Moreover, many potential targets for treatment via tVNS have been suggested, including attention deficit hyperactivity disorder (ADHD) (Beste et al., 2016), autism spectrum disorders (Jin and Kong, 2016), Alzheimer's dementia (Jacobs et al., 2015), post-operative cognitive dysfunction (Xiong et al., 2009), increased risk of type II diabetes (Huang et al., 2014), preterm infants with oromotor dysfunction (Badran et al., 2020), chronic stroke patients (Capone et al., 2017), coronary insufficiency (Afanasiev et al., 2016) and chronic migraine (Straube et al., 2015). “Fast scan cyclic voltammetry of dopamine and serotonin in mouse brain slices,” in Electrochemical Methods for Neuroscience, eds A. C. Michael and L. M. Borland (Francis:CRC Press/Taylor). doi: 10.1016/S1003-5257(14)60022-2, Mertens, A., Raedt, R., Gadeyne, S., Carrette, E., Boon, P., and Vonck, K. (2018). Front. Noller, C. M., Levine, Y. Nat. In a more recent prospective study of 20 patients (Barbella et al., 2018), only one third derived clinical benefit from tVNS. 10, 1042–1044. Interestingly, changes in regional cerebral blood flow induced by VNS are similar to those found in depressed patients treated with selective serotonin reuptake inhibitors (fluoxetine) (Mayberg et al., 2000), either in the amygdala, hippocampus, or parahippocampus (Nemeroff et al., 2006). Mixed evidence for the potential of non-invasive transcutaneous vagal nerve stimulation to improve the extinction and retention of fear. (2018) have found that 10 Hz tVNS for 20 min periods three times per day for 6 months reduced the number of seizures, while 8 Hz stimulation leads to activation in frontal and limbic brain areas as measured by fMRI (Kraus et al., 2007). (2019). Brain Stimul. Neurology 59, 463–464. (2018) found an average seizure reduction of 64.4% in 16 out of 17 of their patients after 6 months of treatment with tVNS. 98(3 Pt 1), 455–459. Somatosensory evoked high-frequency oscillations reflecting thalamo-cortical activity are decreased in migraine patients between attacks. doi: 10.1016/S1474-4422(18)30454-X, Ben-Menachem, E., Hamberger, A., Hedner, T., Hammond, E., Uthman, B., Slater, J., et al. “Recent advances in charge balancing for functional electrical stimulation,” in Conference Proceedings: Annual International Conference of the IEEE Engineering in Medicine and Biology Society. JY, CK, TK, and PS wrote the manuscript. It is a limited-use device that is available in two models: 50 doses and 150 doses. 11, 1225–1238. J. Neural Transm. Optimization of transcutaneous vagus nerve stimulation using functional MRI. Pharmacol. Yu-tian Yu, Shao-yuan Li, Jing-jun Zhao, Man Luo, Xiao Guo and Pei-jing Rong. Initial investigations in this direction have been undertaken in Napadow et al. It attempts to slow your body down and promote relaxation and healing. Biomed. Two randomized, double-blind, sham-controlled studies doi: 10.1111/head.12647, Yuan, H., and Silberstein, S. D. (2016b). Z., Soderblom, E. J., He, X.-P., Moseley, M. A., and McNamara, J. O. Manta, S., Dong, J., Debonnel, G., and Blier, P. (2009). 12 Alongside clinical trials and intervention studies, tVNS has gained increasing interest as a tool for neuromodulation in experimental studies. Neurosci. Decision making, the P3, and the locus coeruleus-norepinephrine system. Int. J. Psychophysiol. Frequent side effects include coughing and shortness of breath. Efficacy and safety of treatment with transcutaneous vagus nerve stimulation in 17 patients with refractory epilepsy evaluated by electroencephalogram, seizure frequency, and quality of life. Anat. Nonimplantable vagus nerve stimulation or transcutaneous vagus nerve stimulation devices are designed to treat medically refractory epilepsy and depression. Relevant outcomes are symptoms, change in disease status, quality of life and functional outcomes. Individuals with epilepsy or depression may benefit from vagus nerve stimulation. doi: 10.1017/S0033291719003490. In addition to depression, tVNS has also been investigated for its use as a treatment option for drug-resistant epilepsy, a neurological disorder characterized by recurring seizures that affects around 50 million people worldwide (Beghi, 2019). doi: 10.1007/s12565-014-0231-4, Krahl, S. (2012). (2012). 190, 9–10. J. Physiol Heart Circ. Front. (2018). Clin. Rev. J. ECT 34, 283–290. [4], "Wearable" devices are being tested and developed that involve transcutaneous stimulation and do not require surgery. 12, 1349–1366. Here we will subsequently discuss issues related to safety, confounding, stimulation parameters, underlying physiology including studies on biomarkers and translational studies. Very recently, problems with the wrongful placement of electrodes in sham-stimulation, in particular the possibility to stimulate muscle zones with potential effects, have been discussed (Cakmak et al., 2017; Liugan et al., 2018). In the last half of the twentieth century, the auricular acupuncture (i.e., needling of specific areas of external auricle) became popular in clinical medicine (Nogier, 1957). 313, H354–H367. Transcutaneous vagus nerve stimulation (tVNS) enhances response selection during sequential action. In addition to NEMOS and gammaCore, which are both manufactured specifically for tVNS, stimulation can also be performed by transcutaneous electrical nerve stimulator (TENS) devices, such as TENS-200, V-TENS PLUS, or TENS-NET 2000. The nucleus ambiguus is the source of most cardiovagal motor neurons. (2019). Psychophysiology 57:e13571. doi: 10.1016/j.autneu.2016.11.003, De Ferrari, G. M., and Schwartz, P. J. Biomed. Those differences are currently not well-understood, and may relate to anatomical differences, physiological state, and stimulation parameters. Table 1. doi: 10.1016/j.brs.2015.11.003, Beghi, E. (2019). Transcutaneous vagus nerve stimulation does not affect attention to fearful faces in high worriers. (2012). Front. doi: 10.1152/ajpheart.1986.251.4.H764, Assenza, G., Campana, C., Colicchio, G., Tombini, M., Assenza, F., Di Pino, G., et al. This book provides an up to date, comprehensive, review of the common urogenital painful conditions. Biol. Handforth et al. The NEMOS® device received European certification (CE certification, which indicates legal conformity and safety, but not necessarily clinical efficacy) as a treatment for epilepsy and depression in 2010, for chronic pain in 2012 and for anxiety in 2019. Unilateral low-level transcutaneous electrical vagus nerve stimulation: a novel noninvasive treatment for myocardial infarction. (2002). 539. doi: 10.1155/2012/786839, Hein, E., Nowak, M., Kiess, O., Biermann, T., Bayerlein, K., Kornhuber, J., et al. Transcutaneous vagus nerve stimulation combined with robotic rehabilitation improves upper limb function after stroke. The justifications mentioned above are also employed to motivate the choice of stimulation parameters. 6, 812–816. Res. Vagus nerve stimulation in rodent models: an overview of technical considerations. Acta Oto Laryngol. 1119, 124–132. doi: 10.1212/WNL.57.5.885, Liu, J., Fang, J., Wang, Z., Rong, P., Hong, Y., Fan, Y., et al. No effect of transcutaneous vagus nerve stimulation on human pupil dilation: a report of three studies. Res. doi: 10.1152/ajpheart.1999.277.6.H2233, Kuo, T. B. J., Lai, C. J., Huang, Y.-T., and Yang, C. C. H. (2005). In particular, neuromodulators such as dopamine, adrenaline, noradrenaline, ATP, and serotonin can be electrochemically detected via fast-scan cyclic voltammetry or amperometry in vivo (Heien et al., 2004; John and Jones, 2007; Gourine et al., 2008; Njagi et al., 2010). These stimulators are isolated from the mains and can be connected to a computer via BNC cable to allow custom stimulation protocols to be delivered. (2019) used high resolution (e.g., 2.75 mm, and 1.2 mm isotropic resolution, respectively) and small Gaussian smoothing kernels (e.g., 2 mm), provide promising spatial precision in their methodological approach. These advantages of MEG offer a powerful tool to study connectivity between brain areas and analyze brain networks and function (Baillet, 2017). doi: 10.1016/j.brs.2019.12.018, Tekdemir, I., Aslan, A., and Elhan, A. 39, 105–110. (2017). (2018a), Fischer et al. Predominantly, these studies are characterized by short stimulation periods, addressing the immediate effects. Transcutaneous noninvasive vagus nerve stimulation (tVNS) in the treatment of schizophrenia: a bicentric randomized controlled pilot study. doi: 10.1038/sj.npp.1301082, Nesbitt, A. D., Marin, J. C. A., Tompkins, E., Ruttledge, M. H., and Goadsby, P. J. Pain Med. The left vagus nerve is stimulated rather than the right because the right plays a role in cardiac function such that stimulating it could have negative cardiac effects. (2015). Moxibust. doi: 10.1016/j.brs.2015.11.008, Ay, I., Sorensen, A. G., and Ay, H. (2011). This should show forms of improvement over that period. A practical guide to perioperative cognitive disorders, the most common complications of anesthesia and surgery in older people. Auricular transcutaneous vagus nerve stimulation improves memory persistence in naïve mice and in an intellectual disability mouse model. Transcutaneous vagus nerve stimulation modulates amygdala functional connectivity in patients with depression. Current directions in the auricular vagus nerve stimulation I–a physiological perspective. The authors found increased activation in the left LC as well as an increase in functional activation in the left thalamus (Dietrich et al., 2008). doi: 10.1111/j.1528-1157.1990.tb05852.x, Woods, A. J., Antal, A., Bikson, M., Boggio, P. S., Brunoni, A. R., Celnik, P., et al. Another theory suggests that VNS can activate inhibitory structures in the brain, with an increase in free gamma-aminobutyric acid (GABA) levels in cerebrospinal fluid and GABA-A receptor density in the hippocampus of patients who responded favorably (Marrosu et al., 2003). ELife 6:e29808. (2018). Factors that go into selecting dose, on a trial or subject basis (such as titration to sensation) are critical to report, but the actual dose applied should also be reported (Peterchev et al., 2012). The stimulation protocol differed to the study of Stefan et al. 73, 938–941. Tinnitus: characteristics, causes, mechanisms, and treatments. (2012). Johnson et al. Transcutaneous vagus nerve stimulation may attenuate postoperative cognitive dysfunction in elderly patients. Transcutaneous vagus nerve stimulation affects implicit spiritual self-representations. doi: 10.1007/s00702-003-0087-6, Fang, J., Egorova, N., and Rong, P. (2017). Differences in the neuronal pathways and neuronal sensitivity may exist and therefore affect response to tVNS (De Couck et al., 2017; Janner et al., 2018). The vagus “nerve” is actually two nerves, a left vagus and a right vagus, with slightly different neural origins and targets. Autonomic Nervous System. (2018b). Cardiovascular autonomic dysfunction in chronic kidney disease: a comprehensive review. However, further investigation suggests that these studies only elucidate the optimal stimulus intensity to induce the greatest vagus sensory evoked potential (VSEP) amplitudes (Polak et al., 2009), and that tVNS causes hypo- and hyperactivations of brain regions of interest relating to a decrease in depressive symptoms (Kraus et al., 2007). A novel transcutaneous vagus nerve stimulation leads to brainstem and cerebral activations measured by functional MRI [Funktionelle Magnetresonanztomographie zeigt Aktivierungen des Hirnstamms und weiterer zerebraler Strukturen unter transkutaner Vagusne]. Correlations between locus coeruleus (LC) neural activity, pupil diameter and behavior in monkey support a role of LC in attention. J. doi: 10.1016/j.brs.2018.07.049, Kile, B. M., Walsh, P. L., McElligott, Z. (2015). 11, 30–37. doi: 10.1177/0333102415607070, Goadsby, P., Grosberg, B., Mauskop, A., Cady, R., and Simmons, K. (2014). Especially in neuropsychiatric populations, adherence must be controlled. J. Headache Pain 16:101. doi: 10.1186/s10194-015-0582-9, Kiyokawa, J., Yamaguchi, K., Okada, R., Maehara, T., and Akita, K. (2014). 6:499. doi: 10.3389/fpsyg.2015.00499, Sellaro, R., Van Leusden, J. W. R., Tona, K.-D., Verkuil, B., Nieuwenhuis, S., and Colzato, L. S. (2015b). 14:85. doi: 10.1186/1471-2202-14-85, Heien, M. L. A. V., Johnson, M. A., and Wightman, R. M. (2004). doi: 10.1007/s11682-015-9502-5, Uthman, B. M., Wilder, B. J., Penry, J. K., Dean, C., Ramsay, R. E., Reid, S. A., et al. Notably, taVNS has been shown to decrease the frequency of action potentials in human gastric muscle cells (Hong et al., 2019; Teckentrup et al., 2020) suggesting that an electrogastrogram could be used to non-invasively track successful vagal stimulation. 2012:679345. doi: 10.1155/2012/679345, Morris, G. L., Gloss, D., Buchhalter, J., Mack, K. J., Nickels, K., and Harden, C. (2013). doi: 10.1016/j.autneu.2014.07.008, Lehtimäki, J., Hyvärinen, P., Ylikoski, M., Bergholm, M., Mäkelä, J. P., Aarnisalo, A., et al. Modulation of vagal tone enhances gastroduodenal motility and reduces somatic pain sensitivity. Zabara, J. 148, 84–92. J. Physiol. Background: Transcutaneous auricular vagus nerve stimulation (taVNS), as a noninvasive intervention, has beneficial effects on major depressive disorder based on clinical observations. It is likely that the reasons for this are multifactorial [see for a detailed discussion, (Burger et al., 2020a)]. The authors declare that the research was conducted in the absence of any commercial or financial relationships that could be construed as a potential conflict of interest. tVNS can also be associated with indirect sporadic effects, due to rare afferent-efferent vagal reflexes via the NTS. Psychiatry 9:20. doi: 10.3389/fpsyt.2018.00020, Koopman, F. A., Chavan, S. S., Miljko, S., Grazio, S., Sokolovic, S., Schuurman, P. R., et al. Nonpharmacological correction of hypersympatheticotonia in patients with chronic coronary insufficiency and severe left ventricular dysfunction. Depression Physician's Manual (2005). This book provides a comprehensive overview on Transcranial Direct Current Stimulation (tDCS) and the clinical applications of this promising technique. 13:227. doi: 10.3389/fnins.2019.00227, Keute, M., Ruhnau, P., Heinze, H. J., and Zaehle, T. (2018). Ther. Studies in rats have shown that vagal fibers originating in the right dorsal nucleus and the right ambiguous nucleus further inert the region of the syno-atrial nodule, while the fibers of the left dorsal motor nucleus and the projected ambiguous further inert into the atrioventricular nodule region (Brack et al., 2004). 11:338. doi: 10.3389/fnhum.2017.00338, Cakmak, Y. O. Neurology 87, 529–538. 3, S255–S259. Nature 524, 88–92. Therefore, we advocate caution when interpreting these results. Philadelphia, PA: Elsevier Limited. of Transcutaneous Auricular Vagus Nerve Stimulation (taVNS): Technique, Targeting, and Considerations. (2018), Yakunina et al. These are the places on the human body where there are cutaneous afferent vagus nerve distributions, and thus, as theoretically proposed by Ventureyra (2000), it is believed that direct stimulation of these nerve fibers should produce therapeutic effects similar to those of VNS. In addition, there may be variation among species in the anatomy and physiology of the vagus requiring comparisons of studies across species to be done mindfully. Psychiatry 3:70. doi: 10.3389/fpsyt.2012.00070, Kreuzer, P. M., Landgrebe, M., Resch, M., Husser, O., Schecklmann, M., Geisreiter, F., et al. (2017), they observed increased activation in the LC as well as both dorsal and median raphe nuclei and in contrast to previous studies, they implemented short duration stimulation events (1s) extended over many minutes of time (Sclocco et al., 2019).
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