Transcutaneous vagus nerve stimulation boosts associative memory in older individuals

Neurobiology of Aging

Volumn 36, Issue 5, 2015, Pages 1860-1867

  Jacobs, Heidi I L ^a,b   Riphagen, Joost M ^c   Razat, Chantalle M ^b   Wiese, Svenja ^b   Sack, Alexander T ^b  

^a MAASTRICHT UNIVERSITY   (Netherlands)

^b MAASTRICHT UNIVERSITY   (Netherlands)

^c Sankt Willibrord Spital ^*  (Germany)

Author keywords

Aging; Memory; Memory modulation; Stimulation; Vagus nerve

Indexed keywords

ADULT; ARTICLE; ASSOCIATIVE MEMORY; CONTROLLED STUDY; FACE NAME ASSOCIATION MEMORY TASK; FEMALE; HAMILTON DEPRESSION RATING SCALE; HUMAN; HUMAN EXPERIMENT; LEARNING AND MEMORY TEST; MALE; MINI MENTAL STATE EXAMINATION; NEUROMODULATION; PILOT STUDY; PRIORITY JOURNAL; RANDOMIZED CONTROLLED TRIAL; SINGLE BLIND PROCEDURE; TASK PERFORMANCE; TRANSCUTANEOUS VAGUS NERVE STIMULATION; VAGUS NERVE STIMULATION; COGNITION DISORDERS; CROSSOVER PROCEDURE; MEMORY; MIDDLE AGED; PHYSIOLOGY; PROCEDURES; TIME FACTOR; TRANSCUTANEOUS ELECTRICAL NERVE STIMULATION; VAGUS NERVE;

PLACEBO;

COGNITION DISORDERS; CROSS-OVER STUDIES; FEMALE; HUMANS; MALE; MEMORY; MIDDLE AGED; PILOT PROJECTS; PLACEBOS; SINGLE-BLIND METHOD; TIME FACTORS; TRANSCUTANEOUS ELECTRIC NERVE STIMULATION; VAGUS NERVE; VAGUS NERVE STIMULATION;

EID: 84933182667     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2015.02.023     Document Type: Article

References (58)

1. Bopp K.L., Verhaeghen P. Aging and verbal memory span: a meta-analysis. J.Gerontol. B Psychol. Sci. Soc. Sci. 2005, 60:P223-P233.
2. Busch V., Zeman F., Heckel A., Menne F., Ellrich J., Eichhammer P. The effect of transcutaneous vagus nerve stimulation on pain perception-an experimental study. Brain Stimul. 2013, 6:202-209.
3. Cahill L., McGaugh J.L. Modulation of memory storage. Curr. Opin. Neurobiol. 1996, 6:237-242.
4. Cahill L., Prins B., Weber M., McGaugh J.L. Beta-adrenergic activation and memory for emotional events. Nature 1994, 371:702-704.
5. Clark K.B., Krahl S.E., Smith D.C., Jensen R.A. Post-training unilateral vagal stimulation enhances retention performance in the rat. Neurobiol. Learn. Mem. 1995, 63:213-216.
6. Clark K.B., Naritoku D.K., Smith D.C., Browning R.A., Jensen R.A. Enhanced recognition memory following vagus nerve stimulation in human subjects. Nat. Neurosci. 1999, 2:94-98.
7. Clark K.B., Smith D.C., Hassert D.L., Browning R.A., Naritoku D.K., Jensen R.A. Posttraining electrical stimulation of vagal afferents with concomitant vagal efferent inactivation enhances memory storage processes in the rat. Neurobiol. Learn. Mem. 1998, 70:364-373.
8. DeGiorgio C.M., Schachter S.C., Handforth A., Salinsky M., Thompson J., Uthman B., Reed R., Collins S., Tecoma E., Morris G.L., Vaughn B., Naritoku D.K., Henry T., Labar D., Gilmartin R., Labiner D., Osorio I., Ristanovic R., Jones J., Murphy J., Ney G., Wheless J., Lewis P., Heck C. Prospective long-term study of vagus nerve stimulation for the treatment of refractory seizures. Epilepsia 2000, 41:1195-1200.
9. Dorr A.E., Debonnel G. Effect of vagus nerve stimulation on serotonergic and noradrenergic transmission. J.Pharmacol. Exp. Ther. 2006, 318:890-898.
10. Duffau H. Brain plasticity: from pathophysiological mechanisms to therapeutic applications. J.Clin. Neurosci. 2006, 13:885-897.
11. Duschek S., Werner N.S., Reyes Del Paso G.A. The behavioral impact of baroreflex function: a review. Psychophysiology 2013, 50:1183-1193.
12. Folstein M.F., Folstein S.E., McHugh P.R. "Mini-mental state." A practical method for grading the cognitive state of patients for the clinician. J.Psychiatr. Res. 1975, 12:189-198.
13. George M.S., Sackeim H.A., Rush A.J., Marangell L.B., Nahas Z., Husain M.M., Lisanby S., Burt T., Goldman J., Ballenger J.C. Vagus nerve stimulation: a new tool for brain research and therapy. Biol. Psychiatry 2000, 47:287-295.
14. Gliebus G., Lippa C.F. The influence of beta-blockers on delayed memory function in people with cognitive impairment. Am. J. Alzheimers Dis. Other Dement. 2007, 22:57-61.
15. Green D.M., Swets J.A. Signal Detection Theory and Biophysics 1966, Wiley, New York.
16. Groves D.A., Brown V.J. Vagal nerve stimulation: a review of its applications and potential mechanisms that mediate its clinical effects. Neurosci. Biobehav. Rev. 2005, 29:493-500.
17. Gur R.C., Ragland J.D., Moberg P.J., Turner T.H., Bilker W.B., Kohler C., Siegel S.J., Gur R.E. Computerized neurocognitive scanning: I. Methodology and validation in healthy people. Neuropsychopharmacology 2001, 25:766-776.
18. Guy S.C., Cahill L. The role of overt rehearsal in enhanced conscious memory for emotional events. Conscious Cogn. 1999, 8:114-122.
19. Hamilton M. Arating scale for depression. J.Neurol. Neurosurg. Psychiatry 1960, 23:56-62.
20. Hassert D.L., Miyashita T., Williams C.L. The effects of peripheral vagal nerve stimulation at a memory-modulating intensity on norepinephrine output in the basolateral amygdala. Behav. Neurosci. 2004, 118:79-88.
21. Hays S.A., Rennaker R.L., Kilgard M.P. Targeting plasticity with vagus nerve stimulation to treat neurological disease. Prog. Brain Res. 2013, 207:275-299.
22. Heck C., Helmers S.L., DeGiorgio C.M. Vagus nerve stimulation therapy, epilepsy, and device parameters: scientific basis and recommendations for use. Neurology 2002, 59(6 Suppl 4):S31-S37.
23. Introini-Collison I., Saghafi D., Novack G.D., McGaugh J.L. Memory-enhancing effects of post-training dipivefrin and epinephrine: involvement of peripheral and central adrenergic receptors. Brain Res. 1992, 572:81-86.
24. Jacobs H.I.L., Dillen K.N., Risius O., Göreci Y., Onur O.A., Fink G.R., Kukolja J. Consolidation in older adults depends upon competition between resting-state networks. Front. Aging Neurosci. 2014, 6:344.
25. Jacobs H.I.L., Wiese S., van de Ven V., Gronenschild E.H.B.M., Verhey F.R.J., Matthews P.M. Relevance of parahippocampal-locus coeruleus connectivity to memory in early dementia. Neurobiol. Aging 2015, 36:618-626.
26. James L.E., Fogler K.A., Tauber S.K. Recognition memory measures yield disproportionate effects of aging on learning face-name associations. Psychol. Aging 2008, 23:657-664.
27. Kraus T., Hosl K., Kiess O., Schanze A., Kornhuber J., Forster C. BOLD fMRI deactivation of limbic and temporal brain structures and mood enhancing effect by transcutaneous vagus nerve stimulation. J.Neural Transm. 2007, 114:1485-1493.
28. Kraus T., Kiess O., Hosl K., Terekhin P., Kornhuber J., Forster C. CNS BOLD fMRI effects of sham-controlled transcutaneous electrical nerve stimulation in the left outer auditory canal-a pilot study. Brain Stimul. 2013, 6:798-804.
29. Kreuzer P.M., Landgrebe M., Husser O., Resch M., Schecklmann M., Geisreiter F., Poeppl T.B., Prasser S.J., Hajak G., Langguth B. Transcutaneous vagus nerve stimulation: retrospective assessment of cardiac safety in a pilot study. Front. Psychiatry 2012, 3:70.
30. Marangell L.B., Rush A.J., George M.S., Sackeim H.A., Johnson C.R., Husain M.M., Nahas Z., Lisanby S.H. Vagus nerve stimulation (VNS) for major depressive episodes: one year outcomes. Biol. Psychiatry 2002, 51:280-287.
31. McIntyre C.K., McGaugh J.L., Williams C.L. Interacting brain systems modulate memory consolidation. Neurosci. Biobehav. Rev. 2012, 36:1750-1762.
32. Meel-van den Abeelen A.S., Lagro J., Gommer E.D., Reulen J.P., Claassen J.A. Baroreflex function is reduced in Alzheimer's disease: a candidate biomarker?. Neurobiol. Aging 2013, 34:1170-1176.
33. Merrill C.A., Jonsson M.A., Minthon L., Ejnell H., C-son Silander H., Blennow K., Karlsson M., Nordlund A., Rolstad S., Warkentin S., Ben-Menachem E., Sjogren M.J. Vagus nerve stimulation in patients with Alzheimer's disease: additional follow-up results of a pilot study through 1 year. J.Clin. Psychiatry 2006, 67:1171-1178.
34. Messer, K., Matas, J., Kittler, J., Luettin, J., Maitre, G. 1999. XM2VTSDB: the extended M2VTS database. Paper presented at the Second International Conference on Audio and Video-based Biometric Person Authentication, Washington D.C., March 1999, 72-77.
35. Miyashita T., Williams C.L. Epinephrine administration increases neural impulses propagated along the vagus nerve: role of peripheral beta-adrenergic receptors. Neurobiol. Learn. Mem. 2006, 85:116-124.
36. Nichols J.A., Nichols A.R., Smirnakis S.M., Engineer N.D., Kilgard M.P., Atzori M. Vagus nerve stimulation modulates cortical synchrony and excitability through the activation of muscarinic receptors. Neuroscience 2011, 189:207-214.
37. Nielson K.A., Jensen R.A. Beta-adrenergic receptor antagonist antihypertensive medications impair arousal-induced modulation of working memory in elderly humans. Behav. Neural Biol. 1994, 62:190-200.
38. Nielson K.A., Yee D., Erickson K.I. Memory enhancement by a semantically unrelated emotional arousal source induced after learning. Neurobiol. Learn. Mem. 2005, 84:49-56.
39. Peuker E.T., Filler T.J. The nerve supply of the human auricle. Clin. Anat. 2002, 15:35-37.
40. Polak T., Markulin F., Ehlis A.C., Langer J.B., Ringel T.M., Fallgatter A.J. Far field potentials from brain stem after transcutaneous vagus nerve stimulation: optimization of stimulation and recording parameters. J.Neural Transm. 2009, 116:1237-1242.
41. Raedt R., Clinckers R., Mollet L., Vonck K., El Tahry R., Wyckhuys T., De Herdt V., Carrette E., Wadman W., Michotte Y., Smolders I., Boon P., Meurs A. Increased hippocampal noradrenaline is a biomarker for efficacy of vagus nerve stimulation in a limbic seizure model. J.Neurochem. 2011, 117:461-469.
42. Ronnlund M., Nyberg L., Backman L., Nilsson L.G. Stability, growth, and decline in adult life span development of declarative memory: cross-sectional and longitudinal data from a population-based study. Psychol. Aging 2005, 20:3-18.
43. Roosevelt R.W., Smith D.C., Clough R.W., Jensen R.A., Browning R.A. Increased extracellular concentrations of norepinephrine in cortex and hippocampus following vagus nerve stimulation in the rat. Brain Res. 2006, 1119:124-132.
44. Roozendaal B., McGaugh J.L. Memory modulation. Behav. Neurosci. 2011, 125:797-824.
45. Sara S.J. The locus coeruleus and noradrenergic modulation of cognition. Nat. Rev. Neurosci. 2009, 10:211-223.
46. Sjogren M.J., Hellstrom P.T., Jonsson M.A., Runnerstam M., Silander H.C., Ben-Menachem E. Cognition-enhancing effect of vagus nerve stimulation in patients with Alzheimer's disease: a pilot study. J.Clin. Psychiatry 2002, 63:972-980.
47. Stanislaw H., Todorov N. Calculation of signal detection theory measures. Behav. Res. Methods Instrum. Comput. 1999, 31:137-149.
48. Stefan H., Kreiselmeyer G., Kerling F., Kurzbuch K., Rauch C., Heers M., Kasper B.S., Hammen T., Rzonsa M., Pauli E., Ellrich J., Graf W., Hopfengartner R. Transcutaneous vagus nerve stimulation (t-VNS) in pharmacoresistant epilepsies: a proof of concept trial. Epilepsia 2012, 53:e115-e118.
49. Strange B.A., Dolan R.J. Beta-adrenergic modulation of emotional memory-evoked human amygdala and hippocampal responses. Proc. Natl. Acad. Sci. U.S. A. 2004, 101:11454-11458.
50. Van der Elst W., van Boxtel M.P.J., van Breukelen G.J.P., Jolles J. Rey's verbal learning test: normative data for 1855 healthy participants aged 24-81 years and the influence of age, sex, education, and mode of presentation. J.Int. Neuropsychol. Soc. 2005, 11:290-302.
51. Van der Elst W., van Boxtel M.P.J., van Breukelen G.J.P., Jolles J. The concept shifting test: adult normative data. Psychol. Assess. 2006, 18:424-432.
52. Van der Elst W., van Boxtel M.P.J., van Breukelen G.J.P., Jolles J. The Letter Digit Substitution Test: normative data for 1,858 healthy participants aged 24-81 from the Maastricht Aging Study (MAAS): influence of age, education, and sex. J.Clin. Exp. Neuropsychol. 2006, 28:998-1009.
53. Van der Elst W., van Boxtel M.P.J., van Breukelen G.J.P., Jolles J. Normative data for the animal, profession and letter M naming verbal fluency tests for Dutch speaking participants and the effects of age, education and sex. J.Int. Neuropsychol. Soc. 2006, 12:80-89.
54. Van der Elst W., van Boxtel M.P.J., van Breukelen G.J.P., Jolles J. The Stroop Color-Word test: influence of age, sex and education; and normative data for a large sample across the adult age range. Assessment 2006, 13:62-79.
55. Vanneste S., De Ridder D. Noninvasive and invasive neuromodulation for the treatment of tinnitus: an overview. Neuromodulation 2012, 15:350-360.
56. Vonck K., De Herdt V., Bosman T., Dedeurwaerdere S., Van Laere K., Boon P. Thalamic and limbic involvement in the mechanism of action of vagus nerve stimulation, a SPECT study. Seizure 2008, 17:699-706.
57. Williams C.L., McGaugh J.L. Reversible lesions of the nucleus of the solitary tract attenuate the memory-modulating effects of posttraining epinephrine. Behav. Neurosci. 1993, 107:955-962.
58. Zuo Y., Smith D.C., Jensen R.A. Vagus nerve stimulation potentiates hippocampal LTP in freely-moving rats. Physiol. Behav. 2007, 90:583-589.