). The prevalence of diabetes also varies greatly by ethnic group. The prevalence of known diabetes in African Americans is more than 1.7 times the rate of whites, whereas for some Native American tribes, the rate is more than 5.2 times that of whites (Black, 2002).

A number of potential pathways, both institutional and individual, to these health disparities have been identified, and include differential access to care, differential treatment, differential exposure to environmental pathogens, and differential exposure to chronic stress (Krieger, 2000). In this latter category, discrimination and racism have been implicated. This stressor is believed to be able to elicit the perception of threat from the environ-



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Critical Perspectives on Racial and Ethnic Differences in Health in Late Life 15 A Neurovisceral Integration Model of Health Disparities in Aging Julian F. Thayer and Bruce H. Friedman Significant ethnic disparities exist in the health of elderly Americans that cover a broad range of disorders, from the psychological to the physiological, and that are manifested in both morbidity and mortality differences. The life expectancies of minority groups in the United States and other industrialized countries are often dramatically reduced (see Chapter 2, this volume; Williams, 1997). Moreover, morbidity is often greater in ethnic minorities. For example, hypertension rates in African Americans are among the highest in the world, with the age-adjusted rate being more than 50 percent higher than for white Americans. African Americans also develop hypertension earlier and have much higher average blood pressures and higher rates of stage 3 hypertension than whites. These factors combine to produce higher rates of stroke mortality (80 percent higher), heart disease mortality (50 percent higher), and hypertension-related end-stage renal disease (320 percent higher) than whites (National High Blood Pressure Education Program, 1997). The prevalence of diabetes also varies greatly by ethnic group. The prevalence of known diabetes in African Americans is more than 1.7 times the rate of whites, whereas for some Native American tribes, the rate is more than 5.2 times that of whites (Black, 2002). A number of potential pathways, both institutional and individual, to these health disparities have been identified, and include differential access to care, differential treatment, differential exposure to environmental pathogens, and differential exposure to chronic stress (Krieger, 2000). In this latter category, discrimination and racism have been implicated. This stressor is believed to be able to elicit the perception of threat from the environ-

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Critical Perspectives on Racial and Ethnic Differences in Health in Late Life ment, which in turn leads to a plethora of negative affective states, such as fear, anxiety, anger and hostility, and depression. Both acutely and chronically, these affective states may lead to negative health outcomes (Kiecolt-Glaser, McGuire, Robles, and Glaser, 2002; Krantz and McCeney, 2002). That ethnic minorities might be differentially exposed to racism-related stress and negative affect has been proposed as a possible causal factor in the observed health disparities (Clark, Anderson, Clark, and Williams, 1999; Williams and Neighbors, 2001). However, any comprehensive model of emotions and health must account for the complex mix of cognitive, affective, behavioral, and physiological concomitants of normal and pathological affective states and dispositions, and how these might impact health. In addition, the concept of stress is often invoked to explain the impact of psychosocial factors on physiological processes and health. However, this concept is plagued by a lack of a precise and widely accepted definition, and by a lack of specificity in the organismic mechanisms by which stress produces its effects (Eriksen and Ursin, 2002). Despite recent attempts to reconceptualize stress effects in terms of allostatic load (McEwen, 1998), the situation has not substantially improved (Eriksen and Ursin, 2002; Kiecolt-Glaser et al., 2002). The impact of multiple pathways on ethnic health disparities must be acknowledged, but this chapter focuses on psychosocial factors. Broadly defined in terms of stress, negative emotion, and perceived racism, the core question is how these psychosocial factors are instantiated in physiological processes that can lead to disease and death. With the added premise that ethnic minorities are differentially and excessively exposed to discrimination and racism, the underlying causes of the health disparities begin to be revealed. Due to the scope of the issues involved, coverage of the literature will be more illustrative than comprehensive. However, wherever possible, references to more comprehensive reviews and key primary sources are provided. We begin in a broad context within which to view the observed health disparities in the elderly by presenting evidence for the role of autonomic imbalance in disease and negative affective states and dispositions. The notion of appropriate energy regulation as a factor in health and disease is emphasized. Next, a brief description of a neurovisceral model of emotion regulation and dysregulation is offered, in which heart rate variability (HRV) is used to index important aspects of autonomic, affective, and cognitive system regulation. This model may help to explicate the complex interrelationships that exist in the connection between psychosocial factors on the one hand and health and disease on the other. This model utilizes a dynamical systems approach, and stresses the role of inhibitory processes via parasympathetic mechanisms in maintaining optimal energy regulation. A discussion follows in which perseverative thinking is viewed

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Critical Perspectives on Racial and Ethnic Differences in Health in Late Life as the core cognitive toxic factor. Evidence is presented on the relationship among perseverative thinking, HRV, and poor health outcomes. The central concomitants of perseverative behavior and their links to hypervigilance also will be considered. Next, the relevance of this model to health disparities is shown. Relevant experimental and correlational data in support of elements of the model are supplied, including how they might relate to health disparities. Finally, we offer recommendations for future research that might flesh out the model and further guide the understanding of health disparities in the elderly. AUTONOMIC IMBALANCE IN DISEASE AND NEGATIVE EMOTIONS There is growing evidence for the role of the autonomic nervous system (ANS) in a wide range of diseases. The ANS is generally conceived to have two major branches—the sympathetic system, associated with energy mobilization, and the parasympathetic system, associated with vegetative and restorative functions. Normally, the activity of these branches is in dynamic balance. For example, there is a well-documented circadian rhythm such that sympathetic activity is higher during daytime hours and parasympathetic activity increases at night. Other periodicities are present, and the activity of the two branches can be rapidly modulated in response to changing environmental demands. More modern conceptions of organism function based on complexity theory hold that organism stability, adaptability, and health are maintained through variability in the dynamic relationship among system elements (Friedman and Thayer, 1998a, 1998b; Thayer and Friedman, 1997; Thayer and Lane, 2000). Thus, patterns of organized variability, rather than static levels, are preserved in the face of constantly changing environmental demands. This conception, in contrast to homeostasis, posits that the system has multiple points of stability, which necessitate a dynamic organization of resources to match specific situational demands. These demands can be conceived in terms of energy regulation such that the points of relative stability represent local energy minima required by the situation. For example, in healthy individuals, average heart rate (HR) is greater during the day, when energy demands are higher, than at night, when energy demands are lower. Thus, the system has a local energy minimum or attractor for daytime and another for nighttime. Because the system operates “far from equilibrium,” the system is always searching for local energy minima to minimize the energy requirements of the organism. Consequentially, optimal system functioning is achieved via lability and variability in its component processes, and rigid regularity is associated with mortality, morbidity, and ill health (Lipsitz and Goldberger, 1992; Peng et al., 1994).

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Critical Perspectives on Racial and Ethnic Differences in Health in Late Life Another corollary of this view is that autonomic imbalance, in which one branch of the ANS dominates over the other, is associated with a lack of dynamic flexibility and health. Empirically, there is a large body of evidence to suggest that autonomic imbalance, in which typically the sympathetic system is hyperactive and the parasympathetic system is hypoactive, is associated with various pathological conditions (Malliani, Pagani, and Lombardi, 1994). In particular, when the sympathetic branch dominates for long periods of time, the energy demands on the system become excessive and ultimately cannot be met, eventuating in death. The prolonged state of alarm associated with negative emotions likewise places an excessive energy demand on the system. On the way to death, however, premature aging and disease characterize a system dominated by negative affect and autonomic imbalance. Like many organs in the body, the heart is dually innervated. Although a wide range of physiologic factors determines HR, the ANS is the most prominent. Importantly, when both cardiac vagal (the primary parasympathetic nerve) and sympathetic inputs are blocked pharmacologically (for example, with atropine plus propranolol, the so-called double blockade), intrinsic HR is higher than the normal resting HR (Jose and Collison, 1970). This fact supports the idea that the heart is under tonic inhibitory control by parasympathetic influences. Thus, resting cardiac autonomic balance favors energy conservation by way of parasympathetic dominance over sympathetic influences. In addition, the HR time series is characterized by beat-to-beat variability over a wide range, which also implicates vagal dominance. Lowered HRV is associated with increased risk of mortality, and HRV has been proposed as a marker for disease (Task Force of the European Society of Cardiology and the North American Society of Pacing Electrophysiology, 1996). Resting HR can be used as a rough indicator of autonomic balance, and several large studies have shown a largely linear, positive dose-response relationship between resting HR and all-cause mortality (see Habib, 1999, for review). This association was independent of gender and ethnicity, and showed a threefold increase in mortality in persons with HR over 90 beats per minute (bpm) compared to those with HRs of less than 60 bpm. It was suggested that this relationship is due to the role of HR as a major determinant of myocardial oxygen demand and the direct link of HR to the rate of myocardial energy use. Brook and Julius (2000) have recently detailed how autonomic imbalance in the sympathetic direction is associated with a range of metabolic, hemodynamic, trophic, and rheologic abnormalities that contribute to elevated cardiac morbidity and mortality. Although the relationship between HR and cardiovascular morbidity and mortality may be assumed, the fact that autonomic imbalance and HR are related to other diseases may not be as obvious. However, links do exist. For example, HRV has been shown to be associated with diabetes mellitus, and decreased HRV has been shown to

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Critical Perspectives on Racial and Ethnic Differences in Health in Late Life precede evidence of disease provided by standard clinical tests (Ziegler, Laude, Akila, and Elgwhozi, 2001). In addition, immune dysfunction and inflammation have been implicated in a wide range of conditions associated with aging including cardiovascular disease, diabetes, osteoporosis, arthritis, Alzheimer’s disease, periodontal disease, and certain types of cancers as well as declines in muscle strength and increased frailty and disability (Ershler and Keller, 2000; Kiecolt-Glaser et al., 2002). The common mechanism seems to involve excess proinflammatory cytokines such as interleuken 1 and 6 and tumor necrosis factor. Importantly, increased parasympathetic tone and acetylcholine (the primary parasympathetic neurotransmitter) have been shown to attenuate release of these proinflammatory cytokines, and sympathetic hyperactivity is associated with their increased production (Das, 2000; Maier and Watkins, 1998; Tracey, 2002). Thus, autonomic imbalance may be a final common pathway to increased morbidity and mortality from a host of conditions and diseases. Although the idea is not new (Sternberg, 1997), several recent reviews have provided strong evidence linking negative affective states and dispositions to disease and ill health (Friedman and Thayer, 1998b; Kiecolt-Glaser et al., 2002; Krantz and McCeney, 2002; Musselman, Evans, and Nemeroff, 1998; Rozanski, Blumenthal, and Kaplan, 1999; Verrier and Mittleman, 2000). All of these reviews implicate altered ANS function and decreased parasympathetic activity as a possible mediator in this link. An additional pathway between psychosocial stressors and ill health is an indirect one, in which psychosocial factors lead to poor lifestyle choices, including a lack of physical activity and the abuse of tobacco, alcohol, and drugs. Both sedentary lifestyle and substance abuse are associated with autonomic imbalance and decreased parasympathetic tone (Ingjaldsson, Laberg, and Thayer, 2003c; Nabors-Oberg, Sollers, Niaura, and Thayer, 2002; Reed, Porges, and Newlin, 1999; Rossy and Thayer, 1998; Weise, Krell, and Brinkhoff, 1986). In fact, the therapeutic effectiveness of smoking cessation, reduced alcohol consumption, and increased physical activity rest in part on their ability to restore autonomic balance and increase parasympathetic tone. In sum, autonomic imbalance and decreased parasympathetic tone in particular may be the final common pathway linking negative affective states and dispositions, including the indirect effects via poor lifestyle, to numerous diseases and conditions associated with aging as well as increased morbidity and mortality. THE MODEL IN A NUTSHELL A comprehensive model of emotions and health must account for the complex mix of cognitive, affective, behavioral, and physiological

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Critical Perspectives on Racial and Ethnic Differences in Health in Late Life concomitants of normal and pathological affective states and dispositions, and how these might impact health. In this chapter, a model is outlined that integrates some of these components into a functional and structural network that may help to guide the understanding of emotion and health. Functionally, this network involves autonomic, affective, and cognitive regulation, and structurally it entails reciprocal inhibitory circuits between prefrontal cortex and subcortical evolutionarily primitive motivational structures, that can be indexed by rhythmic activity of the cardiovascular system. Research that relates functional aspects of this circuitry to psychophysiological regulation will be briefly reviewed. We emphasize the relationships among autonomic, affective, and cognitive regulation in organism health, and propose a group of underlying physiological systems that integrate these functions in the service of self-regulation and adaptability. This network is placed in the context of a dynamical systems model that involves feedback and feedforward circuits, with special attention to negative feedback mechanisms and inhibitory processes. It will be shown that the negative behavioral states and dispositions associated with a relative autonomic sympathetic imbalance reflect a disinhibition of positive feedback circuits that are normally under tonic inhibitory control. Other models have also been proposed to account for the effects of emotions and stress on health and disease. The allostatic load model has garnered much recent attention, particularly in medical circles (McEwen, 1998). The recently proposed psychoneuroimmunology model highlights the increasing role that inflammation has been shown to play in a wide variety of diseases, including cardiovascular disease (Kiecolt-Glaser et al., 2002). The reactivity model has been the stalwart in psychophysiology and behavioral medicine (see Krantz and McCeney, 2002). The neurovisceral integration model (NIM) builds on these prior models, but has important differences from them as well. First, the NIM is a true multilevel model incorporating factors from the sociopolitical to the molecular. Second, the NIM specifies in detail the core cognitive toxic factor, that of perseverative thinking, and explicates its neural and physiological concomitants. Third, the NIM proposes the autonomic nervous system, with an emphasis on the parasympathetic nervous system, as the final common pathway linking psychological and physiological states and dispositions. Fourth, the NIM is based on a nonlinear dynamical systems perspective and highlights the role of feedback and feedforward networks and their interplay in the maintenance of the dynamic flexibility of the organism. Finally, the NIM emphasizes inhibitory, negative feedback processes and explicates their physiological substrates at both the central and peripheral levels. Thus the NIM incorporates many aspects of the prior models and is not contradictory to them, but expands on them in ways

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Critical Perspectives on Racial and Ethnic Differences in Health in Late Life that are needed to account for the extant data and to generate testable hypotheses for future research. The Central Autonomic Network Investigators have identified functional units within the central nervous system (CNS) that support goal-directed behavior and adaptability. One such entity is the central autonomic network (CAN) (Benarroch, 1993, 1997). Functionally, this network is an integrated component of an internal regulation system through which the brain controls visceromotor, neuroendocrine, and behavioral responses that are critical for goal-directed behavior, adaptability, and health. Structurally, the CAN includes the anterior cingulate, insular, orbitofrontal, and ventromedial prefrontal cortices, the central nucleus of the amygdala, the paraventricular and related nuclei of the hypothalamus, the periaquaductal gray matter, the parabrachial nucleus, the nucleus of the solitary tract (NTS), the nucleus ambiguous, the ventrolateral medulla, the ventromedial medulla, and the medullary tegmental field (see Figure 15-1). These components are reciprocally interconnected such that information flows bidirectionally between lower and higher levels of the CNS. The primary output of the CAN is mediated through preganglionic sympathetic and parasympathetic neurons that innervate the heart via the stellate ganglia and vagus nerve, respectively. The interplay of these inputs to the cardiac sino-atrial node produces the complex variability that characterizes the HR time series (Saul, 1990). Thus, the output of the CAN is directly linked to HRV. Notably, vagal influences dominate cardiac chronotropic control (Levy, 1990). In addition, sensory information from peripheral end organs such as the heart and the immune system are fed back to the CAN. Thus, HRV is an indicator of central-peripheral neural feedback and CNS-ANS integration. Moreover, the CAN has many features of a dynamical system. First, the components of the CAN are reciprocally interconnected, allowing for unbroken positive and negative feedback interactions and integration of autonomic responses. Second, the CAN consists of numerous parallel, distributed pathways, which permit multiple avenues to a given response. For example, a HR change of 72 to 90 bpm can be attained by various permutations of sympathetic and vagal input, including increased sympathetic or decreased vagal activity or some combination of the two, or by other processes such as circulating hormones. Moreover, within the CAN, direct and indirect paths can regulate output to preganglionic sympathetic and parasympathetic neurons. Third, CAN activity is state dependent and thus sensitive to initial conditions (see Glass and Mackey, 1988). The CAN receives and integrates visceral, humoral, and environmental information; organizes autonomic, endocrine, and behavioral responses to

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Critical Perspectives on Racial and Ethnic Differences in Health in Late Life FIGURE 15-1 Central nervous system structures involved in neurovisceral integration.

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Critical Perspectives on Racial and Ethnic Differences in Health in Late Life environmental challenges; and is under tonic inhibitory control. This inhibition is achieved by γ-aminobutyric acid (GABA), the main inhibitory CNS neurotransmitter, emanating from interneurons within the NTS. Disruption of this pathway may lead to hypertension and sinus tachycardia, and represents a disinhibition of sympathoexcitatory circuits in the CAN (Benarroch, 1993, 1997; Masterman and Cummings, 1997; Spyer, 1989). Other functional units within the CNS serving executive, social, affective, attentional, and motivated behavior in humans and animals have been identified (Damasio, 1998; Devinsky, Morrell, and Vogt, 1995; Masterman and Cummings, 1997; Spyer, 1989). One such network has been termed the anterior executive region (AER; Devinsky et al., 1995). The AER and its projections regulate behavior by monitoring the motivational quality of internal and external stimuli. The AER network has been called the “rostral limbic system” and includes the anterior, insular, and orbitofrontal cortices, amygdala, periaquaductal gray, ventral striatum, and autonomic brainstem motor nuclei. Damasio (1998) has recognized a similar neural “emotion circuit” for which there is considerable structural overlap with the CAN and the AER (Thayer and Lane, 2000). We propose that the CAN, the AER network, Damasio’s (1998) “emotion circuit,” and related systems (Masterman and Cummings, 1997; Spyer, 1989) represent a common central functional network recognized by different researchers from diverse approaches. This CNS network is associated with the processes of response organization and selection, and serves to control psychophysiological resources in attention and emotion (Friedman and Thayer, 1998a, 1998b; Thayer and Friedman, 1997). Additional structures are flexibly recruited to manage specific behavioral adaptations. This sparsely interconnected neural complex allows for maximal organism flexibility in accommodating rapidly changing environmental demands. When this network is either rigidly coupled or completely uncoupled, the ability to recruit and utilize appropriate neural support to meet a particular demand is hampered, and the organism is thus less adaptive. Autonomic Regulation Autonomically mediated HRV is useful as an index of neurovisceral integration and organismic self-regulation. The interaction of sympathetic and parasympathetic outputs of the CAN at the sino-atrial node produces the complex beat-to-beat variability that marks a healthy, adaptive organism. Vagal activity dominates HR control, and thus HR is under tonic inhibitory vagal control (Levy, 1990; Uijtdehaage and Thayer, 2000). HRV is also associated with prefrontal cortex activity (Lane, Reiman, Ahern, and Thayer, 2001), and the prefrontal cortex has been inversely related to

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Critical Perspectives on Racial and Ethnic Differences in Health in Late Life subcortical activity in structures such as the amygdala that have been implicated in primitive motivation systems (Davidson, 2000). Several lines of research point to the significance of HRV in emotions and health. Decreased HRV is linked with a number of disease states, including cardiovascular disease, diabetes, obesity, and lack of physical exercise (Stein and Kleiger, 1999). Reduced vagally mediated HRV is also associated with a number of psychological disease states, such as anxiety, depression, and hostility. For example, low HRV is consistent with the cardiac symptoms of panic anxiety as well as with its psychological expressions in poor attentional control and emotion regulation, and behavioral inflexibility (Friedman and Thayer, 1998a, 1998b). Similar reductions in HRV have been found in depression (Thayer, Smith, Rossy, Sollers, and Friedman, 1998), generalized anxiety disorder (Thayer, Friedman, and Borkovec, 1996), and posttraumatic stress disorder (Cohen, Matar, Kaplan, and Kotler, 1999). Low levels of vagal cardiovascular influence serve to disinhibit sympathoexcitatory influences. Due to differences in the temporal kinetics of the autonomic neuroeffectors, sympathetic effects on cardiac control are relatively slow (order of magnitude seconds) compared to vagal effects (order of magnitude milliseconds; see Saul, 1990). Thus, when this rapid vagal cardiac control is low, HR cannot change as quickly in response to environmental changes. In this view, the prefrontal cortex modulates subcortical motivational circuits to serve goal-directed behavior. When the prefrontal cortex is taken “offline” for whatever reason, a relative sympathetic dominance associated with disinhibited defensive circuits is released. Human evidence for the inhibitory role of the frontal cortex comes from a recent study of HR and HRV before and after right- and left-side intracarotid sodium amobarbital (ISA) injection (Ahern et al., 1994). HR changes were similar during each hemisphere’s pharmacological inactivation. During the 10-minute inactivations of either hemisphere, HR increased, peaked around the third minute, and gradually declined toward baseline values. These data indicate that the frontal cortex exerts tonic inhibition on brainstem sympathoexcitatory circuits. There were lateralized effects: larger and faster HR increases occurred during right-hemisphere inactivation. Moreover, vagally mediated HRV decreases were also greater in the right-hemisphere inactivations, mirroring the hemispheric effects on HR. These results support anatomical and physiological findings that right-hemispheric autonomic cardiac inputs are associated with greater chronotropic (rate) control. The effects of the ISA test are largely restricted to anterior neural structures, which include the orbital and medial prefrontal cortices (Ahern et al., 1994; Hong et al., 2000). These areas are linked broadly with biopsychological functions such as affective, cognitive, and autonomic regulation (Thayer and Lane, 2000). Additionally, these structures are related to

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Critical Perspectives on Racial and Ethnic Differences in Health in Late Life inhibitory control of behavior in general (Roberts and Wallis, 2000) and cardiac behavior in particular (Verberne and Owens, 1998). It is noteworthy that direct and indirect pathways connect these areas with vagal motor output regions (Ter Horst, 1999). Many researchers have proposed inhibitory cortical-subcortical circuits (Benarroch, 1993, 1997; Masterman and Cummings, 1997; Mayberg et al., 1999; Spyer, 1989), but our group is the first to tie these circuits to HRV (Thayer and Friedman, 2002; Thayer and Lane, 2000). The ISA test results provide compelling evidence that cortical structures tonically inhibit sympathoexcitatory circuits by way of vagal mechanisms. It has been proposed that the prefrontal cortex is taken “offline” during emotional stress to let automatic, prepotent processes regulate behavior (Arnsten and Goldman-Rakic, 1998). This selective prefrontal inactivation may be adaptive by facilitating predominantly nonvolitional behaviors associated with subcortical neural structures such as the amygdala to organize responses without delay from the more deliberative and consciously guided prefrontal cortex. In modern society, however, inhibition, delayed response, and cognitive flexibility are vital for successful adjustment and self-regulation, and prolonged prefrontal inactivity can lead to hypervigilance, defensiveness, and perseveration. A common reciprocal inhibitory cortical-subcortical neural circuit may structurally link psychological processes such as emotion with health-related physiology, and this circuit can be indexed with HRV. This neural network permits the prefrontal cortex to inhibit subcortical structures associated with defensive behaviors, and thus promote flexible responsiveness to environmental changes. For example, when faced with threat, tonic inhibitory subcortical control can be withdrawn quickly, leading to sympathoexcitatory survival (“fight or flight”) responses. However, when this network is disrupted, a rigid, defensive pattern emerges with associated perseverations in cognitive, affective, and autonomic behavior. This protracted state of action readiness and associated sympathetic activity may be the pathogenic state underlying the increased morbidity and mortality found in chronic negative psychological states and dispositions. Affective Regulation Affect regulation is a valuable skill that has clear implications for health. Emotions represent a distillation of an individual’s perception of personally relevant environmental interactions, including not only challenges and threats but also the ability to respond to them (Frijda, 1988). Viewed as such, emotions reflect the integrity of one’s ongoing adjustment to constantly changing environmental demands. Emotions have also been characterized as an organism’s response to the environment that allows for rapid

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Critical Perspectives on Racial and Ethnic Differences in Health in Late Life cognitive challenge. Stereotype threat occurs when members of stereotyped groups find themselves in situations in which others may view them stereotypically such that the pressure to perform well is increased. Importantly, they also found that MAP was elevated during an intervening rest period when performance was not expected, but rumination or perseverative thinking may have occurred. Finally, Chen and Matthews (2001) have recently reported that low socioeconomic status (SES) and African-American children interpret ambiguous scenarios as conveying more hostile intent and inducing greater feelings of anger. In addition, these appraisals were associated with increased vascular responses as measured by impedance cardiography. Importantly, for low-SES African-American children, these appraisals and feelings were associated with vascular responses 3 years later. Thus these appraisal biases grew stronger over time in the African-American children and appeared to sensitize them to interpret ambiguous situations as more and more threatening over time. The authors suggest that this may be the result of the greater exposure of the African American children to discrimination and racism. Similar results have been reported in adult African Americans. Merritt, Bennett, and Williams (2002) found that in response to a story about a negative social interaction in which the actors were ambiguous with respect to ethnicity, the African-American males showed elevated MAP and diastolic blood pressure responses when they reported greater perceptions of racism evident in the story. Again, these elevated responses persisted into recovery periods when the actual stressor was no longer present, but when rumination and perseverative thinking were likely to occur. Taken together, these studies provide empirical support for the psychological profile described earlier and its deleterious effects in African Americns. Due to the excess energy demand that autonomic imbalance places on the organism, individuals exposed to discrimination and racism may have a kind of premature aging that speeds their way to death and disability. The fact that autonomic imbalance continues to predict morbidity and mortality into old age when other risk factors have lost their predictive power adds further to the utility of the neurovisceral integration model in the understanding of health disparities in the elderly. Preliminary Data in Support of the Model We recently completed a pilot study that sought to examine in an elderly African-American sample some of the aspects of the model we have outlined. The total sample included 445 African Americans residing in east Baltimore. Psychophysiological assessment was completed on a subsample of 106 participants (50 males, 56 females) as part of the Healthy Aging in Nationally Diverse Samples (HANDLS) study that has been initiated at the

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Critical Perspectives on Racial and Ethnic Differences in Health in Late Life Intramural Research Program of the National Institute on Aging. This study was designed to examine the nature of health disparities using a multilevel approach ranging from the molecular to the social. Briefly, blood pressure and HR were continuously monitored during administration of two subtasks of the Perception of Affect Test (PAT) in this African-American sample. The PAT involved asking subjects to evaluate emotional expressions (and their intensity) in faces and sentences. Those who were able to correctly identify emotions in these stimuli showed lower blood pressure and total peripheral resistance responses as well as decreased depression scores. Older persons (age 52 and higher) performed more poorly than younger ones at correctly identifying emotions, and older men specifically had more difficulty in correctly identifying disgust and fear than their female counterparts. Older African-American males, therefore, showed the greatest deficits in emotional processing and the largest total peripheral resistance responses to the tasks. A more thorough examination of the physiological responses indicated that HR and blood pressure increased from baseline in response to completion of the PAT tasks. Notably, blood pressure remained elevated during the subsequent recovery period. Indices of blood pressure, cardiac output, and total peripheral resistance revealed signs of elevated peripheral resistance during recovery. In addition, sympathetic (vascular) measures of HRV (reduced high-frequency and increased low-frequency power) and blood pressure variability (reduced high-frequency power) increased during recovery. Previous research showing vascular hyperreactivity among African Americans supports the present results (Brosschot and Thayer, 1999; Jones, Andrawis, and Abernethy, 1999). The present data further suggest that high vascular reactivity may be associated with psychosocial factors. In this sample, higher levels of depressive symptoms were related to larger total peripheral resistance during task and recovery. In older women, self-reported loneliness was positively correlated with total peripheral resistance at baseline and recovery. These results underscore the multiple levels of system function that may contribute to health disparities in cardiovascular disease, especially hypertension. A series of carefully selected genetic polymorphisms implicated in cardiovascular disease will be studied in future work to assess genetic contributions to autonomic balance. These are (1) angiotensin-converting enzyme (ACE) insertion/deletion mutation, (2) endothelial nitric oxide synthase (eNOS) G894T mutation, (3) eNOS T786C mutation, (4), angiotensinogen M235T mutation, (5) apolipoprotein E polymorphisms, and (6) serotonin transporter 5-HTTLPR polymorphism. Common features of these mutations are allelic frequency in populations studied greater than 0.2, association with cardiovascular disease (congestive heart failure, hypertension, myocardial infarction) and/or specific personality traits, and relation to a

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Critical Perspectives on Racial and Ethnic Differences in Health in Late Life measurable physiological difference among genotypes (e.g., decreased nitric oxide production, impaired angiotensin II formation, altered lipoprotein pattern, decreased serotonin transporter transcription efficiency). The study population will be genotyped for this array, and genotype patterns of the six genes as well as single polymorphisms will be linked to variability subgroups in ANS function using quartile analyses. Preliminary observations indicate that high-frequency HRV is decreased in the basal state in the DD genotype of the ACE insertion/deletion polymorphism (Thayer et al., 2003), and that the allelic frequency of the eNOS G894T allele is markedly decreased in the HANDLS study population as compared to a white control group. This finding is intriguing because the T allele has been associated with increased likelihood of cardiovascular disease in other populations. If confirmed, this observation would exclude this source of cardiovascular risk in this African-American population. The DD phenotype of the ACE insertion/deletion gene has been associated with increased levels of circulating ACE and increased risk of sudden cardiac death in some populations. Our finding of decreased HRV and decreased baroreflex sensitivity in the DD phenotype is consistent with the literature linking this phenotype with increased cardiovascular disease risk. These preliminary findings attest to the promise of the candidate gene approach to better understand sources of variability in ANS function. These preliminary data also suggest that psychosocial factors are related to physiological processes that have major implications for the health disparities observed in the United States. For example, depression, which has been suggested as a primary factor in the greater rates of hypertension in African Americans, was associated with both poor affective regulation and increased peripheral resistance. As detailed earlier, increased peripheral resistance is associated with autonomic imbalance via sustained activity in the amygdala and with hypervigilance and perseverative thinking. Increased peripheral resistance is also related to established hypertension and insulin resistance, and thus plays a role in both cardiovascular disease and diabetes (Brook and Julius, 2000). Genetic factors also have been implicated in the health disparities, but our data suggest that at least one genetic polymorphism associated with increased risk in whites may not be a factor in African Americans (see Chapter 8, this volume). Another polymorphism, however, was found to have a relationship with HRV, and thus may interact with psychosocial factors to produce individual differences in disease risk. It is notable in this context that merely having a particular polymorphism is not sufficient to produce risk—the polymorphism must be expressed. Gene expression is a result of a complex process that includes exposure to environmental factors that can determine the expression of a cascade of genetic influences, the outcome of which is difficult to predict.

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Critical Perspectives on Racial and Ethnic Differences in Health in Late Life FUTURE DIRECTIONS AND RECOMMENDATIONS FOR RESEARCH There are a number of important directions for future research. First and foremost, this research must take into account the requisite multiple levels of analysis to explicate the complex factors that contribute to the health disparities (Anderson, 1999; Brosschot and Thayer, 1998). The interaction of factors across these levels will be the source of many insights. This type of multidisciplinary research must face the current grant review system that often establishes narrowly focused study sections, which may miss the value of multilevel initiatives. In addition, longitudinal, prospective studies will be necessary to untangle the causal factors that lead to the observed health disparities. These studies will require a major commitment on the part of funding agencies. It will also be necessary to examine factors across generations, and this will also tax the current review and funding structure. More specific recommendations for research are also justified, such as the need to examine within-ethnic group variability. That is, individual differences exist within each ethnic group. For example, preliminary results of the ACE insertion/deletion polymorphism reported earlier suggest an intraethnic group source of variability that may modify the impact of other genetic as well as psychosocial influences. Such factors need to be identified and explored. Related to this need is the call for examination of intraindividual variability as distinct from interindividual variability. Relationships found among variables between individuals may not generalize to the relationships found among the same variables within individuals (Thayer and Lane, 2000). Thus, the repeated measurement of individuals over time is necessary to explicate those relationships at the individual level (Friedman, 2003). Finally, studies must address the interplay of physiological, behavioral, affective, cognitive, and social processes and their impact on health, health behaviors, and disease. The neurovisceral integration model offers a framework to integrate such work across levels of analysis. It is key that the central nervous system be included, which entails neuroimaging and neuropsychological research to tap brain processes that support and accompany the many complex factors involved in health and disease in aging. REFERENCES Aggleton, J.P., and Young, A. (2000). The enigma of the amygdala: On its contribution to human emotion. In R.D. Lane and L. Nadel (Eds.), Cognitive neuroscience of emotion (pp. 106-128). New York: Oxford University Press.

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