Vagus activation and stress response from an osteopathic perspective
Vagus activation

Vagus activation and stress response from an osteopathic perspective

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Summary

In addition to the superordinate regulation by means of the mesencephalic periaqueductal grey, the neurovegetative system - including vagus activity - is essential in the regulation of stress reactions. This paper explains, discusses and presents essential study results and correlations, dysfunction mechanisms, diagnostics and osteopathic treatment approaches and techniques as well as self-management approaches for the regulation of the vagus.

 

Keywords

Vagal mechanisms of action, vagus dysfunction, diagnosis and interpretation of vagus activity, self-help approaches, osteopathic vagus nerve stimulation (VNS), mesencephalic periaqueductal grey, psychosomatic osteopathy.

 

Abstract

Besides the superordinate regulation by means of the mesencephalic periaqueductal grey, the neurovegetative - among others the vagus activity - is essential in the regulation of stress reactions. This article explains, discusses and presents essential study results and correlations, dysfunction mechanisms, diagnostics and osteopathic treatment approaches and techniques as well as self-management approaches for the regulation of the vagus.

 

Keywords

vagal mechanisms of action, vagus dysfunction, diagnosis and interpretation of vagus activity, self-help approaches, osteopathic vagus nerve stimulation (VNS), mesencephalic periaqueductal grey, psychosomatic osteopathy

Introduction

Superordinate behavioural states such as fight and flight, immobilisation or freezing state and risk assessment - with the associated motor, autonomic and endocrine effects - are coordinated by the mesencephalic periaqueductal grey (PAG) [21], [45], [49], [92]. In this process, vagal afferents are transmitted through the nucleus tractus solitarii to the PAG, hypothalamus, amygdala as well as to the insular, cingulate and prefrontal cortex, where they are integrated into emotional and cognitive processes [7], [19], [20], [95].

Even though popular polyvagal theory does not adequately account for these anatomical features and mechanisms of action, the vagus is nevertheless highly significant [65], [66]. Thus, subdiaphragmatic vagal afferents appear to influence innate fear, learned fear and other behaviours [53], [54]. In addition, vagal afferents modulate spinal nociceptive processes in various experimental models [29], [50].

Evolutionarily, the autonomic nervous system regulated and still regulates the maintenance of the most important bodily functions. Prey animals, for example, reacted to danger from predators by freezing and shutting down their metabolism. This behaviour was regulated by the parasympathetic nervous system, which prioritised such behaviour over metabolic functions if necessary. This clearly shows how the survival of the organism as a whole is hierarchically prioritised in regulatory systems. before individual organ functions. The sympathetic nervous system developed in connection with flight instead of freezing behaviour as well as hunting instinct and fight control mechanisms. This manifests itself in pupil dilation (better twilight vision and sharper peripheral vision), dilation of the limb and lung blood vessels (necessary for flight and fight behaviour) and an increase in stress hormones for faster reactions and glucose supply. Here, too, the focus is on the whole organism and not exclusively on the functioning of individual organs.

The parasympathetic and sympathetic nervous systems do not necessarily act antagonistically. Unmyelinated fibres, mainly originating from the dorsalis nervi vagi nerve, regulate blood flow and activity of the abdominal organs, while myelinated fibres, originating from the ambiguus nerve, regulate the thoracic organs of the heart and lungs as well as speech (superior laryngeal and recurrent nerve) and the hearing of human speech (including the stapedius nerve after connection with the facial nerve). There are also vagal influences on heart rate variability (HRV), blood sugar control and the immune system, as well as voice pitch, appetite and bronchial function. The vagus nerve acts as a link between the peripheral autonomic nervous system and the brain. It also facilitates the storage of memories. Vagus nerve stimulation has been shown to have brain plasticity and memory enhancing effects [69].

Afferents exist in particular from the intestine and other abdominal organs. Thus, afferent fibres of the vagus nerve metabolically influence the microglia of the brain [108].. Normally, the central nervous system is protected by the blood-brain barrier. However, it can potentially be damaged by the vagus, in that efferent from the gastrointestinal tract can activate microglia in vagal structures and alter gut-brain communication [4].

Pathophysiologically, the vagus is important, for example, in headaches, depression and post-traumatic stress disorder (PTSD). In addition, the vagus nerve also has a strong influence on the immune system, heart rate variability, blood sugar control, the development and modulation of headaches (including migraine via serotonin release), our voice pitch, the function of our bronchial tubes, appetite control, the development of depression, etc. [49], [61], [76], [94], [94]. [49], [61], [76], [94], [104].

With increasing age, changes occur at least in the thicker somatomotor vagus fibres, which thin out as they progress [109].

Vagus dysfunctions

Decreased vagus activity

  • Decreased vagus activity occurs, for example, in autoimmune diseases such as ulcerative colitis, lowered immunity, malabsorption and obesity. 
  • Hypotonic vagal activity with normotonic activity of the enteric nervous system can occur in alcohol abuse and type 2 diabetes mellitus. In addition to alcohol abstinence, the vagus nerve can be stimulated therapeutically (see below). 
  • Hypotonic vagal activity with hypotonic activity of the enteric nervous system carries a high risk for neurodegenerative disease patterns. Here, the low immune status should first be improved and the viral load reduced [59], [60] and only then should the vagus nerve be stimulated. In addition, the small intestine region can be stretched to increase myenteric activity [59], [60].

 

Increased vagus activity

The vagus activity can not only be decreased but also increased in a dysfunctional way. 

  • Increased vagus activity occurs, for example, in allergies, Crohn's disease and obesity. 
  • In the case of hypertonic vagus activity, OMT can be used to stretch the diaphragm, the radix mesenterii and the high cervical region.
  • Increased vagus activity in young people can lead to an increase in gastric acid production, increased gastric emptying and possibly diarrhoea. Here, in addition to manual approaches, the mouth region should be cleaned and the pathogen load reduced.

 

Diagnostics

By sense of smell - Hold lavender essential oil under the nose: Stimulation of the vagus promotes gastric emptying. This can be heard, e.g. with the stethoscope in the region of the pylorus. [113]

By means of swallowing -. Drinking a glass of water is used to test the vagus in the oesophagus (norm about 5 seconds; in case of reduced activity and e.g. Parkinson's disease, the swallowing period is reduced).

By means of HRV measurement -. HRV measurement parameters provide insight into the autonomic function of the heart and allow assessments of the functioning of the autonomic nervous system [39]. The vagus nerve conducts information much faster than the sympathetic nervous system. Thus, vagus activation of heart rate is up to 8-fold faster compared to sympathetic activation, so that fluctuations in heart rate are much more strongly determined by the vagus [23].

Using the Ruffier-Dickson test to determine hypotension of the vagus nerve -. After 1 minute in supine position, measure the pulse beats (P1), perform knee bends 30× or for 45 seconds, then measure pulse beats in standing position immediately afterwards (P2) and again after 1 minute in supine position (P3).

The Dickson index is used to assess the heart's ability to recover after exercise. This value correlates with HRV, O2max-measurements, lung elasticity, diaphragmatic mobility, gastric emptying and nitric oxide.

Calculation of the Dickson Index

((P2-70) + 2 (P3-P1))/10

 

Evaluation

<0 = exzellent, 0–2 = sehr gut, 2–4 = gut, 4–6 = mittel, 6–8 = schwach, 8–10 = sehr schwach, >10 = schlechte Anpassung

 

Other possible indications for reduced vagus activity

  • Reduced neck mobility and jaw disorders, CMD (craniomandibular dysfunction).
  • Visceral fat: Here, an abdominal circumference measurement can be taken (vagus activity is reduced in overweight, dysfunctionally increased in obesity).
  • Compression of the pars descendens of the duodenum with the risk of reflux.
  • Positive trigger points of the neck and jaw muscles.
  • Tension restrictions in the area of the vagina carotica.
  • Positive Gesret's point: This is usually located intercostally under the left axilla, more rarely on the right. The test is positive for tenderness and palpation of a kind of fat ball in this region.
  • Viral loads: by blood tests.
  • Presence of proprionibacteria in the oral region: Findings by means of UV lamp.

 

Vagus nerve stimulation (VNS) 

For an overview, see also [62].

Stimulation of the vagus nerve during exposure therapy - as possibly applied in the osteopathic approach of Liem's multimodal bifocal integration - eliminates anxiety, hypervigilance, avoidance behaviour and antisocial behaviour in animal experiments on post-traumatic stress disorder (PTSD) [3], [82], [86], [99], [100], [101], [102]. VNS enhanced the extinction of conditioned fear in experiments on rats, without [82], [85] and with PTSD [55], [98].. VNS can also counteract fear extinction disorders, reduce anxiety-like behaviour, improve other PTSD symptoms [32] and facilitate conditioned fear responses [86].

It has also been shown that the number of key molecules that promote synaptic plasticity can be increased by VNS, e.g.. Acetylcholine [81], Serotonin [75], Norepinephrine [93], Fibroblast growth factor-1 (FGF-1) and the growth factor BDNF (Brain-derived neurotrophic factor) [28], Neurogenesis [89], Fos (a nuclear protein expressed under conditions of high neuronal activity) [80], Tropomyosin receptor kinase B (TrkB) [31], neurexin, cadherin and calcium channels [2], NMDA-receptors (NMDA = N-methyl-D-aspartate) [2], [3].

Transcutaneous electrical vagus nerve stimulation simultaneously shows an improvement in neuronal plasticity, especially in combination with training [42], [43], e.g. in the locus coeruleus [41], [46] and memory consolidation [17], [18], [85].. The combination of VNS with sensory or motor events is able to reorganise the sensory or motor cortex [11].

The combination of VNS and exposure to unamplified conditioned signals was able to enhance the extinction of infralimbic prefrontal cortex - basolateral amygdala signalling pathways in animal experiments [3], [86].

There is evidence that VNS should be used in combination with exposure-based approaches to extinguish conditioned fear and that its isolated application is not sufficient [78].

An autonomic vagovagal loop reaches visceral impulses into the Ncl. tractus solitarii (NTS), which transmits efferents to the Ncl. dorsalis nervi vagi (DMN) to the rostral ventrolateral medulla (RVLM) and to the intermediate lateral medulla (ILM), with the aim of achieving a balance between sympathetic and parasympathetic responses to different physical states. The vagus does not act in isolation. Modulations of the vagovagal loop are triggered by an autonomic forebrain loop, via interactions between the NTS and other brain areas such as the hypothalamus, amygdala, cingulate cortex, insular cortex, prefrontal cortex, which are also involved in neuroendocrine, emotional and cognitive behavioural controls (see Fig. 1).

Vagovagal loop and influencing factors
Fig. 1: Vagovagal loop and influencing factors (from [62]; © Thieme-Verlag, with kind permission).

Indication

Reorganisation of the sensory or motor cortex [11], post-traumatic stress disorder and anxiety disorders [13], [34], [58], [78], [82] as well as chronic low-threshold inflammation, for anti-inflammation, e.g. rheumatoid arthritis.e.g. in rheumatoid arthritis; anti-tumour necrosis factor α (anti-TNF-α), i.e. anti-inflammatory effect, gastroduodenal emptying disorders, possibly drug-resistant epilepsy, depression [9].

 

Vagus stimulation in the craniocervical region according to Liem 

Hand position

  • Thumb in the area of the cavum conchae (ramus auricularis nervi vagi)
  • Index finger on the anguli mastoideae.
  • Middle finger to the mastoids.
  • Ring finger and little finger in the area of the atlantooccipital joint (see Fig. 2).

 

Fig. 2 Legend: Vagus stimulation in the craniocervical region

 

Version

  • The skin in the area of both concha auricularis [44] is stimulated manually with the thumbs and the auricular branches on the proc. mastoideus are stimulated gently with the middle fingers.
  • The index fingers anteriorise the lower jaw. 
  • The ring finger and little finger exert suboccipital inhibition or decompression in the suboccipital region and near the jugular foramen. Here, not only a vagus-stimulating effect but also a cerebral blood flow improvement has already been demonstrated [24], [88], [91].

 

Note

The vagus nerve passes through the middle part of the jugular foramen, caudal to the glossopharyngeal nerve and superficial to the internal jugular vein.

 

Stimulation can also be done by electrostimulation in the ear area following Bonaz or on the mastoid and below the diaphragm [9]. The vagus can be stimulated on the mastoid and diaphragm with a TENS unit at 10 hertz. Needling is also possible [44]

 

Vagus stimulation in the area of the vagina carotica 

The vagus nerve can also be gently stimulated in the area of the vagina carotica. The middle fingers of both hands are positioned about 1 cm apart, medial to the sternocleidomastoid muscle - between the common carotid artery and the internal jugular vein, just below the thyroid cartilage. Stimulation in the region of the course of the vagus nerve is by means of craniocaudal gentle mobilisation.

Fig. 3. legend: Vagus stimulation in the area of the vagina carotica

 

Vagus stimulation in the area of the diaphragm

Medially, the deep diaphragmatic region in the area of the oesophagus (Truncus vagalis anterior and posterior). To do this, let the thumbs sink into the depths on both sides of the xiphoid and follow micro-movements in the area of the oesophagus while the other fingers rest on the lower intercostal spaces. At the same time, the patient slows down breathing by about half.

In the second step the coeliac ganglion, about midway between the navel and the xiphoid, relax (see also Fulford technique [62], p. 520).

 

Reorganisation of the sensory or motor cortex

This allows sensory or motor stimuli, movements, postures and functional OMT to be combined with VNS. In addition, VNS is also used within the framework of multimodal bifocal integration according to Liem. When practising osteopathic heart-focused palpation according to Liem, a vagus-stimulating effect could be proven [112].

 

Further OMT approaches

Rib raising techniques [24] and High-Velocity/Low-Amplitude Techniques (HVLAT) [88] can have a vagus activating effect. A single OMT session in healthy participants already led to a faster recovery of heart rate and sympathovagal balance and prevented the typical rise in cortisol levels after a psychological stressor [30]. 

 

Self-help approaches

Patients can stimulate the vagus independently by the following measures to reduce stress reactions. These can be used as an adjunct to treatment [63], [64]:

 

Deep and slowed breathing with or without HRV feedback. [1], [57], [77] - In a study in which other yogic breathing techniques and kriyas were. - which are physical purification techniques (Ujjayi breathing, Bhastrika, Sudarshan Kriya) - were practised, it was assumed that they have a parasympathetic activating effect [14].

 

Autogenic training [79], Yoga [103] and Tai Chi [15], [71], [72], [111] are said to have vagal activating effects. However, since there are very different types of yoga, e.g. very calm ones like yin yoga, and at the same time very dynamic types like power yoga, future studies should examine the different forms for their vagal effect.

 

Meditation [35], [106] - For example, "loving kindness meditation" increased positive emotions through improved perception of social relationships, which in turn led to an increase in vagal tone. However, this effect was only achieved in those who actually felt increased joy and social connectedness [56]. It is suspected that vagal activation also occurs via deep breathing during meditation [35]. Since there are very different types of meditation, just as in yoga, these variations could be taken into account in future studies.

 

Increase in oxytocin - All interventions that lead to an increase in oxytocin (and vasopressin), such as massage, touch, etc., can be recommended as these improve parasympathetic function [25], [48], [90].

 

Singing, humming, mantra chanting -. Singing increases HRV in healthy 18-year-old women and men. However, this has only been investigated in one study so far. Humming, hymn singing, energetic singing and mantra chanting have each been reported to increase HRV in slightly different ways [107]. For example, singing, especially energetic singing, is also said to be simultaneously arousing, but without significant sympathetic activity, possibly because the vagally triggered activity dampens the sympathetic one. This physiological reaction in singing is said to be able to trigger the homeostatic state of flow [107].

There are two ways in which music could communicate the state of the ANS between singers: Through the laryngeal vocal cord muscles used in singing, mediated by the reccurens nerve of the vagus nerve as well as through a kind of vagal pump stimulated during singing [107]. Chanting the mantra "Om" also activates the vagus. The authors suggest that this may happen through stimulation of its auricular branches [51]. Both mantra and prayer recitation in a study of 23 adults caused an increase in existing cardiovascular rhythms, HRV, and a decrease in blood pressure with rhythm formulas involving breathing at 6 breaths per minute [6]. Singing is also said to release oxytocin [36].

 

Laughter - in a pilot study on laughter yoga, participants showed improved immediate mood and increased HRV after a laughter intervention [22].

 

Pleasant social interaction - Vagal activity increase through the interaction of parental and child positive socialisation [87].

 

Cold exposure - Cold showers and other cold interventions increased parasympathetic activity via activation of cholinergic neurons by the vagus nerve [114], especially when they are repeatedly exercised over a long period of time. Thus, habituation may be associated with decreased sympathetic and concomitant increased parasympathetic activation during cold exposure [40]. The study in humans was conducted at 10°C cold [74]. Acute cold interventions of 4°C also led to parasympathetic stimulation in animal experiments [114].

Before starting the cold intervention, it should be medically clarified whether cold applications should be modified or are contraindicated for certain diseases, such as heart disease. 

 

Tip: Take a cold shower every morning. 

 

Nutrition, food supplements

  • Probiotics such as Lactobacillus rhamnosus, which caused a reduction in stress hormones, depression and anxiety behaviour by means of the vagus nerve [12]. Bifidobacterium longum was also able to reduce anxiety behaviour via the vagus nerve [5].
  • Omega-3 fatty acids, especially rich in fatty fish species [16], [83], [96], [97].
  • Serotonin: Intestinal serotonin stimulates 5-HT3 receptors of vagal afferent fibres to stimulate vagal sensory neurons [115]..
  • Choline: By increasing vagal activity, choline, e.g. contained in eggs, can improve cardiovascular damage [68].
  • Zinc: Orally administered zinc increases food intake by vagal stimulation in rats during early-stage zinc deficiency (i.e. without decreasing plasma and tissue zinc concentrations) [84].

 

Tip: Make sure you get enough zinc in your diet.

 

Fasting - Fasting increases vagal activity [52]: In animal studies, intermittent fasting, as well as calorie-reduced food intake, led to a decrease in the low-frequency component of DPV spectra, a marker of sympathetic tone, and an increase in the high-frequency components of HRV spectra, a marker of parasympathetic activity [73].

 

Physical exercise - Light to moderate physical exercise appears to stimulate gastric emptying by increasing vagal activity [110].

 

Massage - For example, foot massage [70]. Massage by means of vagal stimulation can also support weight gain in premature births [26], [27]. Massage of the sinus carotids can even suppress epileptic seizures [37]. This type of massage should only be performed by specialist therapists.

 

Sleeping position - Sleeping on the right side: In a study of the effect of lying positions on autonomic nerve modulation in patients with coronary artery disease, it was found that vagal activity was highest and sympathetic arousal lowest in the right lateral position. Vagal modulation in the supine position was significantly lowest of all sleep positions studied [113].

 

Electromagnetic fields - Exposure to pulsed electromagnetic fields for 20 minutes resulted in a faster recovery of heart rate variability, especially in the very low frequency range after exercise. After the magnetic field exposure was stopped, the described effects quickly subsided [38].

 

Glucagon-like peptide-1 secretion -. GLP-1 inhibits gastric emptying via vagal afferent-mediated central mechanisms [47]. Stimulation of endogenous GLP-1 secretion by manipulating dietary composition may be a relevant strategy for the treatment of obesity and type 2 diabetes. GLP-1 is mainly synthesised and secreted by enteroendocrine L cells of the digestive tract. Its secretion is mediated in part by direct nutrient uptake through G-protein-coupled receptors. These bind to monosaccharides, peptides and amino acids, monounsaturated and polyunsaturated fatty acids, and short-chain fatty acids. High-fibre foods, nuts, avocados and eggs also appear to influence GLP-1 [8].

Liem T. Vagus activation and stress response from an osteopathic perspective, Osteop Med 2021; 22(4), 10-15.

https://www.sciencedirect.com/science/article/pii/S1615907121001118

literature

  1. Alayan N, Eller L, Bates ME et al. Current evidence on heart rate variability biofeedback as a complementary anticraving intervention. J Altern Complement Med. 2018; 24 (11): 1039-1050.
  2. Alexander GM, Huang YZ, Soderblom EJ et al. Vagal nerve stimulation modifies neuronal activity and the proteome of excitatory synapses of amygdala/piriform cortex. J Neurochem. 2019; 140 (4): 629-644
  3. Alvarez-Dieppa AC, Griffin K, Cavalier S et al. Vagus nerve stimulation enhances extinction of conditioned fear in rats and modulates Arc protein, CaMKII, and GluN2B-containing NMDA receptors in the basolateral amygdala. Neural Plast. 2016; 2016
  4. Ballsmider LA, Vaughn AC, David M et al. Sleeve gastrectomy and Roux-en-Y gastric bypass alter the gut-brain communication. Neural Plast. 2015; 2015
  5. Bercik P, Park AJ, Sinclair D et al. The anxiolytic effect of Bifidobacterium longum NCC3001 involves vagal pathways for gut-brain communication. Neurogastroenterol Motil. 2011; 23 (12): 1132-1139
  6. Bernardi L, Sleight P, Bandinelli G et al. Effect of rosary prayer and yoga mantras on autonomic cardiovascular rhythms: comparative study. BMJ. 2001; 323 (7327): 1446-1449
  7. Berthoud H-R, Neuhuber WL. Functional and chemical anatomy of the afferent vagal system. Auton Neurosci. 2000; 85 (1-3): 1-17
  8. Bodnaruc AM, Prud'homme D, Blanchet R et al. Nutritional modulation of endogenous glucagon-like peptide-1 secretion: a review. Nutr Metab (Lond). 2016; 13 (1): 1-16
  9. Bonaz B, Picq C, Sinniger V et al. Vagus nerve stimulation: from epilepsy to the cholinergic anti-inflammatory pathway. Neurogastroenterol Motil. 2013; 25 (3): 208-221
  10. Bonaz B, Sinniger V, Pellissier S. Anti-inflammatory properties of the vagus nerve: potential therapeutic implications of vagus nerve stimulation. J Physiol. 2016; 594 (20): 5781-5790
  11. Borland MS, Vrana WA, Moreno NA et al. Cortical map plasticity as a function of vagus nerve stimulation intensity. Brain Stimul. 2016; 9 (1): 117-123
  12. Bravo JA, Forsythe P, Chew M V et al. Ingestion of Lactobacillus strain regulates emotional behaviour and central GABA receptor expression in a mouse via the vagus nerve. Proc Natl Acad Sci. 2011; 108 (38): 16050-16055
  13. Breit S, Kupferberg A, Rogler G et al. Vagus nerve as modulator of the brain-gut axis in psychiatric and inflammatory disorders. Front Psychiatry. 2018; 9: 44
  14. Brown RP, Gerbarg PL. Sudarshan Kriya yogic breathing in the treatment of stress, anxiety, and depression: part I-neurophysiologic model. J Altern Complement Med. 2005; 11 (1): 189-201.
  15. Chang R-Y, Koo M, Yu Z-R et al. The effect of t'ai chi exercise on autonomic nervous function of patients with coronary artery disease. J Altern Complement Med. 2008; 14 (9): 1107-1113
  16. Christensen JH. Omega-3 polyunsaturated fatty acids and heart rate variability. Front Physiol. 2011; 2: 84
  17. Clark KB, Krahl SE, Smith DC et al. Post-training unilateral vagal stimulation enhances retention performance in the rat. Neurobiol Learn Mem. 1995; 63 (3): 213-216
  18. Clark KB, Smith DC, Hassert DL et al. Posttraining electrical stimulation of vagal afferents with concomitant vagal efferent inactivation enhances memory storage processes in the rat. Neurobiol Learn Mem. 1998; 70 (3): 364-373
  19. Craig AD. How do you feel? Interoception: the sense of the physiological condition of the body. Nat Rev Neurosci. 2002; 3 (8): 655-666
  20. Critchley HD, Mathias CJ, Dolan RJ. Neuroanatomical basis for first- and second-order representations of bodily states. Nat Neurosci. 2001; 4 (2): 207-212
  21. Deng H, Xiao X, Wang Z. Periaqueductal gray neuronal activities underlie different aspects of defensive behaviors. J Neurosci. 2016; 36 (29): 7580-7588
  22. Dolgoff-Kaspar R, Baldwin A, Johnson MS et al. Effect of laughter yoga on mood and heart rate variability in patients awaiting organ transplantation: a pilot study. Altern Ther. 2012; 18 (4): 53-58
  23. Eller-Berndl D Heart rate variability. Verlag-Haus d. Ärzte; 2010
  24. Emmet D, Nuño V, Pierce-Talsma S. OMT to address the physiologic effects of stress. J Osteopath Med. 2018; 118 (2): e11-e11
  25. Esch T, Stefano GB. The neurobiology of love. Neuroendocrinol Lett. 2005; 26 (3): 175-192
  26. Field T, Diego M, Hernandez-Reif M. Preterm infant massage therapy research: a review. Infant Behav Dev. 2010; 33 (2): 115-124
  27. Field T, Diego M, Hernandez-Reif M. Potential underlying mechanisms for greater weight gain in massaged preterm infants. Infant Behav Dev. 2011; 34 (3): 383-389
  28. Follesa P, Biggio F, Gorini G et al. Vagus nerve stimulation increases norepinephrine concentration and the gene expression of BDNF and bFGF in the rat brain. Brain Res. 2007; 1179 (1): 28-34
  29. Foreman RD, Qin C, Jou CJ. Spinothalamic system and viscerosomatic motor reflexes: functional organization of cardiac and somatic input. Sci Clin Appl Man Ther E-b. Published online 2010: 111
  30. Fornari M, Carnevali L, Sgoifo A. Single osteopathic manipulative therapy session dampens acute autonomic and neuroendocrine responses to mental stress in healthy male participants. J Osteopath Med. 2017; 117 (9): 559-567
  31. Furmaga H, Carreno FR, Frazer A. Vagal nerve stimulation rapidly activates brain-derived neurotrophic factor receptor TrkB in rat brain. PLoS One. 2012; 7 (5)
  32. Furmaga H, Shah A, Frazer A. Serotonergic and noradrenergic pathways are required for the anxiolytic-like and antidepressant-like behavioural effects of repeated vagal nerve stimulation in rats. Biol Psychiatry. 2011; 70 (10): 937-945
  33. George MS, Ward Jr HE, Ninan PT et al. A pilot study of vagus nerve stimulation (VNS) for treatment-resistant anxiety disorders. Brain Stimul. 2008; 1 (2): 112-121
  34. Gerritsen RJS, Band GPH. Breath of life: the respiratory vagal stimulation model of contemplative activity. Front Hum Neurosci. 2018; 12: 397
  35. Grape C, Sandgren M, Hansson L-O et al. Does singing promote well-being?..: An empirical study of professional and amateur singers during a singing lesson. Integr Physiol Behav Sci. 2002; 38 (1): 65-74
  36. Green AL, Weaver DF. Vagal stimulation by manual carotid sinus massage to acutely suppress seizures. J Clin Neurosci. 2014; 21 (1): 179-180
  37. Grote V, Lackner H, Kelz C et al. Short-term effects of pulsed electromagnetic fields after physical exercise are dependent on autonomic tone before exposure. Eur J Appl Physiol. 2007; 101 (4): 495-502
  38. Günther-Borstel J, Schmidt T, Liem T. Heart rate variability: measurement and possible applications in osteopathy. Osteopat Medicine. 2015; 16 (3): 4-8
  39. Harinath K, Malhotra AS, Pal K et al. Autonomic nervous system and adrenal response to cold in man at Antarctica. Wilderness Environ Med. 2005; 16 (2): 81-91
  40. Hassert DL, Miyashita T, Williams CL. The effects of peripheral vagal nerve stimulation at a memory-modulating intensity on norepinephrine output in the basolateral amygdala. Behav Neurosci. 2004; 118 (1): 79
  41. Hays SA. Enhancing rehabilitative therapies with vagus nerve stimulation. Neurotherapeutics. 2016; 13 (2): 382-394
  42. Hays SA, Rennaker RL, Kilgard MP. Targeting plasticity with vagus nerve stimulation to treat neurological disease. Prog Brain Res. 2013; 207: 275-299
  43. He W, Wang X, Shi H et al. Auricular acupuncture and vagal regulation. Evidence-Based Complement Altern Med. 2012; 2012
  44. Holstege G. The periaqueductal gray controls brainstem emotional motor systems including respiration. Prog Brain Res. 2014; 209: 379-405
  45. Hulsey DR, Riley JR, Loerwald KW et al. Parametric characterization of neural activity in the locus coeruleus in response to vagus nerve stimulation. Exp Neurol. 2017; 289: 21-30
  46. Imeryüz N, Yeğen BC, Bozkurt A et al. Glucagon-like peptide-1 inhibits gastric emptying via vagal afferent-mediated central mechanisms. Am J Physiol Liver Physiol. 1997; 273 (4): G920-G927
  47. Iwasaki Y, Maejima Y, Suyama S et al. Peripheral oxytocin activates vagal afferent neurons to suppress feeding in normal and leptin-resistant mice: a route for ameliorating hyperphagia and obesity. Am J Physiol Integr Comp Physiol. 2015; 308 (5): R360-R369.
  48. Jänig W. The Integrative Action of the Autonomic Nervous System Cambridge University Press. Z Zellforsch. 2006; 110: 386-400
  49. Jänig W, Green PG. Acute inflammation in the joint: its control by the sympathetic nervous system and by neuroendocrine systems. Auton Neurosci. 2014; 182: 42-54
  50. Kalyani BG, Venkatasubramanian G, Arasappa R et al. Neurohemodynamic correlates of 'OM'chanting: A pilot functional magnetic resonance imaging study. Int J Yoga. 2011; 4 (1): 3
  51. Khasar SG, Reichling DB, Green PG et al. Fasting is a physiological stimulus of vagus-mediated enhancement of nociception in the female rat. Neuroscience. 2003; 119 (1): 215-221
  52. Klarer M, Arnold M, Günther L et al. Gut vagal afferents differentially modulate innate anxiety and learned fear. J Neurosci. 2014; 34 (21): 7067-7076
  53. Klarer M, Krieger J-P, Richetto J et al. Abdominal vagal afferents modulate the brain transcriptome and behaviors relevant to schizophrenia. J Neurosci. 2018; 38 (7): 1634-1647
  54. Knox D, George SA, Fitzpatrick CJ et al. Single prolonged stress disrupts retention of extinguished fear in rats. Learn Mem. 2012; 19 (2): 43-49
  55. Kok BE, Coffey KA, Cohn MA et al. How Positive Emotions Build Physical Health: Perceived Positive Social Connections Account for the Upward Spiral Between Positive Emotions and Vagal Tone. Psychol Sci. 2013; 24 (7): 1123-1132
  56. Kromenacker BW, Sanova AA, Marcus FI et al. Vagal mediation of low-frequency heart rate variability during slow yogic breathing. Psychosom Med. 2018; 80 (6): 581-587
  57. Lamb DG, Porges EC, Lewis GF et al. Non-invasive vagal nerve stimulation effects on hyperarousal and autonomic state in patients with posttraumatic stress disorder and history of mild traumatic brain injury: preliminary evidence. Front Med. 2017; 4: 124
  58. Li J-M, Darlak KA, Southerland L et al. VIPhyb, an antagonist of vasoactive intestinal peptide receptor, enhances cellular antiviral immunity in murine cytomegalovirus infected mice. PLoS One. 2013; 8 (5): e63381
  59. Li J-M, Hossain MS, Southerland L et al. Pharmacological inhibition of VIP signaling enhances antiviral immunity and improves survival in murine cytomegalovirus-infected allogeneic bone marrow transplant recipients. Blood, J Am Soc Hematol. 2013; 121 (12): 2347-2351.
  60. Liem T. Praxis der Kraniosakralen Osteopathie. Georg Thieme Verlag; 2003
  61. Liem T. Praxis der Kraniosakralen Osteopathie. Georg Thieme Verlag; 2019
  62. Liem T. The osteopathy self-help book. Stuttgart: Trias; 2021
  63. Liem T. Psychosomatic osteopathy. Munich: Elsevier (in print presumably 2022).
  64. Liem T, Neuhuber W. Osteopathic treatment approach to psychoemotional trauma by means of bifocal integration. J Osteopath Med. 2020; 120 (3): 180-189
  65. Liem T, Neuhuber W. Criticism of the polyvagal theory. DO-German Journal of Osteopat. 2021; 19 (02): 34-37
  66. Liu L, Lu Y, Bi X et al. Choline ameliorates cardiovascular damage by improving vagal activity and inhibiting the inflammatory response in spontaneously hypertensive rats. Sci Rep. 2017; 7 (1): 1-13
  67. Loerwald KW, Borland MS, Rennaker II RL et al. The interaction of pulse width and current intensity on the extent of cortical plasticity evoked by vagus nerve stimulation. Brain Stimul. 2018; 11 (2): 271-277
  68. Lu W-A, Chen G-Y, Kuo C-D. Foot reflexology can increase vagal modulation, decrease sympathetic modulation, and lower blood pressure in healthy subjects and patients with coronary artery disease. Altern Ther Health Med. 2011; 17 (4): 8
  69. Lu W-A, Kuo C-D. The effect of Tai Chi Chuan on the autonomic nervous modulation in older persons. Med Sci Sports Exerc. 2003; 35 (12): 1972-1976
  70. Lu W-A, Kuo C-D. Breathing frequency-independent effect of Tai Chi Chuan on autonomic modulation. Clin Auton Res. 2014; 24 (2): 47-52
  71. Mager DE, Wan R, Brown M et al. Caloric restriction and intermittent fasting alter spectral measures of heart rate and blood pressure variability in rats. FASEB J. 2006; 20 (6): 631-637
  72. Mäkinen TM, Mäntysaari M, Pääkkönen T et al. Autonomic nervous function during whole-body cold exposure before and after cold acclimation. Aviat Space Environ Med. 2008; 79 (9): 875-882
  73. Manta S, Dong J, Debonnel G et al. Optimization of vagus nerve stimulation parameters using the firing activity of serotonin neurons in the rat dorsal raphe. Eur Neuropsychopharmacol. 2009; 19 (4): 250-255
  74. Martínez-Jaimes MD, García-Lorenzana M, Munoz-Ortega MH et al. Modulation of innate immune response by the vagus nerve in experimental hepatic amebiasis in rats. Exp Parasitol. 2016; 169: 90-101
  75. Mason H, Vandoni M, Debarbieri G et al. Cardiovascular and respiratory effect of yogic slow breathing in the yoga beginner: what is the best approach? Evidence-Based Complement Altern Med. 2013; 2013
  76. McIntyre CK. Is there a role for vagus nerve stimulation in the treatment of posttraumatic stress disorder? Published online 2018
  77. Miu AC, Heilman RM, Miclea M. Reduced heart rate variability and vagal tone in anxiety: trait versus state, and the effects of autogenic training. Auton Neurosci. 2009; 145 (1-2): 99-103
  78. Naritoku DK, Terry WJ, Helfert RH. Regional induction of fos immunoreactivity in the brain by anticonvulsant stimulation of the vagus nerve. Epilepsy Res. 1995; 22 (1): 53-62
  79. Nichols JA, Nichols AR, Smirnakis SM et al. Vagus nerve stimulation modulates cortical synchrony and excitability through the activation of muscarinic receptors. Neuroscience. 2011; 189: 207-214
  80. Noble LJ, Gonzalez IJ, Meruva VB et al. Effects of vagus nerve stimulation on extinction of conditioned fear and post-traumatic stress disorder symptoms in rats. Transl Psychiatry. 2017; 7 (8): e1217-e1217
  81. O'Keefe Jr JH, Abuissa H, Sastre A et al. Effects of omega-3 fatty acids on resting heart rate, heart rate recovery after exercise, and heart rate variability in men with healed myocardial infarctions and depressed ejection fractions. Am J Cardiol. 2006; 97 (8): 1127-1130
  82. Ohinata K, Takemoto M, Kawanago M et al. Orally administered zinc increases food intake via vagal stimulation in rats. J Nutr. 2009; 139 (3): 611-616
  83. Peña DF, Engineer ND, McIntyre CK. Rapid remission of conditioned fear expression with extinction training paired with vagus nerve stimulation. Biol Psychiatry. 2013; 73 (11): 1071-1077
  84. Peña DF, Childs JE, Willett S et al. Vagus nerve stimulation enhances extinction of conditioned fear and modulates plasticity in the pathway from the ventromedial prefrontal cortex to the amygdala. Front Behav Neurosci. 2014; 8: 327
  85. Perlman SB, Camras LA, Pelphrey KA. Physiology and functioning: parents' vagal tone, emotion socialization, and children's emotion knowledge. J Exp Child Psychol. 2008; 100 (4): 308-315.
  86. Rechberger V, Biberschick M, Porthun J. Effectiveness of an osteopathic treatment on the autonomic nervous system: a systematic review of the literature. Eur J Med Res. 2019; 24 (1): 1-14
  87. Revesz D, Tjernstrom M, Ben-Menachem E et al. Effects of vagus nerve stimulation on rat hippocampal progenitor proliferation. Exp Neurol. 2008; 214 (2): 259-265
  88. Ripplinger CM. From drugs to devices and back again: chemical vagal nerve stimulation for the treatment of heart failure. Cardiovasc Res. 2017; 113 (11): 1270-1272
  89. Roberts B, Makar AE, Canaan R et al. Effect of occipitoatlantal decompression on cerebral blood flow dynamics as evaluated by Doppler ultrasonography. J Osteopath Med. 2021; 121 (2): 171-179.
  90. Roelofs K. Freeze for action: neurobiological mechanisms in animal and human freezing. Philos Trans R Soc B Biol Sci. 2017; 372 (1718): 20160206
  91. Roosevelt RW, Smith DC, Clough RW, Jensen RA, Browning RA. Increased extracellular concentrations of norepinephrine in cortex and hippocampus following vagus nerve stimulation in the rat. Brain Res. 2006 Nov 13;1119(1):124-32. 
  92. Rosas-Ballina M, Tracey KJ. The neurology of the immune system: neural reflexes regulate immunity. Neuron. 2009; 64 (1): 28-32
  93. Saper CB. The central autonomic nervous system: conscious visceral perception and autonomic pattern generation. Annu Rev Neurosci. 2002; 25 (1): 433-469
  94. Singer P, Shapiro H, Theilla M et al. Anti-inflammatory properties of omega-3 fatty acids in critical illness: novel mechanisms and an integrative perspective. Intensive Care Med. 2008; 34 (9): 1580-1592
  95. Skulas-Ray AC, Kris-Etherton PM, Harris WS et al. Effects of marine-derived omega-3 fatty acids on systemic hemodynamics at rest and during stress: a dose-response study. Ann Behav Med. 2012; 44 (3): 301-308
  96. Souza RR, Noble LJ, McIntyre CK. Using the single prolonged stress model to examine the pathophysiology of PTSD. Front Pharmacol. 2017; 8: 615
  97. Souza RR, Oleksiak CR, Tabet MN et al. Vagus nerve stimulation promotes extinction generalization across sensory modalities. Neurobiol Learn Mem. 2021; 181: 107425
  98. Souza RR, Robertson NM, Mathew E et al. Efficient parameters of vagus nerve stimulation to enhance extinction learning in an extinction-resistant rat model of PTSD. Prog Neuro-Psychopharmacology Biol Psychiatry. 2020; 99: 109848
  99. Souza RR, Robertson NM, McIntyre CK et al. Vagus nerve stimulation enhances fear extinction as an inverted-U function of stimulation intensity. Exp Neurol. 2021; 341: 113718
  100. Souza RR, Robertson NM, Pruitt DT et al. Vagus nerve stimulation reverses the extinction impairments in a model of PTSD with prolonged and repeated trauma. Stress. 2019; 22 (4): 509-520
  101. Streeter CC, Gerbarg PL, Saper RB et al. Effects of yoga on the autonomic nervous system, gamma-aminobutyric-acid, and allostasis in epilepsy, depression, and post-traumatic stress disorder. Med Hypotheses. 2012; 78 (5): 571-579
  102. Székely M. The vagus nerve in thermoregulation and energy metabolism. Auton Neurosci. 2000; 85 (1-3): 26-38
  103. Telles S, Raghavendra BR, Naveen KV et al. Changes in autonomic variables following two meditative states described in yoga texts. J Altern Complement Med. 2013; 19 (1): 35-42
  104. Vickhoff B, Malmgren H, Åström R et al. Music structure determines heart rate variability of singers. Front Psychol. 2013; 4: 334
  105. Waise TMZ, Dranse HJ, Lam TKT. The metabolic role of vagal afferent innervation. Nat Rev Gastroenterol Hepatol. 2018; 15 (10): 625-636.
  106. Walter U, Tsiberidou P. Differential age-, gender-, and side-dependency of vagus, spinal accessory, and phrenic nerve calibers detected with precise ultrasonography measures. Muscle Nerve. 2019; 59 (4): 486-491
  107. Wang Y, Kondo T, Suzukamo Y et al. Vagal nerve regulation is essential for the increase in gastric motility in response to mild exercise. Tohoku J Exp Med. 2010; 222 (2): 155-163
  108. Wei G, Li Y, Yue X et al. Tai Chi Chuan modulates heart rate variability during abdominal breathing in elderly adults. PsyCh J. 2016; 5 (1): 69-77
  109. Wischhöfer S, Jung AM. Effect of osteopathic treatment of the heart according to Torsten Liem on the autonomic nervous system in people with an increased stress level - a randomised controlled study. Thesis for the degree of Master of Science. Osteopathie Schule Deutschland, Hamburg, 2020
  110. Yang J-L, Chen G-Y, Kuo C-D. Comparison of effect of 5 recumbent positions on autonomic nervous modulation in patients with coronary artery disease. Circ J. 2008; 72 (6): 902-908
  111. Yuan P-Q, Taché Y, Miampamba M et al. Acute cold exposure induces vagally mediated Fos expression in gastric myenteric neurons in conscious rats. Am J Physiol Liver Physiol. 2001; 281 (2): G560-G568
  112. Zhu JX, Wu XY, Owyang C et al. Intestinal serotonin acts as a paracrine substance to mediate vagal signal transmission evoked by luminal factors in the rat. J Physiol. 2001; 530 (3): 431-442
  113. Lessons by Bruno Donatini at the OSD, Hamburg 2021

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