Transcutaneous Vagal Nerve Stimulation (tVNS): A new neuromodulation tool in healthy humans?

Frontiers in Psychology

Volumn 6, Issue FEB, 2015, Pages

  Van Leusden, Jelle W R ^a   Sellaro, Roberta ^a   Colzato, Lorenza S ^a  

^a LEIDEN UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Cognitive neuroscience; GABA; Neuromodulation; Norepinephrine; tVNS

Indexed keywords

EID: 84926482589     PISSN: None     EISSN: 16641078     Source Type: Journal    
DOI: 10.3389/fpsyg.2015.00102     Document Type: Note

References (38)

1. Aston-Jones, G., Shipley, M. T., Chouvet, G., Ennis, M., van Bockstaele, E., Pieribone, V., et al. (1991). Afferent regulation of locus coeruleus neurons: anatomy, physiology and pharmacology. Prog. Brain Res. 88, 47-75. doi: 10.1016/S0079-6123(08)63799-1.
2. Bartus, R. T., Dean, R. L., Beer, B., and Lippa, A. S. (1982). The cholinergic hypothesis of geriatric memory dysfunction. Science 217, 408-414. doi: 10.1126/science.7046051.
3. Bartus, R. T., Dean, R. L., Pontecorvo, M. J., and Flicker, C. (1985). The cholinergic hypothesis: a historical overview, current perspective, and future directions. Ann. N. Y. Acad. Sci. 444, 332-358.
4. Ben-Menachem, E., Hamberger, A., Hedner, T., Hammond, E. J., Uthman, B. M., Slater, J., et al. (1995). Effects of vagus nerve stimulation on amino acids and other metabolites in the CSF of patients with partial seizures. Epilepsy Res. 20, 221-227. doi: 10.1016/0920-1211(94)00083-9.
5. Berlau, D. J., and McGaugh, J. L. (2006). Enhancement of extinction memory consolidation: the role of the noradrenergic and GABAergic systems within the basolateral amygdala. Neurobiol. Learn. Mem. 86, 123-132. doi: 10.1016/j.nlm.2005.12.008.
6. Borovikova, L. V., Ivanova, S., Zhang, M., Yang, H., Botchkina, G. I., Watkins, L. R., et al. (2000). Vagus nerve stimulation attenuates the systemic inflammatory response to endotoxin. Nature 405, 458-462. doi: 10.1038/35013070.
7. Cahill, L., and McGaugh, J. L. (1998). Mechanisms of emotional arousal and lasting declarative memory. Trends Neurosci. 21, 294-299. doi: 10.1016/S0166-2236(97)01214-9.
8. Chamberlain, S. R., Müller, U., Blackwell, A. D., Robbins, T. W., and Sahakian, B. J. (2006). Noradrenergic modulation of working memory and emotional memory in humans. Psychopharmacology 188, 397-407. doi: 10.1007/s00213-006-0391-6.
9. Clark, K. B., Krahl, S. E., Smith, D. C., and Jensen, R. A. (1995). Post-training unilateral vagal nerve stimulation enhances retention performance in the rat. Neurobiol. Learn. Mem. 63, 213-216. doi: 10.1006/nlme.1995.1024.
10. Clark, K. B., Naritoku, D. K., Smith, D. C., Browning, R. A., and Jensen, R. A. (1999). Enhanced recognition memory following vagus nerve stimulation in human subjects. Nat. Neurosci. 2, 94-98. doi: 10.1038/4600.
11. Colzato, L. S., de Rover, M., van den Wildenberg, P. M., and Nieuwenhuis, S. (2013). Genetic marker of norepinephrine synthesis predicts individual differences in post-error slowing: a pilot study. Neuropsychologia 51, 2600-2604. doi: 10.1016/j.neuropsychologia.2013.07.026.
12. Danielmeier, C., and Ullsperger, M. (2011). Post-error adjustments. Front. Psychol. 2:233. doi: 10.3389/fpsyg.2011.00233.
13. Debener, S., Ullsperger, M., Siegel, M., Fiehler, K., von Cramon, D. Y., and Engel, A. K. (2005). Trial-by-trial coupling of concurrent electroencephalogram and functional magnetic resonance imaging identifies the dynamics of performance monitoring. J. Neurosci. 25, 11730-11737. doi: 10.1523/JNEUROSCI.3286-05.2005.
14. Dietrich, S., Smith, J., Scherzinger, C., Hofmann-Preiss, K., Freitag, T., Eisenkolb, A., et al. (2008). A novel transcutaneous vagus nerve stimulation leads to brain stem and cerebral activations measured by functional MRI. Biomed. Tech. 53, 104-111. doi: 10.1515/BMT.2008.022.
15. Fink, M. (1984). The origins of convulsive therapy. Am. J. Psychiatry 141, 1034-1041.
16. Gehring, W. J., and Fencsik, D. E. (2001). Functions of the medial frontal cortex in the processing of conflict and errors. J. Neurosci. 21, 9430-9437.
17. Ghacibeh, G. A., Shenker, J. I., Shenal, B., Uthman, B. M., and Heilman, K. M. (2006). The influence of vagus nerve stimulation on memory. Cogn. Behav. Neurol. 19, 119-122. doi: 10.1097/01.wnn.0000213908.34278.7d.
18. King, J. A., Korb, F. M., von Cramon, D. Y., and Ullsperger, M. (2010). Post-error behavioral adjustments are facilitated by activation and suppression of task-relevant and task-irrelevant information processing. J. Neurosci. 30, 12759-12769. doi: 10.1523/JNEUROSCI.3274-10.2010.
19. Krämer, U. M., Cunillera, T., Camara, E., Marco-Pallares, J., Cucurell, D., Nager, W., et al. (2007). The impact of catechol-O-methyltransferase and dopamine D4 receptor genotypes on neurophysiological markers of performance monitoring. J. Neurosci. 27, 14190-14198. doi: 10.1523/JNEUROSCI.4229-07.2007.
20. Kraus, T., Hösl, K., Kiess, O., Schanze, A., Kornhuber, J., and Forster, C. (2007). BOLD fMRI deactivation of limbic and temporal brain structures and mood enhancing effect by transcutaneous vagus nerve stimulation. J. Neural. Transm. 114, 1485-1493. doi: 10.1007/s00702-007-0755-z.
21. Kraus, T., Kiess, O., Hösl, K., Terekhin, P., Kornhuber, J., and Forster, C. (2013). CNS BOLD fMRI effects of sham-controlled transcutaneous electric nerve stimulation in the left outer auditory canal-a pilot study. Brain Stimul. 6, 798-804. doi: 10.1016/j.brs.2013.01.011.
22. Kreuzer, P. M., Landgrebe, M., Husser, O., Resch, M., Schecklmann, M., Geisreiter, F., et al. (2012). Transcutaneous vagus nerve stimulation: retrospective assessment of cardiac safety in a pilot study. Front. Psychiatry 3:70. doi: 10.3389/fpsyt.2012.00070.
23. MacDonald, S. W., Nyberg, L., and Bäckman, L. (2006). Intra-individual variability in behavior: links to brain structure, neurotransmission and neuronal activity. Trends Neurosci. 29, 474-480. doi: 10.1016/j.tins.2006.06.011.
24. Marrosu, F., Serra, A., Maleci, A., Puligheddu, M., Biggio, G., and Piga, M. (2003). Correlation between GABA(A) receptor density and vagus nerve stimulation in individuals with drug-resistant partial epilepsy. Epilepsy Res. 55, 59-70. doi: 10.1016/S0920-1211(03)00107-4.
25. Oei, N. Y., Tollenaar, M. S., Elzinga, B. M., and Spinhoven, P. (2010). Propranolol reduces emotional distraction in working memory: a partial mediating role of propranolol-induced cortisol increases? Neurobiol. Learn. Mem. 93, 388-395. doi: 10.1016/j.nlm.2009.12.005.
26. Peuker, E. T., and Filler, T. J. (2002). The nerve supply of the human auricle. Clin. Anat. 15, 35-37. doi: 10.1002/ca.1089.
27. Rabbitt, P. M. (1966). Errors and error correction in choice-response tasks. J. Exp. Psychol. 71, 264-272. doi: 10.1037/h0022853.
28. Raedt, R., Clinckers, R., Mollet, L., Vonck, K., El Tahry, R., Wyckhuys, T., et al. (2011). Increased hippocampus noradrenaline is a biomarker for efficacy of vagus nerve stimulation in a limbic seizure model. J. Neurochem. 117, 461-469. doi: 10.1111/j.1471-4159.2011.07214.x.
29. Roosevelt, R. W., Smith, D. C., Clough, R. W., Jensen, R. A., and Browning, R. A. (2006). Increased extracellular concentrations of norepinephrine in cortex and hippocampus following vagus nerve stimulation in the rat. Brain Res. 1119, 124-132. doi: 10.1016/j.brainres.2006.08.048.
30. Sperling, W., Reulbach, U., Bleich, S., Padberg, F., Kornhuber, J., and Mueck-Weymann, M. (2010). Cardiac effects of vagus nerve stimulation in patients with major depression. Pharmacopsychiatry 43, 7-11. doi: 10.1055/s-0029-1237374.
31. Strange, B. A., and Dolan, R. J. (2004). Beta-adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses. Proc. Natl. Acad. Sci. U.S.A. 101, 11454-11458. doi: 10.1073/pnas.0404282101.
32. Terbeck, S., Kahane, G., McTavish, S., Savulescu, J., Cowen, P. J., and Hewstone, M. (2012). Propranolol reduces implicit negative racial bias. Psychopharmacology 222, 419-424. doi: 10.1007/s00213-012-2657-5.
33. Ullsperger, M., Harsay, H. A., Wessel, J. R., and Ridderinkhof, K. R. (2010). Conscious perception of errors and its relation to the anterior insula. Brain Struct. Funct. 214, 629-643. doi: 10.1007/s00429-010-0261-1.
34. van Loon, A. M., Knapen, T., Scholte, H. S., St. John-Saaltink, E., Donner, T. H., and Lamme, V. A. (2013). GABA shapes the dynamics of bistable perception. Curr. Biol. 23, 823-827. doi: 10.1016/j.cub.2013.03.067.
35. Vonck, K., Raedt, R., Naulaerts, J., De Vogelaere, F., Thiery, E., Van Roost, E., et al. (2014). Vagus nerve stimulation... 25 years later! What do we know about the effects on cognition? Neurosci. Biobehav. Rev. 45, 63-71. doi: 10.1016/j.neubiorev.2014.05.005.
36. Watanabe, H., Shimizu, H., and Matsumoto, K. (1990). Acetylcholine release detected by trans-striatal dialysis in freely moving rats correlates with spontaneous motor activity. Life Sci. 47, 829-832. doi: 10.1016/0024-3205(90)90556-7.
37. Yerkes, R. M., and Dodson, J. D. (1908). The relation of strength of stimulus to rapidity of habit-formation. J. Comp. Neurol. 18, 459-482.
38. Yildiz, A., Quetscher, C., Dharmadhikari, S., Chmielewski, W., Glaubitz, B., Schmidt-Wilcke, T., et al. (2014). Feeling safe in the plane: neural mechanisms underlying superior action control in airplane pilot trainees-a combined EEG/MRS study. Hum. Brain Mapp. 35, 5040-5051. doi: 10.1002/hbm.22530.