Publication guidelines for human heart rate and heart rate variability studies in psychophysiology-Part 1: Physiological underpinnings and foundations of measurement.

This Committee Report provides methodological, interpretive, and reporting guidance for researchers who use measures of heart rate (HR) and heart rate variability (HRV) in psychophysiological research. We provide brief summaries of best practices in measuring HR and HRV via electrocardiographic and photoplethysmographic signals in laboratory, field (ambulatory), and brain-imaging contexts to address research questions incorporating measures of HR and HRV. The Report emphasizes evidence for the strengths and weaknesses of different recording and derivation methods for measures of HR and HRV. Along with this guidance, the Report reviews what is known about the origin of the heartbeat and its neural control, including factors that produce and influence HRV metrics. The Report concludes with checklists to guide authors in study design and analysis considerations, as well as guidance on the reporting of key methodological details and characteristics of the samples under study. It is expected that rigorous and transparent recording and reporting of HR and HRV measures will strengthen inferences across the many applications of these metrics in psychophysiology. The prior Committee Reports on HR and HRV are several decades old. Since their appearance, technologies for human cardiac and vascular monitoring in laboratory and daily life (i.e., ambulatory) contexts have greatly expanded. This Committee Report was prepared for the Society for Psychophysiological Research to provide updated methodological and interpretive guidance, as well as to summarize best practices for reporting HR and HRV studies in humans.

Social interaction modulates autonomic, inflammatory, and depressive-like responses to cardiac arrest and cardiopulmonary resuscitation.

Psychological factors, including depression and social isolation, are important determinants of cardiovascular health. The current study uses a well-validated mouse model of cardiac arrest/cardiopulmonary resuscitation (CA/CPR) to examine the effect of social environment on several pathophysiological and behavioral responses to cerebral ischemia. Male experimental mice were either housed in pairs with an ovariectomized female or socially isolated for the duration of the experiment. Cardiac arrest increased the mRNA expression of the proinflammatory cytokines TNF-α, IL-1ß, and IL-6, as well as the microglia marker MAC-1; expression of each of these factors, except IL-6, was further increased among socially isolated mice. Furthermore, socially isolated animals exposed to the CA/CPR procedure displayed significantly higher levels of neuronal cell death and microglia staining within the hippocampus at 7 d following surgery. Social isolation also exacerbated CA/CPR-induced depressive-like behavior and cardiac autonomic dysregulation. In the absence of ischemic damage, social environment had no significant effect on the expression of neuronal cell death, autonomic cardiac control, or behavior. Together, these data suggest that social factors influence the pathophysiological trajectory following cardiac arrest.

Variation in the oxytocin receptor gene influences neurocardiac reactivity to social stress and HPA function: a population based study.

Oxytocin (OT) is a nonapeptide neurohormone that is involved in a broad array of physiological and behavioral processes related to health including hypothalamic-pituitary-adrenal (HPA) axis functioning, autonomic nervous system (ANS) activity and social behaviors. The present study sought to explore the influence of genetic variation in the oxytocin receptor (SNP; rs53576) on autonomic and neurohormonal functioning across both resting and psychological stress conditions in a population based sample of older adults. Results revealed that A carrier males showed higher levels of resting sympathetic cardiac control as compared to their G/G counter parts. However, G/G participants displayed significantly higher levels of sympathetic reactivity to psychological stress with G/G males showing the highest levels of sympathetic response to stress. Although no significant effects were detected for heart rate or parasympathetic cardiac control across resting and stress conditions, results revealed that G/G participants generally displayed heightened stroke volume and cardiac output reactivity to the psychological stressor. Furthermore, analysis of diurnal fluctuations in salivary cortisol revealed that G/G participants displayed lower awakening cortisol levels and less variation in salivary cortisol across the day as compared to A carrier individuals.

Photoperiod alters autonomic regulation of the heart.

Outside of the tropics, environmental conditions fluctuate in a generally predictable manner across the year. Many small mammals have evolved mechanisms, such as seasonal breeding and annual adjustments in physiology, morphology, and behavior, that promote winter survival when food is scarce and thermoregulation is challenging. Photoperiod (day length) is a cue used by many seasonal breeders to predict seasonal changes in environmental conditions. One system that is uniquely situated to mediate photoperiod-induced alterations in physiology is the autonomic nervous system (ANS). The 2 branches of the ANS are key regulators of immune responses, thermoregulation, and energy balance, functions that undergo marked shifts in baseline and reactivity following acclimation to short day lengths. Although previous studies have investigated the effects of photoperiod on ANS endpoints, this study examined the direct effects of photoperiod on integrated ANS function. To test the hypothesis that short day lengths increase parasympathetic and sympathetic tones, we maintained adult male Siberian hamsters (Phodopus sungorus) to either long or short photoperiods and then analyzed electrocardiogram recordings. Short day lengths increased both parasympathetic tone, as measured by respiratory sinus arrhythmia, and sympathetic control of the heart, measured with autonomic blockade. Additionally, short day lengths enhanced the withdrawal of parasympathetic control and the increase of sympathetic tone in response to acute restraint stress. Finally, these effects were discovered to be independent of circulating androgens. These data indicate that the ANS of Siberian hamsters undergoes profound changes following prolonged exposure to short winter-like day lengths.

The insula and evaluative processes.

The insula has been implicated as a component of central networks subserving evaluative and affective processes. This study examined evaluative valence and arousal ratings in response to picture stimuli in patients with lesions of the insula and two contrast groups: a control-lesion group (the primary contrast group) and an amygdala-lesion group. Patients rated the positivity and negativity of picture stimuli (from very unpleasant to very pleasant) and how emotionally arousing they found the pictures to be. Compared with patients in the control-lesion group, patients with insular lesions reported reduced arousal in response to both unpleasant and pleasant stimuli, as well as marked attenuation of valence ratings. In contrast, the arousal ratings of patients with amygdala lesions were selectively attenuated for unpleasant stimuli, and these patients' positive and negative valence ratings did not differ from those of the control-lesion group. Results support the view that the insular cortex may play a broad role in integrating affective and cognitive processes, whereas the amygdala may have a more selective role in affective arousal, especially for negative stimuli.

Multilevel analysis: Integrating multiple levels of neurobehavioral systems.

Traditional disciplines have frequently dealt with complex phenomena from a given level of analysis, be that molecular, cellular, organ system, or organismic level. This can yield highly valuable information on biological and psychological processes. There is an explanatory value added, however, by an integrative multilevel approach, in which different levels of analysis and different levels of the neural organization are considered in the models and theories of psychological functions. This is the essence of the emerging discipline of social neuroscience, promoted by John Cacioppo and Gary Berntson, which seeks to inform the interactions between social psychological and biological processes.

Neural Circuits of Interoception.

The present paper considers recent progress in our understanding of the afferent/ascending neural pathways and neural circuits of interoception. Of particular note is the extensive role of rostral neural systems, including cortical systems, in the recognition of internal body states, and the reciprocal role of efferent/descending systems in the regulation of those states. Together these reciprocal interacting networks entail interoceptive circuits that play an important role in a broad range of functions beyond the homeostatic maintenance of physiological steady-states. These include the regulation of behavioral, cognitive, and affective processes across conscious and nonconscious levels of processing. We highlight recent advances and knowledge gaps that are important for accelerating progress in the study of interoception.

SOCIAL NEUROSCIENCE AND ITS RELATIONSHIP TO SOCIAL PSYCHOLOGY.

Social species create emergent organizations beyond the individual. These emergent structures evolved hand in hand with neural, hormonal, cellular, and genetic mechanisms to support them because the consequent social behaviors helped these organisms survive, reproduce, and care for offspring sufficiently long that they too reproduced. Social neuroscience seeks to specify the neural, hormonal, cellular, and genetic mechanisms underlying social behavior, and in so doing to understand the associations and influences between social and biological levels of organization. Success in the field, therefore, is not measured in terms of the contributions to social psychology per se, but rather in terms of the specification of the biological mechanisms underlying social interactions and behavior-one of the major problems for the neurosciences to address in the 21st century.

Presidential Address 2011: Autonomic modes of control and health.

Understanding psychosomatic relations, and their implications for heath, is importantly dependent on our conceptual and measurement models. The historical view of reciprocal control of the autonomic branches is applicable in some contexts, but not others. Control of the autonomic branches can vary reciprocally, independently, and even coactively. Assessment of sympathovagal balance, based on a reciprocal model of regulation of the autonomic branches, may have applications in orthostatic contexts and in insulin resistance in diabetes. However, it does not adequately capture the pattern of autonomic control that is relevant for myocardial infarction (MI; in humans) and experimental cardiac arrest (in mice). A measure of sympathovagal balance (cardiac autonomic balance) was predictive and informative of the autonomic contributions to diabetes but was blind to autonomic contributions to cardiac arrest and its sequelae. However, a metric designed to capture the coactivity dimension of cardiac autonomic regulation (CAR) was predictive of MI and its sequelae. Both human and animal model studies revealed that low CAR (low sympathetic and especially low parasympathetic control) predicted the occurrence of MI and the neuroinflammatory consequences of cardiac arrest. These effects were importantly modulated by social support in both humans and animals, via an apparent oxytocinergic pathway that impacts parasympathetic cardiac control and CAR, and thus neuroinflammation. Results indicate the importance of a physiologically meaningful model of autonomic control in understanding health implications of the modes of autonomic control.

Should heart rate variability be "corrected" for heart rate? Biological, quantitative, and interpretive considerations.

Metrics of heart period variability are widely used in the behavioral and biomedical sciences, although somewhat confusingly labeled as heart rate variability (HRV). Despite their wide use, HRV metrics are usually analyzed and interpreted without reference to prevailing levels of cardiac chronotropic state (i.e., mean heart rate or mean heart period). This isolated treatment of HRV metrics is nontrivial. All HRV metrics routinely used in the literature exhibit a known and positive relationship with the mean duration of the interval between two beats (heart period): as the heart period increases, so does its variability. This raises the question of whether HRV metrics should be "corrected" for the mean heart period (or its inverse, the heart rate). Here, we outline biological, quantitative, and interpretive issues engendered by this question. We provide arguments that HRV is neither uniformly nor simply a surrogate for heart period. We also identify knowledge gaps that remain to be satisfactorily addressed with respect to assumptions underlying existing HRV correction approaches. In doing so, we aim to stimulate further progress toward the rigorous use and disciplined interpretation of HRV. We close with provisional guidance on HRV reporting that acknowledges the complex interplay between the mean and variability of the heart period.

Nucleus basalis magnocellularis and substantia innominata corticopetal cholinergic lesions attenuate freezing induced by predator odor.

Previous studies have demonstrated that corticopetal cholinergic lesions applied to the nucleus basalis magnocellularis and substantia innominata (NBM/SI) attenuate operant suppression induced by aversive events. However, these lesions have no effect on open-arm behavior in the elevated plus-maze or changes in startle reactivity induced by bright light. This raises the possibility that NBM/SI corticopetal cholinergic lesions alter operant behavior and/or appetitive state, as opposed to the aversive state operant suppression is supposed to index. To address this concern, the authors documented the effect of NBM/SI corticopetal cholinergic lesions on freezing induced by a component of fox feces (2,4,5-trimethylthiazoline [TMT]), a paradigm that does not involve food deprivation or operant performance. TMT presentation induced freezing behavior, and this effect was attenuated by NBM/SI corticopetal cholinergic lesions. Because predator odor presentation, but not presentation of a predator, induces defense behaviors that are sensitive to anxiolytic drugs, the results of the study suggest that NBM/SI corticopetal cholinergic lesions attenuate anxiety-like states.

Cortical modulation by nucleus basalis magnocellularis corticopetal cholinergic neurons during anxiety-like states is reflected by decreases in delta.

Previous research has demonstrated that nucleus basalis magnocellularis (nbm) corticopetal cholinergic neurons modulate anxiety-like states, but cortical modulation by these neurons during anxiety-like states has not been characterized. In order to address this, we documented the effect of nbm corticopetal cholinergic lesions on cortical activity in direct (prefrontal cortex) and indirect (retrosplenial cortex) targets of nbm corticopetal cholinergic neurons during footshock induced operant suppression. The gamma/delta ratio and theta were used as indices of cortical activity, because these components of the electroencephalogram (EEG) are sensitive to basal forebrain corticopetal cholinergic modulation. During operant suppression, increases in the gamma/delta ratio and augmented theta were observed in both cortical EEGs. Lesions attenuated operant suppression and the gamma/delta ratio, but had no effect on increased theta. The effect of nbm corticopetal cholinergic lesions on the gamma/delta ratio was driven by the effect of the lesions on the delta band. The results of the study demonstrate that during anxiety-like states 1) decreases in delta reflect the action of nbm corticopetal cholinergic neurons, 2) nbm corticopetal cholinergic neurons alter neural processes in direct and indirect cortical targets, and 3) cortical theta is not dependent on the integrity of nbm corticopetal cholinergic neurons.

Spirituality and autonomic cardiac control.

BACKGROUND: Spirituality has been suggested to be associated with positive health, but potential biological mediators have not been well characterized. PURPOSE AND METHODS: The present study examined, in a population-based sample of middle-aged and older adults, the potential relationship between spirituality and patterns of cardiac autonomic control, which may have health significance. Measures of parasympathetic (high-frequency heart rate variability) and sympathetic (pre-ejection period) cardiac control were obtained from a representative sample of 229 participants. Participants completed questionnaires to assess spirituality (closeness to and satisfactory relationship with God). Personality, demographic, anthropometric, health behavior, and health status information was also obtained. A series of hierarchical regression models was used to examine the relations between spirituality, the autonomic measures, and two derived indexes--cardiac autonomic balance (CAB, reflecting parasympathetic to sympathetic balance) and cardiac autonomic regulation (CAR, reflecting total autonomic control). RESULTS: Spirituality, net of demographics, or other variables were found to be associated with enhanced parasympathetic as well as sympathetic cardiac control (yielding a higher CAR) but was not associated with CAB. Although the number of cases was small (N = 11), both spirituality and CAR were significant negative predictors of the prior occurrence of a myocardial infarction. CONCLUSIONS: In a population-based sample, spirituality appears to be associated with a specific pattern of CAR, characterized by a high level of cardiac autonomic control, irrespective of the relative contribution of the two autonomic branches. This pattern of autonomic control may have health significance.

Whither vagal tone.

Measures of respiratory sinus arrhythmia (RSA) have been widely applied in the physiological and psychophysiological literature as an index of vagal control of the heart. Despite an extensive literature, however, differences in interpretation remain within the field. A guiding conception for several contributions in this issue is the notion of separate brainstem centers involved in parasympathetic control, with distinct evolutionary origins and significance and with divergent influences on cardiac vagal tone as it relates to psychological and behavioral processes. We here consider the biological foundations for this view, discuss some methodological and interpretative caveats for RSA applications and offer suggestions for further development of the field.

Impedance cardiography in healthy children and children with congenital heart disease: Improving stroke volume assessment.

INTRODUCTION: Stroke volume (SV) and cardiac output are important measures in the clinical evaluation of cardiac patients and are also frequently used in research applications. This study was aimed to improve SV scoring derived from spot-electrode based impedance cardiography (ICG) in a pediatric population of healthy volunteers and patients with a corrected congenital heart defect. METHODS: 128 healthy volunteers and 66 patients participated. First, scoring methods for ambiguous ICG signals were optimized to improve agreement of B- and X-points with aortic valve opening/closure in simultaneously recorded transthoracic echocardiography (TTE). Building on the improved scoring of B- and X-points, the Kubicek equation for SV estimation was optimized by testing the agreement with the simultaneously recorded SV by TTE. Both steps were initially done in a subset of the sample of healthy children and then validated in the remaining subset of healthy children and in a sample of patients. RESULTS: SV assessment by ICG in healthy children strongly improved (intra class correlation increased from 0.26 to 0.72) after replacing baseline thorax impedance (Z0) in the Kubicek equation by an equation (7.337-6.208∗dZ/dtmax), where dZ/dtmax is the amplitude of the ICG signal at the C-point. Reliable SV assessment remained more difficult in patients compared to healthy controls. CONCLUSIONS: After proper adjustment of the Kubicek equation, SV assessed by the use of spot-electrode based ICG is comparable to that obtained from TTE. This approach is highly feasible in a pediatric population and can be used in an ambulatory setting.

Effect of nucleus basalis magnocellularis cholinergic lesions on fear-like and anxiety-like behavior.

Previous research has suggested that cholinergic neurons in the nucleus basalis magnocellularis and substantia innominata (NBM/SI) may be important in mediating aversive states. The authors investigated the effect of NBM/SI cholinergic lesions, induced with 192 IgG saporin, on behavioral measures of aversive states in rats. Behavior in the elevated plus maze and behavioral suppression induced by 2 fear-conditioned stimuli, a tone and a light, were evaluated. Lesions had no effect on any measures in the elevated plus maze but attenuated operant suppression induced by the light and attenuated freezing induced by the tone, though this last effect was not statistically significant. The results of the study suggest that NBM/SI cholinergic neurons may be important in mediating selective aspects of aversive states.

Up- and down-regulating facial disgust: affective, vagal, sympathetic, and respiratory consequences.

Relative to watching in a natural manner, people asked to suppress or exaggerate their facial response to a negative emotional stimulus experience greater activation of the sympathetic nervous system but report a similar subjective emotional experience. The present research extends prior research on response modulation in two important ways. First, discrete indicators of cardiac vagal and sympathetic control (respiratory sinus arrhythmia (RSA) and pre-ejection period (PEP), respectively) were included as dependent measures along with interbeat interval (IBI) and skin conductance (EDR). Second, to help generalize results across response-focused modulation techniques, participants suppressed, exaggerated, or exerted no control over their responses while watching a disgust-eliciting film (for control purposes, a fourth group was asked to watch a neutral film naturally). Response modulation was associated with significantly decreased PEP (increased cardiac sympathetic control) relative to those in the natural-watch conditions. All participants evidenced increased EDR while watching the disgusting clip, but facial modulation did not produce EDR reactivity beyond that of watching the disgusting film naturally. Exaggerators experienced decreased IBI during modulation (perhaps due to increased muscle contraction) whereas all other groups showed increased IBI (i.e., the orienting response). Neither emotional experience nor facial modulation reliably impacted RSA, respiration rate, or inspiratory depth.

Differential mobilization of functionally distinct natural killer subsets during acute psychologic stress.

OBJECTIVE AND METHODS: Two functionally distinct natural killer (NK) subsets can be identified according to surface CD56 expression: CD56lo cells compose the majority of NK cells and function as cytotoxic cells, whereas CD56hi cells have an immunomodulatory function through the secretion of cytokines. These NK subsets also differ in the expression levels of adhesion molecules such as CD62L and CD11a, indicating distinct potentials to migrate to lymphoid and nonlymphoid tissues. We investigated whether NK cell mobilization during acute stress varies according to these functional and phenotypic distinctions. METHODS AND RESULTS: Fifty-three undergraduate students performed a public-speaking task and 21 students participated in a control session. The task increased heart rate and catecholamines. No change was observed for the immunoregulatory CD56hi NK subset, whereas the number of cytotoxic CD56lo NK cells tripled. In line with the observation that NK mobilization is related to cytotoxic function, we found larger increases in NK cells that express higher levels of CD16 (a receptor that mediates antibody-dependent cytotoxicity). Consistent with known subset differences in adhesion molecule expression, we also found larger stress-induced increases for NK cells that were CD62L-negative and CD11ahi. Plasma levels of soluble CD62L remained unaltered, suggesting that the increase in CD62L-negative NK cells did not result from CD62L shedding. Regression analyses demonstrated independent contributions of epinephrine and norepinephrine to NK subset mobilization. CONCLUSION: The marked specificity and robustness of these effects support the idea that NK cell mobilization is a functionally relevant response that is aimed at protecting the organism during acutely stressful situations.

Visceral afferent bias on cortical processing: role of adrenergic afferents to the basal forebrain cholinergic system.

Intraperitoneal epinephrine enhances the cerebral auditory evoked potential (AEP), an effect that is dependent on the basal forebrain cortical cholinergic system. The present study examined the hypothesis that ascending noradrenergic projections from brainstem autonomic substrates to the basal forebrain cholinergic system represent an essential component of the ascending pathway mediating this effect of epinephrine. Epinephrine again enhanced the AEP in rats, and this effect was attenuated by infusion of the selective alpha1 adrenergic antagonist terazosin into the basal forebrain. Moreover, infusions of the selective alpha1 adrenergic agonist phenylephrine into the basal forebrain mimicked the priming effects of epinephrine. Results support the hypothesis that noradrenergic afferents to the basal forebrain cholinergic system represent a component of an ascending visceral afferent system.

Stress-related immune changes in middle-aged and older women: 1-year consistency of individual differences.

This study reviews prior research and reports longer-term consistency of stress-related immune variables in middle-aged and older women who performed mental math and speech tasks 2 times 1 year apart. Leukocyte subsets, mitogen-induced lymphocyte proliferation, and natural killer cell activity were measured at baseline, after tasks, and after 30-min recovery. Epstein-Barr virus (EBV) antibody titers were assessed at baseline. Pearson coefficients and standardized maximum-likelihood estimates of year-to-year covariances for leukocyte subsets and EBV titers showed moderately high to high baseline and posttask consistency and lower recovery consistency; consistency for other functional immune assays and reactivity scores for all variables was moderate to low. Results support longitudinal study of psychosocial context effects on tonic immune function and posttask scores.