#PAGE_PARAMS# #ADS_HEAD_SCRIPTS# #MICRODATA#

Influence of transcutaneous vagus nerve stimulation on cardiac vagal activity: Not different from sham stimulation and no effect of stimulation intensity


Autoři: Uirassu Borges aff001;  Sylvain Laborde aff001;  Markus Raab aff001
Působiště autorů: German Sport University Cologne, Germany aff001;  Normandie University, France aff002;  London South Bank University, England aff003
Vyšlo v časopise: PLoS ONE 14(10)
Kategorie: Research Article
prolekare.web.journal.doi_sk: https://doi.org/10.1371/journal.pone.0223848

Souhrn

The present study investigated the effects of transcutaneous vagus nerve stimulation on cardiac vagal activity, the activity of the vagus nerve regulating cardiac functioning. We applied stimulation on the left cymba conchae and tested the effects of different stimulation intensities on a vagally-mediated heart rate variability pagerameter (i.e., the root mean square of successive differences) as well as on subjective ratings of strength of perceived stimulation intensity and unpleasantness due to the stimulation. Three experiments (within-subject designs, M = 61 healthy participants each) were carried out: In Experiment 1, to choose one fixed stimulation intensity for the subsequent studies, we compared three preset stimulation intensities (i.e., 0.5, 1.0 and 1.5 mA) with each other. In Experiment 2, we compared the set stimulation method with the free stimulation method, in which the participants were instructed to freely choose an intensity. In Experiment 3, to control for placebo effects, we compared both methods (i.e., set stimulation vs. free stimulation) with their respective sham stimulations. In the three experiments, an increase of cardiac vagal activity was found from resting to the stimulation phases. However, this increase in cardiac vagal activity was not dependent on stimulation intensity (Experiment 1), the method used to stimulate (i.e., set vs. free; Experiment 2), or whether stimulation was active or sham (Experiment 3). This pattern of results was solidly supported by Bayesian estimations. On the subjective level, higher stimulation intensities were perceived as significantly stronger and a stronger stimulation was generally also perceived as more unpleasant. The results suggest that cardiac vagal activity may be similarly influenced by afferent vagal stimuli triggered by active and sham stimulation with different stimulation intensities. Potential explanations for these findings and its implications for future research with tVNS are discussed.

Klíčová slova:

Analysis of variance – Prefrontal cortex – Cognition – Sensory perception – Functional electrical stimulation – Ears – Heart rate – Time measurement


Zdroje

1. Colzato LS, Vonck K. Transcutaneous Vagus and Trigeminal Nerve Stimulation. In: Theory-Driven Approaches to Cognitive Enhancement [Internet]. Cham: Springer International Publishing; 2017 [cited 2019 Mar 24]. p. 115–26. Available from: http://link.springer.com/10.1007/978-3-319-57505-6_9

2. Redgrave J, Day D, Leung H, Laud PJ, Ali A, Lindert R, et al. Safety and tolerability of Transcutaneous Vagus Nerve stimulation in humans; a systematic review. Brain Stimulation [Internet]. 2018 Nov [cited 2019 Apr 30];11(6):1225–38. Available from: http://www.ncbi.nlm.nih.gov/pubmed/30217648 doi: 10.1016/j.brs.2018.08.010 30217648

3. Beste C, Steenbergen L, Sellaro R, Grigoriadou S, Zhang R, Chmielewski W, et al. Effects of Concomitant Stimulation of the GABAergic and Norepinephrine System on Inhibitory Control–A Study Using Transcutaneous Vagus Nerve Stimulation. Brain Stimulation. 2016 Nov;9(6):811–8. doi: 10.1016/j.brs.2016.07.004 27522167

4. Burger AM, Verkuil B, Fenlon H, Thijs L, Cools L, Miller HC, et al. Mixed evidence for the potential of non-invasive transcutaneous vagal nerve stimulation to improve the extinction and retention of fear. Behaviour Research and Therapy. 2017 Oct;97:64–74. doi: 10.1016/j.brat.2017.07.005 28719827

5. Antonino D, Teixeira A, Maia-lopes PM, Souza MC, Sabino-Carvalho JL, Murray AR, et al. Non-invasive vagus nerve stimulation acutely improves spontaneous cardiac barore fl ex sensitivity in healthy young men: A randomized placebo-controlled trial. 2017;1–7.

6. Badran BW, Mithoefer OJ, Summer CE, LaBate NT, Glusman CE, Badran AW, et al. Short trains of transcutaneous auricular vagus nerve stimulation (taVNS) have parameter-specific effects on heart rate. Brain Stimulation. 2018 Jul;11(4):699–708. doi: 10.1016/j.brs.2018.04.004 29716843

7. Peuker ET, Filler TJ. The nerve supply of the human auricle. Clinical Anatomy. 2002 Jan;15(1):35–7. doi: 10.1002/ca.1089 11835542

8. Foote SL, Bloom FE, Aston-Jones G. Nucleus locus ceruleus: new evidence of anatomical and physiological specificity. Physiological Reviews [Internet]. 1983 Jul [cited 2019 May 3];63(3):844–914. Available from: http://www.ncbi.nlm.nih.gov/pubmed/6308694 doi: 10.1152/physrev.1983.63.3.844 6308694

9. Aihara M, Ida I, Yuuki N, Oshima A, Kumano H, Takahashi K, et al. HPA axis dysfunction in unmedicated major depressive disorder and its normalization by pharmacotherapy correlates with alteration of neural activity in prefrontal cortex and limbic/paralimbic regions. Psychiatry Research: Neuroimaging [Internet]. 2007 Aug 15 [cited 2019 Mar 24];155(3):245–56. Available from: http://www.ncbi.nlm.nih.gov/pubmed/17587554 doi: 10.1016/j.pscychresns.2006.11.002 17587554

10. Thayer JF, Ph D, Hansen AL, Ph D, Saus-rose E, Psychol C, et al. Heart Rate Variability, Prefrontal Neural Function, and Cognitive Performance: The Neurovisceral Integration Perspective on Self-regulation, Adaptation, and Health. 2009;141–53.

11. Thayer JF, Ph D, Hansen AL, Ph D, Saus-rose E, Psychol C, et al. Heart Rate Variability, Prefrontal Neural Function, and Cognitive Performance: The Neurovisceral Integration Perspective on Self-regulation, Adaptation, and Health. 2009;141–53.

12. Malik M, Camm AJ, Bigger JT, Breithart G, Cerutti S, Cohen R. 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. Circulation. 1996 Mar;93(5):1043–65. 8598068

13. Murray AR, Atkinson L, Mahadi MK, Deuchars SA, Deuchars J. The strange case of the ear and the heart: The auricular vagus nerve and its influence on cardiac control. Autonomic Neuroscience: Basic and Clinical [Internet]. 2016;199:48–53. Available from: https://doi.org/10.1016/j.autneu.2016.06.004

14. van Leusden JWR Van, Sellaro R, Colzato LS. Transcutaneous Vagal Nerve Stimulation (tVNS): a new neuromodulation tool in healthy humans? 2015;6(February):2013–6.

15. Kreuzer PM, Landgrebe M, Husser O, Resch M, Schecklmann M, Geisreiter F, et al. Transcutaneous vagus nerve stimulation: retrospective assessment of cardiac safety in a pilot study. 2012;3(August):1–7.

16. Yakunina N, Kim SS. Optimization of Transcutaneous Vagus Nerve Stimulation Using Functional MRI. 2016;2016.

17. Fischer R, Ventura-Bort C, Hamm A, Weymar M. Transcutaneous vagus nerve stimulation (tVNS) enhances conflict-triggered adjustment of cognitive control. Cognitive, Affective, & Behavioral Neuroscience. 2018 Aug;18(4):680–93.

18. Ventura-Bort C, Wirkner J, Genheimer H, Wendt J, Hamm AO, Weymar M. Effects of Transcutaneous Vagus Nerve Stimulation (tVNS) on the P300 and Alpha-Amylase Level: A Pilot Study. Frontiers in Human Neuroscience. 2018 Jun;12:202. doi: 10.3389/fnhum.2018.00202 29977196

19. Sellaro R, Leusden JWR Van, Tona K, Verkuil B, Nieuwenhuis S, Colzato LS. Transcutaneous Vagus Nerve Stimulation Enhances Post-error Slowing. 2014;2126–32.

20. Colzato LS, Ritter SM, Steenbergen L. Transcutaneous vagus nerve stimulation (tVNS) enhances divergent thinking. Neuropsychologia. 2018 Mar;111:72–6. doi: 10.1016/j.neuropsychologia.2018.01.003 29326067

21. Nemeroff CB, Mayberg HS, Krahl SE, Mcnamara J, Frazer A, Henry TR, et al. VNS Therapy in Treatment-Resistant Depression: Clinical Evidence and Putative Neurobiological Mechanisms. 2006;1345–55.

22. Badran BW, Dowdle LT, Mithoefer OJ, Labate NT, Brown JC, Devries WH, et al. Neurophysiologic effects of transcutaneous auricular vagus nerve stimulation (taVNS) via electrical stimulation of the tragus: A concurrent taVNS/fMRI study and review. Brain Stimulation [Internet]. 2018;11(3):492–500. Available from: https://doi.org/10.1016/j.brs.2017.12.009 29361441

23. Dietrich S, Smith J, Scherzinger C, Hofmann-Preiß K, Freitag T, Eisenkolb A, et al. A novel transcutaneous vagus nerve stimulation leads to brainstem and cerebral activations measured by functional MRI. Biomedizinische Technik/Biomedical Engineering [Internet]. 2008 Jan 1 [cited 2019 Apr 30];53(3):104–11. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18601618 doi: 10.1515/BMT.2008.022 18601618

24. Frangos E, Ellrich J, Komisaruk BR. Brain Stimulation Non-invasive Access to the Vagus Nerve Central Projections via Electrical Stimulation of the External Ear: fMRI Evidence in Humans. Brain Stimulation [Internet]. 2015;8(3):624–36. Available from: https://doi.org/10.1016/j.brs.2014.11.018 25573069

25. Kraus T, Kiess O, Hösl K, Terekhin P, Kornhuber J, Forster C. Brain Stimulation CNS BOLD fMRI Effects of Sham-Controlled Transcutaneous Electrical Nerve Stimulation in the Left Outer Auditory Canal e A Pilot Study. 2013;6:798–804.

26. Clancy JA, Mary DA, Witte KK, Greenwood JP, Deuchars SA, Deuchars J. Non-invasive Vagus Nerve Stimulation in Healthy Humans Reduces Sympathetic Nerve Activity. Brain Stimulation. 2014 Nov;7(6):871–7. doi: 10.1016/j.brs.2014.07.031 25164906

27. Couck M De, Cserjesi R, Caers R, Zijlstra WP, Widjaja D, Wolf N, et al. Basic and Clinical Effects of short and prolonged transcutaneous vagus nerve stimulation on heart rate variability in healthy subjects. Autonomic Neuroscience: Basic and Clinical [Internet]. 2017;203:88–96. Available from: https://doi.org/10.1016/j.autneu.2016.11.003

28. Burger AM, Does W Van Der, Thayer JF, Brosschot JF, Verkuil B. Transcutaneous vagus nerve stimulation reduces spontaneous but not induced negative thought intrusions in high worriers. Biological Psychology [Internet]. 2019;142(January):80–9. Available from: https://doi.org/10.1016/j.biopsycho.2019.01.014

29. Burger AM, Verkuil B, Van Diest I, Van der Does W, Thayer JF, Brosschot JF. The effects of transcutaneous vagus nerve stimulation on conditioned fear extinction in humans. Neurobiology of Learning and Memory [Internet]. 2016 Jul [cited 2019 May 3];132:49–56. Available from: http://www.ncbi.nlm.nih.gov/pubmed/27222436 doi: 10.1016/j.nlm.2016.05.007 27222436

30. Heathers JAJ. Sympathovagal balance from heart rate variability: an obituary. Experimental Physiology [Internet]. 2012 Apr [cited 2019 Apr 30];97(4):556–556. Available from: http://www.ncbi.nlm.nih.gov/pubmed/22525665 doi: 10.1113/expphysiol.2011.063867 22525665

31. Peltola MA. Role of editing of R–R intervals in the analysis of heart rate variability. Frontiers in Physiology. 2012 May;3:148. doi: 10.3389/fphys.2012.00148 22654764

32. Berntson GG, Cacioppo JT, Quigley KS. Respiratory sinus arrhythmia: autonomic origins, physiological mechanisms, and psychophysiological implications. Psychophysiology [Internet]. 1993 Mar [cited 2019 Aug 7];30(2):183–96. Available from: http://www.ncbi.nlm.nih.gov/pubmed/8434081

33. Laborde S, Mosley E, Thayer JF. Heart Rate Variability and Cardiac Vagal Tone in Psychophysiological Research–Recommendations for Experiment Planning, Data Analysis, and Data Reporting. Frontiers in Psychology. 2017 Feb;08:213.

34. Steenbergen L, Sellaro R, Stock A-K, Verkuil B, Beste C, Colzato LS. Transcutaneous vagus nerve stimulation (tVNS) enhances response selection during action cascading processes. European Neuropsychopharmacology. 2015 Jun;25(6):773–8. doi: 10.1016/j.euroneuro.2015.03.015 25869158

35. Busch V, Zeman F, Heckel A, Menne F, Ellrich J, Eichhammer P. Brain Stimulation The effect of transcutaneous vagus nerve stimulation on pain perception e An experimental study. Brain Stimulation [Internet]. 2013;6(2):202–9. Available from: https://doi.org/10.1016/j.brs.2012.04.006 22621941

36. Yerkes RM, Dodson JD. The relation of strength of stimulus to rapidity of habit-formation. Journal of Comparative Neurology and Psychology [Internet]. 1908 Nov 1 [cited 2019 Apr 30];18(5):459–82. Available from: http://doi.wiley.com/10.1002/cne.920180503

37. Liu W, Lian Z, Liu Y. Heart rate variability at different thermal comfort levels. European Journal of Applied Physiology [Internet]. 2008 Jun 20 [cited 2019 May 5];103(3):361–6. Available from: http://www.ncbi.nlm.nih.gov/pubmed/18351379 doi: 10.1007/s00421-008-0718-6 18351379

38. Clark KB, Naritoku DK, Smith DC, Browning RA, Jensen RA. Enhanced recognition memory following vagus nerve stimulation in human subjects. 1999;2(1).

39. Loerwald KW, Borland MS, Rennaker RL, Hays SA, Kilgard MP. The interaction of pulse width and current intensity on the extent of cortical plasticity evoked by vagus nerve stimulation. Brain Stimulation [Internet]. 2018 Mar 1 [cited 2019 Apr 11];11(2):271–7. Available from: https://www.sciencedirect.com/science/article/pii/S1935861X17309634?via%3Dihub

40. Quintana DS, Heathers JAJ. Considerations in the assessment of heart rate variability in biobehavioral research. 2014;5(July):1–10.

41. Faul F, Erdfelder E, Lang A-G, Buchner A. G*Power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods [Internet]. 2007 May [cited 2019 Mar 25];39(2):175–91. Available from: http://www.springerlink.com/index/10.3758/BF03193146 17695343

42. Wagenmakers E-J. A practical solution to the pervasive problems of p values. Psychonomic Bulletin & Review [Internet]. 2007 Oct [cited 2019 Apr 30];14(5):779–804. Available from: http://www.springerlink.com/index/10.3758/BF03194105

43. Wetzels R, Matzke D, Lee MD, Rouder JN, Iverson GJ, Wagenmakers E. Statistical Evidence in Experimental Psychology: An Empirical Comparison Using 855 t Tests. 2011; Available from: https://doi.org/10.1177/1745691611406923

44. Berntson GG. Respiratory sinus arrhythmia: Autonomic origins physiological mechanisms and psychophysiological implications.

45. Burger AM, Van Diest I, Van der Does W, Korbee JN, Waziri N, Brosschot JF, et al. The effect of transcutaneous vagus nerve stimulation on fear generalization and subsequent fear extinction. Neurobiology of Learning and Memory [Internet]. 2019 May 12 [cited 2019 May 3];161:192–201. Available from: http://www.ncbi.nlm.nih.gov/pubmed/30986531 doi: 10.1016/j.nlm.2019.04.006 30986531

46. Albusoda A, Farmer AD, Aziz Q. What drives the hypoalgesic effect of neurostimulation? The Lancet Gastroenterology and Hepatology [Internet]. 2018;3(1):13. Available from: https://doi.org/10.1016/S2468-1253(17)30364-3 29254614

47. Rangon C-M. Reconsidering Sham in Transcutaneous Vagus Nerve Stimulation studies. Clinical Neurophysiology [Internet]. 2018 Nov [cited 2019 Apr 30];129(11):2501–2. Available from: https://linkinghub.elsevier.com/retrieve/pii/S1388245718312264 doi: 10.1016/j.clinph.2018.08.027 30268709

48. Yakunina N, Kim SS, Nam E-C. Optimization of Transcutaneous Vagus Nerve Stimulation Using Functional MRI. Neuromodulation: Technology at the Neural Interface. 2017 Apr;20(3):290–300.

49. Thayer JF, Lane RD. Neuroscience and Biobehavioral Reviews Claude Bernard and the heart–brain connection: Further elaboration of a model of neurovisceral integration. 2009;33:81–8.

50. Doheny EP, Caulfield BM, Minogue CM, Lowery MM. The effect of subcutaneous fat thickness on the efficacy of transcutaneous electrical stimulation. In: 2008 30th Annual International Conference of the IEEE Engineering in Medicine and Biology Society [Internet]. IEEE; 2008 [cited 2019 Apr 30]. p. 5684–7. Available from: http://ieeexplore.ieee.org/document/4650504/

51. Keller T, Kuhn A. Skin properties and the influence on electrode design for transcutaneous (surface) electrical stimulation. In Springer, Berlin, Heidelberg; 2009 [cited 2019 Apr 30]. p. 492–5. Available from: http://link.springer.com/10.1007/978-3-642-03889-1_131

52. Kemp J, Després O, Pebayle T, Dufour A. Clinical Neurophysiology Age-related decrease in sensitivity to electrical stimulation is unrelated to skin conductance: An evoked potentials study. Clinical Neurophysiology [Internet]. 2014;125(3):602–7. Available from: https://doi.org/10.1016/j.clinph.2013.08.020

53. 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 Research [Internet]. 2006 Nov [cited 2019 Apr 30];1119(1):124–32. Available from: https://linkinghub.elsevier.com/retrieve/pii/S0006899306024474 doi: 10.1016/j.brainres.2006.08.04 16962076

54. Warren CM, Tona KD, Ouwerkerk L, Paridon J Van, Poletiek F, Bosch JA, et al. The neuromodulatory and hormonal effects of transcutaneous vagus nerve stimulation as evidenced by salivary alpha amylase, salivary cortisol, pupil diameter, and the P3 event-related potential. Brain Stimulation [Internet]. 2018; Available from: https://doi.org/10.1016/j.brs.2018.12.224

55. Keute M, Demirezen M, Graf A, Mueller NG, Zaehle T. No modulation of pupil size and event-related pupil response by transcutaneous auricular vagus nerve stimulation (taVNS). Scientific Reports. 2019 Dec;9(1):11452. doi: 10.1038/s41598-019-47961-4 31391505

56. Joshi S, Li Y, Kalwani RM, Gold JI. Relationships between Pupil Diameter and Neuronal Activity in the Locus Coeruleus, Colliculi, and Cingulate Cortex. Neuron [Internet]. 2016 Jan 6 [cited 2019 Apr 9];89(1):221–34. Available from: http://www.ncbi.nlm.nih.gov/pubmed/26711118 doi: 10.1016/j.neuron.2015.11.028 26711118

57. Larkin WD, Reilly JP, Kittler LB. Individual Differences in Sensitivity to Transient Electrocutaneous Stimulation. 1986;(5):495–504.

58. Lehrer PM, Gevirtz R, Medical DVA. Heart rate variability biofeedback: how and why does it work? 2014;5(July):1–9.


Článok vyšiel v časopise

PLOS One


2019 Číslo 10
Najčítanejšie tento týždeň
Najčítanejšie v tomto čísle
Kurzy

Zvýšte si kvalifikáciu online z pohodlia domova

Aktuální možnosti diagnostiky a léčby litiáz
nový kurz
Autori: MUDr. Tomáš Ürge, PhD.

Všetky kurzy
Prihlásenie
Zabudnuté heslo

Zadajte e-mailovú adresu, s ktorou ste vytvárali účet. Budú Vám na ňu zasielané informácie k nastaveniu nového hesla.

Prihlásenie

Nemáte účet?  Registrujte sa

#ADS_BOTTOM_SCRIPTS#