High-dose ethanol intoxication decreases 1/f neural noise or scale-free neural activity in the resting state.
1/f neural noise
alcohol
resting state EEG
Journal
Addiction biology
ISSN: 1369-1600
Titre abrégé: Addict Biol
Pays: United States
ID NLM: 9604935
Informations de publication
Date de publication:
11 2020
11 2020
Historique:
received:
18
03
2019
revised:
08
07
2019
accepted:
11
07
2019
pubmed:
2
8
2019
medline:
29
9
2021
entrez:
2
8
2019
Statut:
ppublish
Résumé
Binge drinking is a frequent phenomenon in many western societies and has been associated with an increased risk of developing alcohol use disorder later in life. Yet, the effects of high-dose alcohol intoxication on neurophysiological processes are still quite poorly understood. This is particularly the case given that neurophysiological brain activity not only contains recurring (oscillatory) patterns of activity, but also a significant fraction of "scale-free" or arrhythmic dynamics referred to as 1/f type activity, pink noise, or 1/f neural noise. Neurobiological considerations suggest that it should be modulated by alcohol intoxication. To investigate this assumption, we collected resting state EEG data from n = 23 healthy young male subjects in a crossover design, where each subject was once tested sober and once tested while intoxicated (mean breath alcohol concentration of 1.1 permille ±0.2). Analyses of the 1/f neural dynamics showed that ethanol intoxication decreased resting state 1/f neural noise, as compared with a sober state. The effects were strongest when the eyes were closed and particularly reliable in the beta frequency band. Given that the dynamics of the beta band have been shown to strongly depend on GABA
Substances chimiques
Receptors, GABA-A
0
Ethanol
3K9958V90M
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
e12818Informations de copyright
© 2019 Society for the Study of Addiction.
Références
Courtney KE, Polich J. Binge drinking in young adults: data, definitions, and determinants. Psychol Bull. 2009;135(1):142-156.
Montgomery C, Fisk JE, Murphy PN, Ryland I, Hilton J. The effects of heavy social drinking on executive function: a systematic review and meta-analytic study of existing literature and new empirical findings. Hum Psychopharmacol. 2012;27(2):187-199.
Davies M. The role of GABAA receptors in mediating the effects of alcohol in the central nervous system. J Psychiatry Neurosci JPN. 2003;28:263-274.
Kumar S, Porcu P, Werner DF, et al. The role of GABAA receptors in the acute and chronic effects of ethanol: a decade of progress. Psychopharmacology (Berl). 2009;205(4):529-564.
Baumgarten TJ, Oeltzschner G, Hoogenboom N, Wittsack H-J, Schnitzler A, Lange J. Beta peak frequencies at rest correlate with endogenous GABA+/Cr concentrations in sensorimotor cortex areas. PLoS ONE. 2016;11(6):e0156829.
Gaetz W, Edgar JC, Wang DJ, Roberts TPL. Relating MEG measured motor cortical oscillations to resting γ-aminobutyric acid (GABA) concentration. Neuroimage. 2011;55(2):616-621.
Muthukumaraswamy SD, Myers JFM, Wilson SJ, et al. The effects of elevated endogenous GABA levels on movement-related network oscillations. Neuroimage. 2013;66:36-41.
Osinski BL, Kim A, Xiao W, Mehta NM, Kay LM. Pharmacological manipulation of the olfactory bulb modulates beta oscillations: testing model predictions. J Neurophysiol. 2018;120(3):1090-1106.
Jensen O, Goel P, Kopell N, Pohja M, Hari R, Ermentrout B. On the human sensorimotor-cortex beta rhythm: sources and modeling. Neuroimage. 2005;26(2):347-355.
Hall SD, Barnes GR, Furlong PL, Seri S, Hillebrand A. Neuronal network pharmacodynamics of GABAergic modulation in the human cortex determined using pharmaco-magnetoencephalography. Hum Brain Mapp. 2009;n/a-n/a.
Baker MR, Baker SN. The effect of diazepam on motor cortical oscillations and corticomuscular coherence studied in man. J Physiol. 2003;546(3):931-942.
Rosen BQ, O'Hara R, Kovacevic S, Schulman A, Padovan N, Marinkovic K. Oscillatory spatial profile of alcohol's effects on the resting state: anatomically-constrained MEG. Alcohol. 2014;48(2):89-97.
Rangaswamy M, Porjesz B, Chorlian DB, et al. Beta power in the EEG of alcoholics. Biol Psychiatry. 2002;52(8):831-842.
Rangaswamy M, Porjesz B, Chorlian DB, et al. Resting EEG in offspring of male alcoholics: beta frequencies. Int J Psychophysiol Off J Int Organ Psychophysiol. 2004;51:239-251.
Fein G, Allen J. EEG spectral changes in treatment-naive, actively drinking alcoholics. Alcohol Clin Exp Res. 2005;29(4):538-546.
He BJ. Scale-free brain activity: past, present, and future. Trends Cogn Sci. 2014;18(9):480-487.
Buzsáki G. Rhythms of the Brain. Oxford University Press; 2006.
Voytek B, Kramer MA, Case J, et al. Age-related changes in 1/f neural electrophysiological noise. J Neurosci. 2015;35(38):13257-13265.
Muthukumaraswamy SD, Liley DTJ. 1/f electrophysiological spectra in resting and drug-induced states can be explained by the dynamics of multiple oscillatory relaxation processes. Neuroimage. 2018;179:582-595.
Gireesh ED, Plenz D. Neuronal avalanches organize as nested theta- and beta/gamma-oscillations during development of cortical layer 2/3. Proc Natl Acad Sci U S A. 2008;105(21):7576-7581.
Palva JM, Zhigalov A, Hirvonen J, Korhonen O, Linkenkaer-Hansen K, Palva S. Neuronal long-range temporal correlations and avalanche dynamics are correlated with behavioral scaling laws. Proc Natl Acad Sci U S A. 2013;110(9):3585-3590.
Stock A-K, Wolff N, Beste C. Opposite effects of binge drinking on consciously vs. subliminally induced cognitive conflicts. Neuroimage. 2017;162:117-126.
Babor TF, Higgins-Biddle JC, Saunders JB, Monteiro MG. The Alcohol Use Disorders Identification Test Guidelines for Use in Primary Care. Second ed. Geneva, Switzerland: World Health Organization; 2001.
Stock A-K, Hoffmann S, Beste C. Effects of binge drinking and hangover on response selection sub-processes-a study using EEG and drift diffusion modeling. Addict Biol. 2017;22(5):1355-1365.
Stock A-K, Blaszkewicz M, Beste C. Effects of binge drinking on action cascading processes: an EEG study. Arch Toxicol. 2014;88(2):475-488.
Wolff N, Gussek P, Stock A-K, Beste C. Effects of high-dose ethanol intoxication and hangover on cognitive flexibility. Addict Biol. 2018;23(1):503-514.
Widmark EMP. Die theoretischen Grundlagen und die praktische Verwendbarkeit der gerichtlich-medizinischen Alkoholbestimmung. Berlin: Urban und Schwarzenberg; 1932.
Watson PE, Watson ID, Batt RD. Total body water volumes for adult males and females estimated from simple anthropometric measurements. Am J Clin Nutr. 1980;33(1):27-39.
Friedman RS, McCarthy DM, Bartholow BD, Hicks JA. Interactive effects of alcohol outcome expectancies and alcohol cues on nonconsumptive behavior. Exp Clin Psychopharmacol. 2007;15(1):102-114.
Read JP, Curtin JJ. Contextual influences on alcohol expectancy processes. J Stud Alcohol Drugs. 2007;68(5):759-770.
Oostenveld R, Fries P, Maris E, Schoffelen J-M. FieldTrip: open source software for advanced analysis of MEG, EEG, and invasive electrophysiological data. Comput Intell Neurosci 2011;2011: 1-9.
Dave S, Brothers TA, Swaab TY. 1/f neural noise and electrophysiological indices of contextual prediction in aging. Brain Res. 1691;2018:34-43.
He BJ, Zempel JM, Snyder AZ, Raichle ME. The temporal structures and functional significance of scale-free brain activity. Neuron. 2010;66(3):353-369.
Miller KJ, Sorensen LB, Ojemann JG, den Nijs M. Power-law scaling in the brain surface electric potential. PLoS Comput Biol. 2009;5:e1000609.
Touboul J, Destexhe A. Power-law statistics and universal scaling in the absence of criticality. Phys Rev E. 2017;95(1).
Welch PD. The use of fast Fourier transform for the estimation of power spectra: a method based on time averaging over short, modified periodograms. IEEE Trans Audio Electroacoust. 1967;15:70-73.
Pertermann M, Mückschel M, Adelhöfer N, Ziemssen T, Beste C. On the interrelation of 1/f neural noise and norepinephrine system activity during motor response inhibition. J Neurophysiol. 2019. https://doi.org/10.1152/jn.00701.2018
Manning JR, Jacobs J, Fried I, Kahana MJ. Broadband shifts in local field potential power spectra are correlated with single-neuron spiking in humans. J Neurosci. 2009;29(43):13613-13620.
Voytek B, Knight RT. Dynamic network communication as a unifying neural basis for cognition, development, aging, and disease. Biol Psychiatry. 2015;77(12):1089-1097.
Musall S, von Pföstl V, Rauch A, Logothetis NK, Whittingstall K. Effects of neural synchrony on surface EEG. Cereb Cortex N Y N 1991. 2014;24:1045-1053.
Katzner S, Nauhaus I, Benucci A, Bonin V, Ringach DL, Carandini M. Local origin of field potentials in visual cortex. Neuron. 2009;61(1):35-41.
Podvalny E, Noy N, Harel M, et al. A unifying principle underlying the extracellular field potential spectral responses in the human cortex. J Neurophysiol. 2015;114(1):505-519.
Gao R, Peterson EJ, Voytek B. Inferring synaptic excitation/inhibition balance from field potentials. Neuroimage. 2017;158:70-78.
Iversen LL, Iversen SD, Bloom FE, Roth RH. Introduction to Neuropsychopharmacology. New York: Oxford University Press; 2009.
Barry RJ, Clarke AR, Johnstone SJ, Magee CA, Rushby JA. EEG differences between eyes-closed and eyes-open resting conditions. Clin Neurophysiol Off J Int Fed Clin Neurophysiol. 2007;118(12):2765-2773.
Barry RJ, De Blasio FM. EEG differences between eyes-closed and eyes-open resting remain in healthy ageing. Biol Psychol. 2017;129:293-304.
Nutt D, Wilson S, Lingford-Hughes A, Myers J, Papadopoulos A, Muthukumaraswamy S. Differences between magnetoencephalographic (MEG) spectral profiles of drugs acting on GABA at synaptic and extrasynaptic sites: a study in healthy volunteers. Neuropharmacology. 2015;88:155-163.
Mason BJ, Quello S, Shadan F. Gabapentin for the treatment of alcohol use disorder. Expert Opin Investig Drugs. 2018;27(1):113-124.