Vagal tone

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Vagal tone is activity of the vagus nerve, the 10th cranial nerve and a fundamental component of the parasympathetic branch of the autonomic nervous system. This branch of the nervous system is not under conscious control and is largely responsible for the regulation of several body compartments at rest. Vagal activity results in various effects, including: heart rate reduction, vasodilation/constriction of vessels, glandular activity in the heart, lungs, and digestive tract, liver, immune system regulation as well as control of gastrointestinal sensitivity, motility and inflammation. [1]

Contents

In this context, tone specifically refers to the continual nature of baseline parasympathetic action that the vagus nerve exerts. While baseline vagal input is constant, the degree of stimulation it exerts is regulated by a balance of inputs from sympathetic and parasympathetic divisions of the autonomic nervous system, with parasympathetic activity generally being dominant. Vagal tone is frequently used to assess heart function, and is also useful in assessing emotional regulation and other processes that alter, or are altered by, changes in parasympathetic activity. [2] [3]

Measurements of vagal tone can be performed by means of either invasive or noninvasive procedures. Invasive procedures are in the minority and include vagus nerve stimulation by specific manual, breathing or electrical techniques. Noninvasive techniques mainly rely on the investigation of heart rate and heart rate variability. [4] [5] [6]

Noninvasive vagal tone quantification

In most cases, vagal tone is not measured directly. Instead the processes affected by the vagus nerve – specifically heart rate and heart rate variability – are measured and used as a surrogate for vagal tone. Increased vagal tone (and thus vagal action) is generally associated with a lower heart rate and increased heart rate variability. However, during graded orthostatic tilt, vagal tone withdrawal is an indirect indicator of cardiovascular fitness. [7]

Vagal innervation of the heart

Heart rate is largely controlled by the heart's internal pacemaker activity. In a healthy heart, the main pacemaker is a collection of cells on the border of the atria and vena cava called the sinoatrial node. Heart cells exhibit automaticity, the ability to generate electrical activity independent of external stimulation. The electrical activity spontaneously generated by the sinoatrial node sets the pace for the rest of the heart. [1]

In absence of external stimuli, sinoatrial pacing generally, while awake, maintains the heart rate in the range of 60–100 beats per minute (bpm). [8] The two branches of the autonomic nervous system work together to increase or slow the heart rate. The vagus nerve acts on the sinoatrial node, slowing its conduction and modulating vagal tone, via the neurotransmitter acetylcholine and downstream changes to ionic currents and calcium of heart cells. [4] Because of its effect on heart rate, and cardio health, vagal tone can be measured and understood by examining its correlation to heart rate modulation and heart rate variability. [5]

Respiratory sinus arrhythmia

Respiratory sinus arrhythmia (RSA) is typically a benign, normal variation in heart rate that occurs during each breathing cycle: the heart rate increases when breathing in and decreases when breathing out. [1] RSA was first recognized by Carl Ludwig in 1847 [9] but is still imperfectly understood. [10] It has been observed in humans from the early stages of life through adulthood, [11] [1] and is found in several different species. [12] [13] [14]

During inhalation, the intra-thoracic pressure lowers due to the contraction and downward movement of the diaphragm and the expansion of the chest cavity. Atrial pressure is also lowered as a result, causing increased blood flow to the heart, which in turn decreases baroreceptors firing response which diminishes vagal tone. This causes an increase in heart rate. [1]

During exhalation, the diaphragm relaxes, moving upward, and decreases the size of the chest cavity, causing an increase in intrathoracic pressure. This increase in pressure inhibits venous return to the heart resulting in both reduced atrial expansion and increased activation of baroreceptors. This relieves the suppression of vagal tone and leads to a decreased heart rate. [1]

Heart rate (HR) (first row), tidal volume (Vt) (second row), Vt and superimposed HR (third row). It is clearly visible the HR modulation: HR increases with inspiration and decreases with expiration. VivoSenseHR vs Vt.jpg
Heart rate (HR) (first row), tidal volume (Vt) (second row), Vt and superimposed HR (third row). It is clearly visible the HR modulation: HR increases with inspiration and decreases with expiration.
Heart rate (HR) (first row), ECG signal (ECG) (second row), and respiration (third row) for a newborn subject in a 15-seconds recording. HR expresses oscillations synchronous with respect to respiration. RSA neonatal ECG+RESP+HR.png
Heart rate (HR) (first row), ECG signal (ECG) (second row), and respiration (third row) for a newborn subject in a 15-seconds recording. HR expresses oscillations synchronous with respect to respiration.
RSA magnitude estimation based on a multivariate approach based on joint analysis of ECG and respiration. The green line shows the heart rate variations averaged over several breathing cycles. It is clearly visible heart rate increase-decrease trend which is typical of RSA. RSA Bartsch method.png
RSA magnitude estimation based on a multivariate approach based on joint analysis of ECG and respiration. The green line shows the heart rate variations averaged over several breathing cycles. It is clearly visible heart rate increase-decrease trend which is typical of RSA.

RSA as a vagal tone estimator

Respiratory sinus arrhythmia is frequently used as a noninvasive method for investigating vagal tone, in physiological, behavioral, and several clinical studies. [16] [17] [18] This can be done using electrocardiography (ECG) recording, [19] although other methods are also being developed that take advantage of the interactions between ECG and respiration. [20] [15] Interpretation of RSA measurements must be done with care, however, as several factors including differences between individuals can change the relationship between RSA and vagal tone. [21]

Evolution and physiology

It has been suggested that RSA may have evolved to save energy for both cardiac and respiratory systems by reducing the heart rate [22] and by suppressing ineffective ventilation during the ebb of perfusion (delivery of blood from arteries to capillaries for oxygenation and nutrition). [23] [24]

RSA has been found to increase in subjects in resting state and to decrease in states of stress or tension. It is increased in supine position and decreased in prone position, and is on average higher and more pronounced during the day as compared to the night. [22] RSA has also been extensively used to quantify vagal tone withdrawal in graded orthostatic tilt. [7] [25]

Typically, expression of RSA decreases with age. [26] However, adults in excellent cardiovascular health, such as endurance runners, swimmers, and cyclists, are likely to have a more pronounced RSA. Professional athletes on average maintain very high vagal tone and consequently higher RSA levels. RSA is less prominent in individuals with diabetes and cardiovascular disease. [27]

Insights into psychology and disease

Vagal tone research has the potential to offer insight into social behavior, social interactions, and human psychology. Much of this work has been focused on newborns and children. [26] Baseline vagal tone can be used either as a potential predictor of behavior or as a signal of mental health (particularly emotion regulation, anxiety, and internalizing and externalizing disorders). [28] [29]

The polyvagal theory by Porges is an influential model of how the vagal pathways respond to novelty and to stressful external stimuli. [30] [31] [32] The theory proposes that there are two vagal systems, one that is shared with reptiles and amphibia and a second, more recent, system that is unique to mammals. The two pathways behave differently and can work against each other. This theory can account for several psychophysiological phenomena and psychosomatic illnesses. [30] [26] However, recent studies indicate that the vagal "system" described by Porges as being unique to mammals existed long before the evolution of mammals. [33] [34]

Other estimates of vagal tone

There are several methods of estimating vagal tone other than measuring RSA, including:

See also

Related Research Articles

<span class="mw-page-title-main">Vagus nerve</span> Cranial nerve X, for visceral innervation

The vagus nerve, also known as the tenth cranial nerve, cranial nerve X, or simply CN X, is a cranial nerve that carries sensory fibers that create a pathway that interfaces with the parasympathetic control of the heart, lungs, and digestive tract. It comprises two nerves—the left and right vagus nerves—but they are typically referred to collectively as a single subsystem. The vagus is the longest nerve of the autonomic nervous system in the human body and comprises both sensory and motor fibers. The sensory fibers originate from neurons of the nodose ganglion, whereas the motor fibers come from neurons of the dorsal motor nucleus of the vagus and the nucleus ambiguus. The vagus was also historically called the pneumogastric nerve.

<span class="mw-page-title-main">Parasympathetic nervous system</span> Division of the autonomic nervous system

The parasympathetic nervous system (PSNS) is one of the three divisions of the autonomic nervous system, the others being the sympathetic nervous system and the enteric nervous system. The enteric nervous system is sometimes considered part of the autonomic nervous system, and sometimes considered an independent system.

Heart rate is the frequency of the heartbeat measured by the number of contractions of the heart per minute. The heart rate can vary according to the body's physical needs, including the need to absorb oxygen and excrete carbon dioxide, but is also modulated by numerous factors, including genetics, physical fitness, stress or psychological status, diet, drugs, hormonal status, environment, and disease/illness as well as the interaction between and among these factors. It is usually equal or close to the pulse measured at any peripheral point.

<span class="mw-page-title-main">Sinoatrial node</span> Group of cells located in the wall of the right atrium of the heart

The sinoatrial node is an oval shaped region of special cardiac muscle in the upper back wall of the right atrium made up of cells known as pacemaker cells. The sinus node is approximately 15 mm long, 3 mm wide, and 1 mm thick, located directly below and to the side of the superior vena cava.

<span class="mw-page-title-main">Cardiac conduction system</span> Aspect of heart function

The cardiac conduction system(CCS) (also called the electrical conduction system of the heart) transmits the signals generated by the sinoatrial node – the heart's pacemaker, to cause the heart muscle to contract, and pump blood through the body's circulatory system. The pacemaking signal travels through the right atrium to the atrioventricular node, along the bundle of His, and through the bundle branches to Purkinje fibers in the walls of the ventricles. The Purkinje fibers transmit the signals more rapidly to stimulate contraction of the ventricles.

The cardiovascular centre is a part of the human brain which regulates heart rate through the nervous and endocrine systems. It is considered one of the vital centres of the medulla oblongata.

The baroreflex or baroreceptor reflex is one of the body's homeostatic mechanisms that helps to maintain blood pressure at nearly constant levels. The baroreflex provides a rapid negative feedback loop in which an elevated blood pressure causes the heart rate to decrease. Decreased blood pressure decreases baroreflex activation and causes heart rate to increase and to restore blood pressure levels. Their function is to sense pressure changes by responding to change in the tension of the arterial wall The baroreflex can begin to act in less than the duration of a cardiac cycle and thus baroreflex adjustments are key factors in dealing with postural hypotension, the tendency for blood pressure to decrease on standing due to gravity.

<span class="mw-page-title-main">Heart rate variability</span> Variation in the time intervals between heartbeats

Heart rate variability (HRV) is the physiological phenomenon of variation in the time interval between heartbeats. It is measured by the variation in the beat-to-beat interval.

The oculocardiac reflex, also known as Aschner phenomenon, Aschner reflex, or Aschner–Dagnini reflex, is a decrease in pulse rate associated with traction applied to extraocular muscles and/or compression of the eyeball. The reflex is mediated by nerve connections between the ophthalmic branch of the trigeminal cranial nerve via the ciliary ganglion, and the vagus nerve of the parasympathetic nervous system. Nerve fibres from the maxillary and mandibular divisions of the trigeminal nerve have also been documented. These afferents synapse with the visceral motor nucleus of the vagus nerve, located in the reticular formation of the brain stem. The efferent portion is carried by the vagus nerve from the cardiovascular center of the medulla to the heart, of which increased stimulation leads to decreased output of the sinoatrial node. This reflex is especially sensitive in neonates and children, particularly during strabismus correction surgery. Oculocardiac reflex can be profound during eye examination for retinopathy of prematurity. However, this reflex may also occur with adults. Bradycardia, junctional rhythm and asystole, all of which may be life-threatening, can be induced through this reflex. This reflex has been seen to occur during many pan facial trauma surgeries due to stimulation of any of the three branches of trigeminal nerve.

The Hering–Breuer inflation reflex, named for Josef Breuer and Ewald Hering, is a reflex triggered to prevent the over-inflation of the lung. Pulmonary stretch receptors present on the wall of bronchi and bronchioles of the airways respond to excessive stretching of the lung during large inspirations.

The Bainbridge reflex or Bainbridge effect, also called the atrial reflex, is an increase in heart rate due to an increase in central venous pressure. Increased blood volume is detected by stretch receptors located in both sides of atria at the venoatrial junctions.

<span class="mw-page-title-main">Wandering atrial pacemaker</span> Medical condition

Wandering atrial pacemaker (WAP) is an atrial rhythm where the pacemaking activity of the heart originates from different locations within the atria. This is different from normal pacemaking activity, where the sinoatrial node is responsible for each heartbeat and keeps a steady rate and rhythm. Causes of wandering atrial pacemaker are unclear, but there may be factors leading to its development. It is often seen in the young, the old, and in athletes, and rarely causes symptoms or requires treatment. Diagnosis of wandering atrial pacemaker is made by an ECG.

<span class="mw-page-title-main">Polyvagal theory</span> Unproven constructs pertaining to the vagus nerve

Polyvagal theory is a collection of unproven, evolutionary, neuroscientific, and psychological constructs pertaining to the role of the vagus nerve in emotion regulation, social connection and fear response, introduced in 1994 by Stephen Porges.

Cold shock response is a series of neurogenic cardio-respiratory responses caused by sudden immersion in cold water.

The Bezold–Jarisch reflex involves a variety of cardiovascular and neurological processes which cause hypopnea, hypotension and bradycardia in response to noxious stimuli detected in the cardiac ventricles. The reflex is named after Albert von Bezold and Adolf Jarisch Junior. The significance of the discovery is that it was the first recognition of a chemical (non-mechanical) reflex.

<span class="mw-page-title-main">Stephen Porges</span> Scientist and professor

Stephen W. Porges is an American psychologist and neuroscientist. He is the Professor of Psychiatry at the University of North Carolina at Chapel Hill. Porges is also currently Director of the Kinsey Institute Traumatic Stress Research Consortium at Indiana University Bloomington, which studies trauma. He was previously a professor at the University of Illinois, Chicago, where he was director of the Brain-Body Center at the College of Medicine, and at the University of Maryland.

A vagal maneuver is an action used to stimulate the parasympathetic nervous system by activating the vagus nerve. The vagus nerve is the longest nerve of the autonomic nervous system and helps regulate many critical aspects of human physiology, including heart rate, blood pressure, sweating, and digestion through the release of acetylcholine. Common maneuvers that activate the vagus nerve include the Valsalva maneuver and carotid sinus massage, which can serve diagnostic or therapeutic functions.

<span class="mw-page-title-main">Arrhythmia</span> Group of medical conditions characterized by irregular heartbeat

Arrhythmias, also known as cardiac arrhythmias, heart arrhythmias, or dysrhythmias, are irregularities in the heartbeat, including when it is too fast or too slow. A resting heart rate that is too fast – above 100 beats per minute in adults – is called tachycardia, and a resting heart rate that is too slow – below 60 beats per minute – is called bradycardia. Some types of arrhythmias have no symptoms. Symptoms, when present, may include palpitations or feeling a pause between heartbeats. In more serious cases, there may be lightheadedness, passing out, shortness of breath or chest pain. While most cases of arrhythmia are not serious, some predispose a person to complications such as stroke or heart failure. Others may result in sudden death.

Neurocardiology is the study of the neurophysiological, neurological and neuroanatomical aspects of cardiology, including especially the neurological origins of cardiac disorders. The effects of stress on the heart are studied in terms of the heart's interactions with both the peripheral nervous system and the central nervous system.

<span class="mw-page-title-main">Sinus arrhythmia</span> Irregular heart rhythm originating in the sinus node

Sinus arrhythmia is a commonly encountered variation of normal sinus rhythm. Sinus arrhythmia characteristically presents with an irregular rate in which the variation in the R-R interval vary by more than 0.12 seconds. Additionally, P waves are typically mono-form and in a pattern consistent with atrial activation originating from the sinus node.

References

  1. 1 2 3 4 5 6 Berntson GG, Cacioppo JT, Quigley KS (March 1993). "Respiratory sinus arrhythmia: autonomic origins, physiological mechanisms, and psychophysiological implications". Psychophysiology. 30 (2): 183–96. doi:10.1111/j.1469-8986.1993.tb01731.x. PMID   8434081.
  2. Diamond LM, Fagundes CP, Butterworth MR (2011). "Attachment Style, Vagal Tone, and Empathy During Mother-Adolescent Interactions". Journal of Research on Adolescence. 22 (1): 165–184. doi:10.1111/j.1532-7795.2011.00762.x.
  3. Grossman P, Wilhelm FH, Spoerle M (August 2004). "Respiratory sinus arrhythmia, cardiac vagal control, and daily activity". American Journal of Physiology. Heart and Circulatory Physiology. 287 (2): H728–34. doi:10.1152/ajpheart.00825.2003. PMID   14751862.
  4. 1 2 Howland RH (June 2014). "Vagus Nerve Stimulation". Current Behavioral Neuroscience Reports. 1 (2): 64–73. doi:10.1007/s40473-014-0010-5. PMC   4017164 . PMID   24834378.
  5. 1 2 Porges SW, Doussard-Roosevelt JA, Maiti AK (2008). "Vagal tone and the physiological regulation of emotion". Monographs of the Society for Research in Child Development. 59 (2–3): 167–86. doi:10.1111/j.1540-5834.1994.tb01283.x. PMID   7984159.
  6. Brock C, Jessen N, Brock B, Jakobsen PE, Hansen TK, Rantanen JM, Riahi S, Dimitrova YK, Dons-Jensen A, Aziz Q, Drewes AM, Farmer AD (October 2017). "Cardiac vagal tone, a non-invasive measure of parasympathetic tone, is a clinically relevant tool in Type 1 diabetes mellitus". Diabetic Medicine. 34 (10): 1428–1434. doi:10.1111/dme.13421. PMID   28703868. S2CID   25030686.
  7. 1 2 3 Montano N, Ruscone TG, Porta A, Lombardi F, Pagani M, Malliani A (October 1994). "Power spectrum analysis of heart rate variability to assess the changes in sympathovagal balance during graded orthostatic tilt". Circulation. 90 (4): 1826–31. doi: 10.1161/01.CIR.90.4.1826 . PMID   7923668.
  8. Nunan D, Sandercock GR, Brodie DA (November 2010). "A quantitative systematic review of normal values for short-term heart rate variability in healthy adults". Pacing and Clinical Electrophysiology. 33 (11): 1407–17. doi:10.1111/j.1540-8159.2010.02841.x. PMID   20663071. S2CID   44378765.
  9. Ludwig, Carl (1847). "On the influence of respiratory movements on blood flow in the aortic system [in German]". Arch Anat Physiol Leipzig. 13: 242–302.
  10. De Burgh Daly M (1985), "Interactions Between Respiration and Circulation", Comprehensive Physiology, John Wiley & Sons, Inc., pp. 529–594, doi:10.1002/cphy.cp030216, ISBN   9780470650714
  11. Hathorn MK (April 1987). "Respiratory sinus arrhythmia in new-born infants". The Journal of Physiology. 385: 1–12. doi:10.1113/jphysiol.1987.sp016480. PMC   1192333 . PMID   3656159.
  12. Myers MM, Fifer W, Haiken J, Stark RI (June 1990). "Relationships between breathing activity and heart rate in fetal baboons". The American Journal of Physiology. 258 (6 Pt 2): R1479–85. doi:10.1152/ajpregu.1990.258.6.R1479. PMID   2360694.
  13. Hayano J, Yasuma F, Okada A, Mukai S, Fujinami T (August 1996). "Respiratory sinus arrhythmia. A phenomenon improving pulmonary gas exchange and circulatory efficiency". Circulation. 94 (4): 842–7. doi:10.1161/01.CIR.94.4.842. PMID   8772709.
  14. Castellini MA, Rea LD, Sanders JL, Castellini JM, Zenteno-Savin T (November 1994). "Developmental changes in cardiorespiratory patterns of sleep-associated apnea in northern elephant seals". The American Journal of Physiology. 267 (5 Pt 2): R1294–301. doi:10.1152/ajpregu.1994.267.5.R1294. PMID   7977857.
  15. 1 2 Bartsch RP, Schumann AY, Kantelhardt JW, Penzel T, Ivanov PC (June 2012). "Phase transitions in physiologic coupling". Proceedings of the National Academy of Sciences of the United States of America. 109 (26): 10181–6. Bibcode:2012PNAS..10910181B. doi: 10.1073/pnas.1204568109 . PMC   3387128 . PMID   22691492.
  16. Hayano J, Sakakibara Y, Yamada M, Kamiya T, Fujinami T, Yokoyama K, Watanabe Y, Takata K (March 1990). "Diurnal variations in vagal and sympathetic cardiac control". The American Journal of Physiology. 258 (3 Pt 2): H642–6. doi:10.1152/ajpheart.1990.258.3.H642. PMID   2316678.
  17. Porges SW (1986), "Respiratory Sinus Arrhythmia: Physiological Basis, Quantitative Methods, and Clinical Implications", Cardiorespiratory and Cardiosomatic Psychophysiology, Springer US, pp. 101–115, doi:10.1007/978-1-4757-0360-3_7, ISBN   9781475703627
  18. Pagani M, Lombardi F, Guzzetti S, Rimoldi O, Furlan R, Pizzinelli P, Sandrone G, Malfatto G, Dell'Orto S, Piccaluga E (August 1986). "Power spectral analysis of heart rate and arterial pressure variabilities as a marker of sympatho-vagal interaction in man and conscious dog". Circulation Research. 59 (2): 178–93. doi: 10.1161/01.RES.59.2.178 . PMID   2874900.
  19. Grossman P, van Beek J, Wientjes C (November 1990). "A comparison of three quantification methods for estimation of respiratory sinus arrhythmia". Psychophysiology. 27 (6): 702–14. doi:10.1111/j.1469-8986.1990.tb03198.x. PMID   2100356.
  20. Dick TE, Hsieh YH, Dhingra RR, Baekey DM, Galán RF, Wehrwein E, Morris KF (2014). Cardiorespiratory coupling: common rhythms in cardiac, sympathetic, and respiratory activities. Progress in Brain Research. Vol. 209. Elsevier. pp. 191–205. doi:10.1016/b978-0-444-63274-6.00010-2. ISBN   9780444632746. PMC   4052709 . PMID   24746049.
  21. Grossman, Paul; Taylor, Edwin W. (2007). "Toward understanding respiratory sinus arrhythmia: relations to cardiac vagal tone, evolution and biobehavioral functions". Biological Psychology. 74 (2): 263–285. doi:10.1016/j.biopsycho.2005.11.014. ISSN   0301-0511. PMID   17081672. S2CID   16818862.
  22. 1 2 Hayano, Junichiro; Yasuma, Fumihiko (2003-04-01). "Hypothesis: respiratory sinus arrhythmia is an intrinsic resting function of cardiopulmonary system". Cardiovascular Research. 58 (1): 1–9. doi: 10.1016/s0008-6363(02)00851-9 . ISSN   0008-6363. PMID   12667941.
  23. Ben-Tal A, Shamailov SS, Paton JF (April 2012). "Evaluating the physiological significance of respiratory sinus arrhythmia: looking beyond ventilation-perfusion efficiency". The Journal of Physiology. 590 (8): 1989–2008. doi:10.1113/jphysiol.2011.222422. PMC   3573317 . PMID   22289913.
  24. Hayano J, Yasuma F, Okada A, Mukai S, Fujinami T (August 1996). "Respiratory sinus arrhythmia. A phenomenon improving pulmonary gas exchange and circulatory efficiency". Circulation. 94 (4): 842–7. doi:10.1161/01.cir.94.4.842. PMID   8772709.
  25. 1 2 Lewis GF, Furman SA, McCool MF, Porges SW (February 2012). "Statistical strategies to quantify respiratory sinus arrhythmia: are commonly used metrics equivalent?". Biological Psychology. 89 (2): 349–64. doi:10.1016/j.biopsycho.2011.11.009. PMC   3269511 . PMID   22138367.
  26. 1 2 3 Graziano P, Derefinko K (September 2013). "Cardiac vagal control and children's adaptive functioning: a meta-analysis". Biological Psychology. 94 (1): 22–37. doi:10.1016/j.biopsycho.2013.04.011. PMC   4074920 . PMID   23648264.
  27. Masi CM, Hawkley LC, Rickett EM, Cacioppo JT (February 2007). "Respiratory sinus arrhythmia and diseases of aging: obesity, diabetes mellitus, and hypertension". Biological Psychology. 74 (2): 212–23. doi:10.1016/j.biopsycho.2006.07.006. PMC   1804292 . PMID   17034928.
  28. Connell AM, Hughes-Scalise A, Klostermann S, Azem T (October 2011). "Maternal depression and the heart of parenting: respiratory sinus arrhythmia and affective dynamics during parent-adolescent interactions". Journal of Family Psychology. 25 (5): 653–62. doi:10.1037/a0025225. PMID   21875198.
  29. Porges, SW; Doussard-Roosevelt, JA; Maiti, AK (1994). "Vagal tone and the physiological regulation of emotion". Monographs of the Society for Research in Child Development. 59 (2–3): 167–86. doi:10.1111/j.1540-5834.1994.tb01283.x. ISSN   0037-976X. JSTOR   1166144. PMID   7984159. A review of research indicates that baseline levels of cardiac vagal tone and vagal tone reactivity abilities are associated with behavioral measures of reactivity, the expression of emotion, and self-regulation skills. Thus, we propose that cardiac vagal tone can serve as an index of emotion regulation. Historically, the vagus and other components of the parasympathetic nervous system have not been incorporated in theories of emotion.
  30. 1 2 Porges SW (July 1995). "Orienting in a defensive world: mammalian modifications of our evolutionary heritage. A Polyvagal Theory". Psychophysiology. 32 (4): 301–18. doi: 10.1111/j.1469-8986.1995.tb01213.x . PMID   7652107.
  31. Porges SW (August 2003). "The Polyvagal Theory: phylogenetic contributions to social behavior". Physiology & Behavior. 79 (3): 503–13. doi:10.1016/S0031-9384(03)00156-2. PMID   12954445. S2CID   14074575.
  32. Porges SW (December 2003). "Social engagement and attachment: a phylogenetic perspective". Annals of the New York Academy of Sciences. 1008 (1): 31–47. Bibcode:2003NYASA1008...31P. doi:10.1196/annals.1301.004. PMID   14998870. S2CID   1377353.
  33. Monteiro, Diana (2018). "Cardiorespiratory interactions previously identified as mammalian are present in the primitive lungfish". Science Advances. 4 (2): eaaq0800. Bibcode:2018SciA....4..800M. doi: 10.1126/sciadv.aaq0800 . PMC   5833999 . PMID   29507882.
  34. Taylor, E. W. (2010). "Autonomic control of cardiorespiratory interactions in fish, amphibians and reptiles". Brazilian Journal of Medical and Biological Research. 43 (7): 600–610. doi: 10.1590/S0100-879X2010007500044 . PMID   20464342.
  35. 1 2 Malik, M.; Bigger, J. T.; Camm, A. J.; Kleiger, R. E.; Malliani, A.; Moss, A. J.; Schwartz, P. J. (March 1996). "Heart rate variability. Standards of measurement, physiological interpretation, and clinical use. Task Force of the European Society of Cardiology and the North American Society of Pacing and Electrophysiology". European Heart Journal. 17 (3): 354–81. doi: 10.1093/oxfordjournals.eurheartj.a014868 . PMID   8737210.
  36. Myers MM, Elliott AJ, Odendaal HJ, Burd L, Angal J, Groenewald C, Nugent JD, Yang JS, Isler JR, Dukes KA, Robinson F, Fifer WP (August 2017). "Cardiorespiratory physiology in the safe passage study: protocol, methods and normative values in unexposed infants". Acta Paediatrica. 106 (8): 1260–1272. doi:10.1111/apa.13873. PMC   5530586 . PMID   28419567.
  37. DeBenedittis G, Cigada M, Bianchi A, Signorini MG, Cerutti S (April 1994). "Autonomic changes during hypnosis: a heart rate variability power spectrum analysis as a marker of sympatho-vagal balance". The International Journal of Clinical and Experimental Hypnosis. 42 (2): 140–52. doi:10.1080/00207149408409347. PMID   8200716.