Heart Rate Measures of Psychological States and Processes Multiple Determinism

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There is now an extensive history of theory and research on the potential links between psychological states, autonomic regulation, and disease processes. A common measure in this literature has been heart rate. The electrical signature of the heart beat is readily recorded as the electrocardiogram (EKG) by noninvasive surface electrodes, and heart rate has been known for centuries to be sensitive to psychological states. It is theorized, for example, that decreases in heart rate are triggered by an external direction of attention, a decrease in arousal, passive coping, or an orienting response; whereas increases in heart rate have been said to reflect inwardly directed attention, an increase in arousal, effort, active coping, or a startle or defensive response (Graham, 1984; Lacey & Lacey, 1980; Obrist, 1981). A potential advantage of heart rate is the fact that it may reflect implicit psychological states in the absence of verbal or other behavioral actions and thus may provide a metric of psychological processes that may otherwise not be apparent.

The principle of multiple determinism, however, cautions against an overly simplistic interpretation of heart rate and heart rate change. Not only is there a wide range of psychological states or processes that influence heart rate, physical (e.g., temperature, posture) and physiological (e.g., activity, blood pressure) variables also impact heart rate. Hence, the utility of heart rate as an index of psychological processes is dependent on the rigor of the experimental design and the interpretive logic to be applied. This is underscored by the high error rates (both hits and misses) in the misapplication of physiological measures to the detection of deception (see Committee report, 2003; Lykken, 1998).

Part of the difficulty in this area relates to the multiple mappings across levels of organization and analysis. Although a fear stimulus may alter heart rate, there are many translations in this cascade: from the stimulus to percept, from percept to emotion, and from emotion to autonomic outflows. There is one further translation involved as the heart is not an autonomic organ, per se, but is merely regulated by the autonomic nervous system. As each translation likely entails multiple mappings from one stage of processing to the next, the overall intricacy in psychophysiological relations can be staggering. The corollary of proximity emphasizes the advantages of bridging across more proximal levels. A major goal of multilevel research is to progressively elucidate the mapping between disparate levels by building a series of local bridges among more adjacent levels.

The measurement model: heart versus autonomic outflow. The heart is dually innervated by the sympathetic and parasympathetic divisions of the autonomic nervous system, with the sympathetic system exerting a positive chronotropic effect (increasing heart rate) and the parasympathetic system exerting a negative chronotropic influence (decreasing heart rate). Changes in heart rate represent at best an indirect reflection of autonomic control. One legacy from the Walter Cannon era is that the autonomic branches are subject to reciprocal central control, with increases in activity of one branch associated with decreases in the activity of the other (see Berntson & Cacioppo, 2000; Berntson, Cacioppo, & Quigley, 1991). Within this conceptual framework, heart rate should reflect the state of sympathetic-parasympathetic balance, and this appears to hold for many autonomic reflexes that are organized at lower levels of the brain stem. Higher neurobehavioral substrates, however, can inhibit, modulate, or bypass lower reflex substrates and thereby exert broader and more flexible control over the autonomic branches (Berntson & Cacioppo, 2000; Berntson et al., 1991).

In behavioral contexts, one can see not only the classical reciprocal mode of control, but also independent changes of the autonomic branches, or even the concurrent coactivation or coinhibition of both branches. This clearly necessitates an expansion of the theoretical model, and hence the measurement model, from the classical bipolar continuum from sympathetic to parasympathetic dominance, to a bivariate autonomic space that more appropriately characterizes the multiple modes of control. As illustrated in Figure 12.1, the bivariate model subsumes the bipolar model for a reciprocal mode of control, but also expands this model to capture independent or coactive changes that cannot be represented in the bipolar model. This in turn raises serious questions about the utility of heart rate measures as an index of autonomic outflow, as increases in heart rate, for example, could result from an independent increase in sympathetic control, an independent decrease in parasympathetic control, a sympathetically domi

FIGURE 12.1. Conceptual models of autonomic control. Left: Bipolar model of reciprocal sympathetic/parasympathetic control. Right: Bivariate model of sympathetic and parasympathetic control that allows independent and coactive as well as reciprocal modes of autonomic response.

nated coactivation, or a parasympathetically dominated coinhihition. This ambiguity is illustrated by the isofunctional contour lines in the three-dimensional map of Figure 12.2, which illustrates the chronotropic state of the heart as a function of location within the autonomic plane.2 These contour lines illustrate loci within the autonomic plane (i.e., different combinations of sympathetic and parasympathetic activities) that translate into equivalent chronotropic states. Consequently, the chronotropic state of the heart does not map simply on patterns of autonomic outflow, as a given chronotropic state is ambiguous with regard to its autonomic origins. Because neurobehavioral substrates control autonomic outflows, not the heart directly, measures of the chronotropic state of the heart necessarily entail a loss of fidelity in psychophysiological mappings.

Metrics of autonomic space. Differences in the modes of cardiac control for physiological reflexes and psychological contexts are illustrated by a human study of autonomic responses to an orthostatic stressor (assumption of an upright posture) and to psychological stressors (mental arithmetic, speech stressor, and speeded reaction time task). Before considering those results, however, a measurement issue must be addressed. The change in measurement model from a bipolar to a bivariate representation has obvious implications for experimental dependent measures. If heart rate or heart period are not adequate, how does one measure autonomic outflows? That is, what constitutes a valid measure of sympathetic and parasympathetic activities? In anesthetized animal studies, direct recordings have been made of neural firing in sympathetic and parasympathetic cardiac nerves. This is not feasible in human subjects, however, and has limited applicability even in animals as the requirement for anesthesia precludes meaningful psychophysiological investigations. Microneurography (using a fine microelectrode) has been applied to

2From here on, the chronotropic state of the heart will be designated in the metric of heart period, or the reciprocal of heart rate. The former has advantages as heart period is more linearly related to neural activity within the autonomic branches.

FIGURE 12.2. Three-dimensional autonomic space representation of chronotropic control of the heart. The effector surface depicts the heart period level for all possible loci within the autonomic plane. Parasympathetic and sympathetic axes are scaled in proportion to the extent of their functional range of control, and the curvature in the surface reflects nonlinear-ities in these controls. Beta (on the abscissa) illustrates the heart period in the absence of autonomic control. The curved lines on the autonomic plane are isofunctional contour lines, which represent varying combinations of sympathetic and parasympathetic control that yield comparable heart period effects. Reprinted from Behavioral Brain Research, 94, Berntson, Sarter, and Cacioppo "Anxiety and Cardiovascular Reactivity: The Basal Forebrain Cholinergic Link," 225-248. Copyright (1998), Elsevier.

FIGURE 12.2. Three-dimensional autonomic space representation of chronotropic control of the heart. The effector surface depicts the heart period level for all possible loci within the autonomic plane. Parasympathetic and sympathetic axes are scaled in proportion to the extent of their functional range of control, and the curvature in the surface reflects nonlinear-ities in these controls. Beta (on the abscissa) illustrates the heart period in the absence of autonomic control. The curved lines on the autonomic plane are isofunctional contour lines, which represent varying combinations of sympathetic and parasympathetic control that yield comparable heart period effects. Reprinted from Behavioral Brain Research, 94, Berntson, Sarter, and Cacioppo "Anxiety and Cardiovascular Reactivity: The Basal Forebrain Cholinergic Link," 225-248. Copyright (1998), Elsevier.

measure autonomic neural activity in conscious humans, but this technique is only applicable for rather superficial autonomic nerves (e.g., Macefield, Elam, & Wallin, 2002).

Another approach to measuring the separate contributions of the autonomic branches to cardiac control entails pharmacological blockade of the branches. Blockade of the parasympathetic branch, for example, will prevent the action of that branch and reveal the isolated contribution of the sympathetic branch, and vice versa. This has been problematic, however, as blocking one branch may indirectly alter the other (e.g., by reflex adjustments) . Moreover, although drugs may be highly specific to a receptor type and can thus differentiate sympathetic and parasympathetic effector synapses, they are not specific as to the target organ and may exert actions at some remote site, including the brain. Such remote actions could alter the psychological states of interest or otherwise bias reactivity. The complications with pharmacological blockades have been sufficiently serious as to question their validity and limit their application. A new measurement methodology was clearly needed.

A more extensive pharmacological protocol and a more comprehensive analytical approach provided that methodology (Berntson, Cacioppo, & Quigley, 1994). Consider the observed heart period response (0) to some evocative stimulus occurring at the vertical line in Figure 12.3. As depicted, blockade of the parasympathetic branch would reveal the isolated sympathetic response 0Pblk, which provides an estimate of the sympathetic contribution (termed the residual estimate or s'). At the same time, the response decrement from the unblocked condition (0 - 0Pblk) offers an estimate of the normal contribution of the parasympathetic branch (termed the subtractive estimate, or p'). Conversely, blockade of the sympathetic branch (0Sblk) provides a residual index of the isolated parasympathetic response (p') and the response decrement from the unblocked

Figure 12.3. Illustration of heart period response in pharmacological blockade analyses. Solid line illustrates the observed response in the absence of blockade (under saline control conditions). Dashed lines illustrate the response under selective sympathetic and parasympathetic blockades. Arrows illustrate the residual (s' and p') and subtractive (s" and p") estimates of sympathetic and parasympathetic control. From "Autonomic Cardiac Control. I. Estimation and Validation from Pharmacological Blockades," by G. G. Bertson, J. T. Cacioppo, and K. S. Quigley, 1994, Psychophysiology, 31, 572-585. Copyright 1994 by Blackwell Publishing, Ltd. Reprinted with permission.

Figure 12.3. Illustration of heart period response in pharmacological blockade analyses. Solid line illustrates the observed response in the absence of blockade (under saline control conditions). Dashed lines illustrate the response under selective sympathetic and parasympathetic blockades. Arrows illustrate the residual (s' and p') and subtractive (s" and p") estimates of sympathetic and parasympathetic control. From "Autonomic Cardiac Control. I. Estimation and Validation from Pharmacological Blockades," by G. G. Bertson, J. T. Cacioppo, and K. S. Quigley, 1994, Psychophysiology, 31, 572-585. Copyright 1994 by Blackwell Publishing, Ltd. Reprinted with permission.

condition (0 - 0Sblk) offers an estimate of the normal contribution of the sympathetic branch (s'O-

The preceding analyses provide two estimates of the functional contributions of each autonomic branch, and an overall estimate can be derived as the means:

Estimate of sympathetic response (at time t) =

ASt = (Ast' + As")/ 2 Estimate of parasympathetic response (at time t) =

More important, because the residual and sub-tractive estimates are derived from distinct pharmacological blockers (muscarinic cholinergic antagonists for the parasympathetic branch and adrenergic antagonists for the sympathetic branch), their side effects and remote actions would be different. If the estimates agree, despite these differences, one would have increased confidence in the estimates of autonomic control. Moreover, any discrepancy in the independent estimates could be indexed by an error term (eblk), which is the difference between the two estimates at a given point in time. This value can be formally shown to be equivalent for the two branches. Thus

As the discrepancy between the two estimates becomes larger, eblkt increases, and one would have lower confidence in the estimate. This is formalized in a validity coefficient:

v5 = (leffect sizel/ leffect sizel + eblk)

The validity coefficient can range from 0 when the error is very large relative to the estimated response, to 1.0 when the error term is negligible. An example of this analysis is shown in Figure 12.4 for orienting responses of rats to auditory stimuli. The top panel illustrates the observed responses under the control condition and after sympathetic (atenolol) and parasympathetic (scopolamine) blockade. The lower panels illustrate the overall as well as the residual and subtractive estimates of the contributions of the branches to the observed

Response to Lo Intensity Tone (OR)

Response to Hi Intensity Tone (DR)

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