Respiratory sinus arrhythmia: a transdiagnostic biomarker of emotion dysregulation and psychopathology

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Highlights

  • RSA is a valid and reliable biomarker of emotion regulation capacity in humans.

  • Low tonic RSA and excessive RSA reactivity to emotion evocation mark PFC dysfunction.

  • Effective cortical regulation of subcortical neural circuits marks psychological health.

In the past two decades, respiratory sinus arrhythmia (RSA)  an index of parasympathetic nervous system (PNS)-mediated cardiac control  has emerged as a reliable peripheral biomarker of emotion regulation (ER). Reduced RSA and excessive RSA reactivity (i.e., withdrawal) to emotional challenge are observed consistently among individuals with poor ER capabilities, including those with various forms of internalizing and externalizing psychopathology, and those with specific psychopathological syndromes, including anxiety, phobias, attention problems, autism, callousness, conduct disorder, depression, non-suicidal self-injury, panic disorder, and trait hostility. Emerging evidence suggests that low RSA and excessive RSA reactivity index poor ER because they are downstream peripheral markers of prefrontal cortex (PFC) dysfunction. Poorly modulated inhibitory efferent pathways from the medial PFC to the PNS result in reduced RSA and excessive RSA reactivity. According to this perspective, RSA is a non-invasive proxy for poor executive control over behavior, which characterizes most forms of psychopathology.

Introduction

Although the study of human emotion can be traced at least as far back as Darwin [1], for much of the 20th century psychological science was dominated by behavioral and cognitive paradigms that viewed emotional states as subjective, unquantifiable, and unamenable to scientific inquiry [2]. Beginning in the mid-1990s, these paradigms gave way to the contemporary view that emotional experience and expression are integral to both positive and negative psychological adjustment. This paradigm shift was facilitated by several developments, including a 1990, yearlong seminar on emotion held at the National Institute of Mental Health, and a 1991 conference on the development of emotion regulation (ER) that was sponsored by the John D. and Catherine T. MacArthur Foundation Early Childhood Network. From these, landmark volumes on the nature of emotion [3] and ER [4] emerged. Among other important contributions, chapters in these volumes demonstrated how emotional states can be inferred, verified, and quantified by measuring appropriate biological systems [5, 6, 7]. The study of emotion soon became mainstream, and is currently central to the positive and negative valence systems of the Research Domain Criteria (RDoC) [8].

Section snippets

Emotion dysregulation and psychopathology

It is now widely recognized that problems with ER confer vulnerability to a wide range of psychopathological outcomes [9], and that difficulties with ER characterize almost all forms of psychopathology [10•, 11•]. ER can be defined as the set of processes through which emotional experience and expression are shaped in the service of adaptive behavior [12]. Such shaping of emotion may occur through various mechanisms, including attentional, cognitive, social, and behavioral [13]. In contrast,

Central nervous system substrates of emotion dysregulation

Recognition that emotion dysregulation plays such a prominent role in vulnerability to psychopathology has led to considerable research on its central nervous system (CNS) substrates. Taken together, this research demonstrates that ER is subserved by top–down, cortical (prefrontal) brain networks that mature into the early 20s [17•, 18•, 19•]. Trait anxiety, which confers vulnerability to internalizing disorders (e.g., anxiety, depression), is volitionally regulated through prefrontal

Peripheral nervous system markers of emotion dysregulation

Although the CNS substrates of ER are well characterized [16], measuring CNS processes requires neuroimaging protocols that are expensive, limited in ecological validity, and difficult to use with certain populations, such as young children and those with severe psychopathology. For these reasons and others, many researchers have turned to peripheral nervous system markers of ER, most notably respiratory sinus arrhythmia (RSA). The term RSA refers to ebbing and flowing of heart rate (HR)

Conclusions

A primary aim of psychophysiological research is to use peripheral measures to make inferences about CNS processes that are difficult and in some cases impossible to index noninvasively [26]. However, much of the literature on RSA-behavior relations is either agnostic with respect to central nervous system substrates of RSA, or implies that the PNS plays a causal role in ER. As reviewed above, it is far more likely that the PNS  via the vagus nerve  mediates links between the PFC and

References and recommended reading

Papers of particular interest, published within the period of review, have been highlighted as:

  • • of special interest

  • •• of outstanding interest

References (48)

  • G. Dawson

    Frontal electroencephalographic correlates of individual differences in emotion expression in infants: a brain systems perspective on emotion

    Monogr Soc Res Child

    (1994)
  • J. Panksepp

    The clearest physiological distinctions between emotions will be found in the brain

  • National Institute of Mental Health. Research Domain Criteria Matrix. From...
  • P.M. Cole et al.

    Emotion dysregulation as a risk factor for psychopathology

  • T.P. Beauchaine

    Vagal tone, development, and Gray's motivational theory: toward an integrated model of autonomic nervous system functioning in psychopathology

    Dev Psychopathol

    (2001)
  • Beauchaine TP, Thayer JF: Heart rate variability: a transdiagnostic biomarker of psychopathology, Int J Psychophysiol,...
  • R.A. Thompson

    Emotion and self-regulation

  • A. Aldao et al.

    Emotion regulation strategies and psychopathology: a meta-analysis

    Clin Psychol Rev

    (2010)
  • T.P. Beauchaine et al.

    Instantiating the multiple levels of analysis perspective in a program of study on externalizing behavior

    Dev Psychopathol

    (2012)
  • T.P. Beauchaine et al.

    Polyvagal theory and developmental psychopathology: emotion dysregulation and conduct problems from preschool to adolescence

    Biol Psychol

    (2007)
  • Beauchaine TP: Future directions in emotion dysregulation and youth psychopathology, J Clin Child Adol Psychol, in...
  • N. Gogtay et al.

    Dynamic mapping of human cortical development during childhood through early adulthood

    Proc Natl Acad Sci USA

    (2004)
  • Snyder JJ: Coercive family processes in the development of externalizing behavior: Incorporating neurobiology into...
  • T.F. Heatherton et al.

    Cognitive neuroscience of self-regulation failure

    Trends Cogn Sci

    (2011)
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