The effects of bifrontal anodal transcranial direct current stimulation (tDCS) on sleepiness and vigilance in partially sleep-deprived subjects: A multidimensional study.
diurnal sleepiness
neurobehavioural performance
sleep deprivation
sleepiness
transcranial electrical stimulation
Journal
Journal of sleep research
ISSN: 1365-2869
Titre abrégé: J Sleep Res
Pays: England
ID NLM: 9214441
Informations de publication
Date de publication:
08 2023
08 2023
Historique:
revised:
21
02
2023
received:
16
12
2022
accepted:
21
02
2023
medline:
17
7
2023
pubmed:
6
3
2023
entrez:
5
3
2023
Statut:
ppublish
Résumé
In recent years, transcranial electrical stimulation techniques have demonstrated their ability to modulate our levels of sleepiness and vigilance. However, the outcomes differ among the specific aspects considered (physiological, behavioural or subjective). This study aimed to observe the effects of bifrontal anodal transcranial direct current stimulation. Specifically, we tested the ability of this stimulation protocol to reduce sleepiness and increase vigilance in partially sleep-deprived healthy participants. Twenty-three subjects underwent a within-subject sham-controlled stimulation protocol. We compared sleepiness and vigilance levels before and after the two stimulation conditions (active versus sham) by using behavioural (reaction-time task), subjective (self-report scales) and physiological (sleep-onset latency and electroencephalogram power [n = 20] during the Maintenance of Wakefulness Test) measures. We showed the efficacy of the active stimulation in reducing physiological sleepiness and preventing vigilance drop compared with the sham stimulation. Consistently, we observed a reduction of perceived sleepiness following the active stimulation for both self-report scales. However, the stimulation effect on subjective measures was not statistically significant probably due to the underpowered sample size for these measures, and to the possible influence of motivational and environmental factors. Our findings confirm the ability of this technique to influence vigilance and sleepiness, pointing out the potential for new treatment developments based on transcranial electrical stimulation.
Types de publication
Clinical Trial
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
e13869Commentaires et corrections
Type : CommentIn
Informations de copyright
© 2023 The Authors. Journal of Sleep Research published by John Wiley & Sons Ltd on behalf of European Sleep Research Society.
Références
Agboada, D., Mosayebi-Samani, M., Kuo, M.-F., & Nitsche, M. A. (2020). Induction of long-term potentiation-like plasticity in the primary motor cortex with repeated anodal transcranial direct current stimulation-better effects with intensified protocols? Brain Stimulation, 13(4), 987-997.
Åkerstedt, T., & Gillberg, M. (1990). Subjective and objective sleepiness in the active individual. International Journal of Neuroscience, 52(1-2), 29-37.
Annarumma, L., D'Atri, A., Alfonsi, V., & De Gennaro, L. (2018). The efficacy of transcranial current stimulation techniques to modulate resting-state EEG, to affect vigilance and to promote sleepiness. Brain Sciences, 8(7), 137.
Benjamini, Y., & Yekutieli, D. (2001). The control of the false discovery rate in multiple testing under dependency. The Annals of Statistics, 29(4), 1165-1188.
Bermudez, E. B., Klerman, E. B., Czeisler, C. A., Cohen, D. A., Wyatt, J. K., & Phillips, A. J. K. (2016). Prediction of vigilant attention and cognitive performance using self-reported alertness, circadian phase, hours since awakening, and accumulated sleep loss. PLoS One, 11(3), e0151770.
Bernardi, G., Siclari, F., Yu, X., Zennig, C., Bellesi, M., Ricciardi, E., Cirelli, C., Ghilardi, M. F., Pietrini, P., & Tononi, G. (2015). Neural and behavioral correlates of extended training during sleep deprivation in humans: Evidence for local, task-specific effects. Journal of Neuroscience, 35(11), 4487-4500.
Borbély, A. A. (1982). A two process model of sleep regulation. Human Neurobiology, 1(3), 195-204.
Borbély, A. A., Baumann, F., Brandeis, D., Strauch, I., & Lehmann, D. (1981). Sleep deprivation: Effect on sleep stages and EEG power density in man. Electroencephalography and Clinical Neurophysiology, 51(5), 483-493.
Brunyé, T. T., Hussey, E. K., Fontes, E. B., & Ward, N. (2019). Modulating applied task performance via transcranial electrical stimulation. Frontiers in Human Neuroscience, 13, 140.
Cheng, J.-X., Zhao, X., Qiu, J., Jiang, Y., Ren, J., Sun, S., Wang, R., & Su, C. (2021). Effects of transcranial direct current stimulation on performance and recovery sleep during acute sleep deprivation: A pilot study. Sleep Medicine, 79, 124-133.
Cluydts, R., De Valck, E., Verstraeten, E., & Theys, P. (2002). Daytime sleepiness and its evaluation. Sleep Medicine Reviews, 6(2), 83-96.
Dalong, G., Jiyuan, L., Ying, Z., Lei, Z., Yanhong, H., & Yongcong, S. (2020). Transcranial direct current stimulation reconstructs diminished thalamocortical connectivity during prolonged resting wakefulness: A resting-state fMRI pilot study. Brain Imaging and Behavior, 14(1), 278-288.
D'Atri, A., De Simoni, E., Gorgoni, M., Ferrara, M., Ferlazzo, F., Rossini, P. M., & De Gennaro, L. (2015). Frequency-dependent effects of oscillatory-tDCS on EEG oscillations: A study with better OSCillation detection method (BOSC). Archives Italiennes de Biologie, 153(2-3), 124-134.
D'Atri, A., De Simoni, E., Gorgoni, M., Ferrara, M., Ferlazzo, F., Rossini, P. M., & De Gennaro, L. (2016). Electrical stimulation of the frontal cortex enhances slow-frequency EEG activity and sleepiness. Neuroscience, 324, 119-130.
D'Atri, A., Romano, C., Gorgoni, M., Scarpelli, S., Alfonsi, V., Ferrara, M., Ferlazzo, F., Rossini, P. M., & De Gennaro, L. (2017). Bilateral 5 Hz transcranial alternating current stimulation on fronto-temporal areas modulates resting-state EEG. Scientific Reports, 7(1), 15672.
D'Atri, A., Scarpelli, S., Gorgoni, M., Alfonsi, V., Annarumma, L., Giannini, A. M., Ferrara, M., Ferlazzo, F., Rossini, P. M., & De Gennaro, L. (2019). Bilateral theta transcranial alternating current stimulation (tACS) modulates EEG activity: When tACS works awake it also works asleep. Nature and Science of Sleep, 11, 343-356.
De Gennaro, L., Marzano, C., Veniero, D., Moroni, F., Fratello, F., Curcio, G., Ferrara, M., Ferlazzo, F., Novelli, L., & Pellicciari, M. C. (2007). Neurophysiological correlates of sleepiness: A combined TMS and EEG study. NeuroImage, 36(4), 1277-1287.
De Valck, E., & Cluydts, R. (2003). Sleepiness as a state-trait phenomenon, comprising both a sleep drive and a wake drive. Medical Hypotheses, 60(4), 509-512.
Faul, F., Erdfelder, E., Lang, A. G., & Buchner, A. (2007). G* power 3: A flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behavior Research Methods, 39(2), 175-191.
Fertonani, A., & Miniussi, C. (2017). Transcranial electrical stimulation: What we know and do not know about mechanisms. The Neuroscientist, 23(2), 109-123.
Finelli, L. A., Baumann, H., Borbély, A. A., & Achermann, P. (2000). Dual electroencephalogram markers of human sleep homeostasis: Correlation between theta activity in waking and slow-wave activity in sleep. Neuroscience, 101(3), 523-529.
Frase, L., Maier, J. G., Zittel, S., Freyer, T., Riemann, D., Normann, C., Feige, B., Nitsche, M. A., & Nissen, C. (2015). Bifrontal anodal transcranial direct current stimulation (tDCS) improves daytime vigilance and sleepiness in a patient with organic hypersomnia following reanimation. Brain Stimulation: Basic, Translational, and Clinical Research in Neuromodulation, 8(4), 844-846.
Frase, L., Piosczyk, H., Zittel, S., Jahn, F., Selhausen, P., Krone, L., Feige, B., Mainberger, F., Maier, J. G., & Kuhn, M. (2016). Modulation of total sleep time by transcranial direct current stimulation (tDCS). Neuropsychopharmacology, 41(10), 2577-2586.
Frase, L., Selhausen, P., Krone, L., Tsodor, S., Jahn, F., Feige, B., Maier, J. G., Mainberger, F., Piosczyk, H., & Kuhn, M. (2019). Differential effects of bifrontal tDCS on arousal and sleep duration in insomnia patients and healthy controls. Brain Stimulation, 12(3), 674-683.
Galbiati, A., Abutalebi, J., Iannaccone, S., Borsa, V. M., Musteata, S., Zucconi, M., Giora, E., & Ferini-Strambi, L. (2016). The effects of transcranial direct current stimulation (tDCS) on idiopathic hypersomnia: A pilot study. Archives Italiennes de Biologie, 154(1), 1-5.
Gorgoni, M., Bartolacci, C., D'Atri, A., Scarpelli, S., Marzano, C., Moroni, F., Ferrara, M., & De Gennaro, L. (2019). The spatiotemporal pattern of the human electroencephalogram at sleep onset after a period of prolonged wakefulness. Frontiers in Neuroscience, 13, 1-15.
Gorgoni, M., D'Atri, A., Scarpelli, S., Ferrara, M., & De Gennaro, L. (2020). The electroencephalographic features of the sleep onset process and their experimental manipulation with sleep deprivation and transcranial electrical stimulation protocols. Neuroscience & Biobehavioral Reviews, 114, 25-37.
Gorgoni, M., Ferlazzo, F., Ferrara, M., Moroni, F., D'Atri, A., Fanelli, S., Torriglia, I. G., Lauri, G., Marzano, C., & Rossini, P. M. (2014). Topographic electroencephalogram changes associated with psychomotor vigilance task performance after sleep deprivation. Sleep Medicine, 15(9), 1132-1139.
Guerrero, A. F., & Achermann, P. (2019). Brain dynamics during the sleep onset transition: An EEG source localization study. Neurobiology of Sleep and Circadian Rhythms, 6, 24-34.
Horne, J. (2010). Sleepiness as a need for sleep: When is enough, enough? Neuroscience & Biobehavioral Reviews, 34(1), 108-118.
Johns, M. W. (2002). Sleep propensity varies with behaviour and the situation in which it is measured: The concept of somnificity. Journal of Sleep Research, 11(1), 61-67.
Khitrov, M. Y., Laxminarayan, S., Thorsley, D., Ramakrishnan, S., Rajaraman, S., Wesensten, N. J., & Reifman, J. (2014). PC-PVT: A platform for psychomotor vigilance task testing, analysis, and prediction. Behavior Research Methods, 46(1), 140-147.
Kim, H., & Young, T. (2005). Subjective daytime sleepiness: Dimensions and correlates in the general population. Sleep, 28(5), 625-634.
Kirov, R., Weiss, C., Siebner, H. R., Born, J., & Marshall, L. (2009). Slow oscillation electrical brain stimulation during waking promotes EEG theta activity and memory encoding. Proceedings of the National Academy of Sciences, 106(36), 15460-15465.
Krone, L., Frase, L., Piosczyk, H., Selhausen, P., Zittel, S., Jahn, F., Kuhn, M., Feige, B., Mainberger, F., Klöppel, S., & Riemann, D. (2017). Top-down control of arousal and sleep: Fundamentals and clinical implications. Sleep Medicine Reviews, 31, 17-24.
Langner, R., & Eickhoff, S. B. (2013). Sustaining attention to simple tasks: A meta-analytic review of the neural mechanisms of vigilant attention. Psychological Bulletin, 139(4), 870-900.
Littner, M. R., Kushida, C., Wise, M., Davila, G., Morgenthaler, T., Lee-Chiong, T., Hirshkowitz, M., Loube, D. L., Bailey, D., & Berry, R. B. (2005). Practice parameters for clinical use of the multiple sleep latency test and the maintenance of wakefulness test. Sleep, 28(1), 113-121.
Luna, F. G., Román-Caballero, R., Barttfeld, P., Lupiáñez, J., & Martín-Arévalo, E. (2020). A high-definition tDCS and EEG study on attention and vigilance: Brain stimulation mitigates the executive but not the arousal vigilance decrement. Neuropsychologia, 142, 107447.
Magnin, M., Rey, M., Bastuji, H., Guillemant, P., Mauguière, F., & Garcia-Larrea, L. (2010). Thalamic deactivation at sleep onset precedes that of the cerebral cortex in humans. Proceedings of the National Academy of Sciences, 107(8), 3829-3833.
Marzano, C., Moroni, F., Gorgoni, M., Nobili, L., Ferrara, M., & De Gennaro, L. (2013). How we fall asleep: Regional and temporal differences in electroencephalographic synchronization at sleep onset. Sleep Medicine, 14(11), 1112-1122.
McIntire, L. K., McKinley, R. A., Goodyear, C., & Nelson, J. (2014). A comparison of the effects of transcranial direct current stimulation and caffeine on vigilance and cognitive performance during extended wakefulness. Brain Stimulation, 7(4), 499-507.
Merker, B. (2013). Cortical gamma oscillations: The functional key is activation, not cognition. Neuroscience & Biobehavioral Reviews, 37(3), 401-417.
Monk, T. H. (1989). A visual analogue scale technique to measure global vigor and affect. Psychiatry Research, 27(1), 89-99.
Monte-Silva, K., Kuo, M.-F., Hessenthaler, S., Fresnoza, S., Liebetanz, D., Paulus, W., & Nitsche, M. A. (2013). Induction of late LTP-like plasticity in the human motor cortex by repeated non-invasive brain stimulation. Brain Stimulation, 6(3), 424-432.
Nelson, J. T., McKinley, R. A., Golob, E. J., Warm, J. S., & Parasuraman, R. (2014). Enhancing vigilance in operators with prefrontal cortex transcranial direct current stimulation (tDCS). NeuroImage, 85, 909-917.
Nir, Y., Andrillon, T., Marmelshtein, A., Suthana, N., Cirelli, C., Tononi, G., & Fried, I. (2017). Selective neuronal lapses precede human cognitive lapses following sleep deprivation. Nature Medicine, 23(12), 1474-1480.
Parasuraman, R., & Davies, D. R. (1977). A taxonomic analysis of vigilance performance. In vigilance (pp. 559-574). Springer.
Reifman, J., Kumar, K., Khitrov, M. Y., Liu, J., & Ramakrishnan, S. (2018). PC-PVT 2.0: An updated platform for psychomotor vigilance task testing, analysis, prediction, and visualization. Journal of Neuroscience Methods, 304, 39-45.
Sarasso, S., Proserpio, P., Pigorini, A., Moroni, F., Ferrara, M., De Gennaro, L., De Carli, F., Russo, G. L., Massimini, M., & Nobili, L. (2014). Hippocampal sleep spindles preceding neocortical sleep onset in humans. NeuroImage, 86, 425-432.
Saturnino, G., Antunes, A., Stelzer, J., & Thielscher, A. (2015). SimNIBS: A versatile toolbox for simulating fields generated by transcranial brain stimulation. In 21st Annual Meeting of the Organization for Human Brain Mapping (OHBM 2015), Conference Paper.
Stagg, C. J., & Nitsche, M. A. (2011). Physiological basis of transcranial direct current stimulation. The Neuroscientist, 17(1), 37-53.
Vyazovskiy, V. V., Olcese, U., Hanlon, E. C., Nir, Y., Cirelli, C., & Tononi, G. (2011). Local sleep in awake rats. Nature, 472(7344), 443-447.
Werth, E., Achermann, P., & Borbély, A. A. (1996). Brain topography of the human sleep EEG: Antero-posterior shifts of spectral power. Neuroreport, 8(1), 123-127.
Wright, K. P., Jr., Hull, J. T., & Czeisler, C. A. (2002). Relationship between alertness, performance, and body temperature in humans. American Journal of Physiology-Regulatory, Integrative and Comparative Physiology, 283(6), R1370-R1377.
Xie, J., Wang, L., Xiao, C., Ying, S., Ren, J., Chen, Z., Yu, Y., Xu, D., Yao, D., & Wu, B. (2021). Low frequency transcranial alternating current stimulation accelerates sleep onset process. IEEE Transactions on Neural Systems and Rehabilitation Engineering, 29, 2540-2549.
Yavari, F., Jamil, A., Samani, M. M., Vidor, L. P., & Nitsche, M. A. (2018). Basic and functional effects of transcranial electrical stimulation (tES)-An introduction. Neuroscience & Biobehavioral Reviews, 85, 81-92.