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01-05-2018 | Original Paper

Brain Networks are Independently Modulated by Donepezil, Sleep, and Sleep Deprivation

Authors: Jonathan Wirsich, Marc Rey, Maxime Guye, Christian Bénar, Laura Lanteaume, Ben Ridley, Sylviane Confort-Gouny, Catherine Cassé-Perrot, Elisabeth Soulier, Patrick Viout, Franck Rouby, Marie-Noëlle Lefebvre, Christine Audebert, Romain Truillet, Elisabeth Jouve, Pierre Payoux, David Bartrés-Faz, Régis Bordet, Jill C. Richardson, Claudio Babiloni, Paolo Maria Rossini, Joelle Micallef, Olivier Blin, Jean-Philippe Ranjeva, The Pharmacog Consortium

Published in: Brain Topography | Issue 3/2018

Abstract

Resting-state connectivity has been widely studied in the healthy and pathological brain. Less well-characterized are the brain networks altered during pharmacological interventions and their possible interaction with vigilance. In the hopes of finding new biomarkers which can be used to identify cortical activity and cognitive processes linked to the effects of drugs to treat neurodegenerative diseases such as Alzheimer’s disease, the analysis of networks altered by medication would be particularly interesting. Eleven healthy subjects were recruited in the context of the European Innovative Medicines Initiative ‘PharmaCog’. Each underwent five sessions of simultaneous EEG-fMRI in order to investigate the effects of donepezil and memantine before and after sleep deprivation (SD). The SD approach has been previously proposed as a model for cognitive impairment in healthy subjects. By applying network based statistics (NBS), we observed altered brain networks significantly linked to donepezil intake and sleep deprivation. Taking into account the sleep stages extracted from the EEG data we revealed that a network linked to sleep is interacting with sleep deprivation but not with medication intake. We successfully extracted the functional resting-state networks modified by donepezil intake, sleep and SD. We observed donepezil induced whole brain connectivity alterations forming a network separated from the changes induced by sleep and SD, a result which shows the utility of this approach to check for the validity of pharmacological resting-state analysis of the tested medications without the need of taking into account the subject specific vigilance.

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Achard S, Salvador R, Whitcher B, Suckling J, Bullmore E (2006) A resilient, low-frequency, small-world human brain functional network with highly connected association cortical hubs. J Neurosci 26(1):63–72. https://doi.org/10.1523/JNEUROSCI.3874-05.2006 CrossRefPubMed

Alkire MT, Hudetz AG, Tononi G (2008) Consciousness and anesthesia. Science 322:876–880. https://doi.org/10.1126/science.1149213 CrossRefPubMedPubMedCentral

Allen PJ, Polizzi G, Krakow K, Fish DR, Lemieux L (1998) Identification of EEG events in the MR scanner: the problem of pulse artifact and a method for its subtraction. Neuroimage 8:229–239. https://doi.org/10.1006/nimg.1998.0361 CrossRefPubMed

Allen PJ, Josephs O, Turner R (2000) A method for removing imaging artifact from continuous EEG recorded during functional MRI. Neuroimage 12(2):230–239. https://doi.org/10.1006/nimg.2000.0599 CrossRefPubMed

Babiloni C, Del Percio C, Bordet R, Bourriez JL, Bentivoglio M, Payoux P, Derambure P, Dix S, Infarinato F, Lizio R, Triggiani AI, Richardson JC, Rossini PM (2013) Effects of acetylcholinesterase inhibitors and memantine on resting-state electroencephalographic rhythms in Alzheimer’s disease patients. Clin Neurophysiol 124(5):837–850. https://doi.org/10.1016/j.clinph.2012.09.017 CrossRefPubMed

Balsters JH, O’Connell RG, Martin MP, Galli A, Cassidy SM, Kilcullen SM, Delmonte S, Brennan S, Meaney JF, Fagan AJ, Bokde AL, Upton N, Lai R, Laruelle M, Lawlor B, Robertson IH (2011) Donepezil impairs memory in healthy older subjects: behavioural, EEG and simultaneous EEG/fMRI biomarkers. PLoS ONE 6(9):e24126. https://doi.org/10.1371/journal.pone.0024126 CrossRefPubMedPubMedCentral

Barttfeld P, Uhrig L, Sitt JD, Sigman M, Jarraya B, Dehaene S (2015) Signature of consciousness in the dynamics of resting-state brain activity. Proc Natl Acad Sci USA 112:887–892. https://doi.org/10.1073/pnas.1418031112 CrossRefPubMedPubMedCentral

Bassett DS, Bullmore ET (2009) Human brain networks in health and disease. Curr Opin Neurol 22(4):340–347. https://doi.org/10.1097/WCO.0b013e32832d93dd CrossRefPubMedPubMedCentral

Bodenmann S, Landolt HP (2010) Effects of modafinil on the sleep EEG depend on Val158Met genotype of COMT. Sleep 33(8):1027–1035CrossRefPubMedPubMedCentral

Cajochen C, Brunner DP, Krauchi K, Graw P, Wirz-Justice A (1995) Power density in theta/alpha frequencies of the waking EEG progressively increases during sustained wakefulness. Sleep 18(10):890–894CrossRefPubMed

Cassé-Perrot C, Lanteaume L, Deguil J, Bordet R, Auffret A, Otten L, Blin O, Bartrés-Faz D, Micallef J (2016) Neurobehavioral and cognitive changes induced by sleep deprivation in healthy volunteers. CNS Neurol Disord Drug Targets 15(7):777–801CrossRefPubMed

Cera N, Tartaro A, Sensi SL (2014) Modafinil alters intrinsic functional connectivity of the right posterior insula: a pharmacological resting state fMRI study. PLoS ONE 9(9):e107145. https://doi.org/10.1371/journal.pone.0107145 CrossRefPubMedPubMedCentral

Chee MW, Chuah LY (2008) Functional neuroimaging insights into how sleep and sleep deprivation affect memory and cognition. Curr Opin Neurol 21(4):417–423. https://doi.org/10.1097/WCO.0b013e3283052cf7 CrossRefPubMed

Chuah LY, Chee MW (2008) Cholinergic augmentation modulates visual task performance in sleep-deprived young adults. J Neurosci 28(44):11369–11377. https://doi.org/10.1523/JNEUROSCI.4045-08.2008 CrossRefPubMed

Chuah LY, Chong DL, Chen AK, Rekshan WR 3rd, Tan JC, Zheng H, Chee MW (2009) Donepezil improves episodic memory in young individuals vulnerable to the effects of sleep deprivation. Sleep 32(8):999–1010CrossRefPubMedPubMedCentral

Dinges DF, Arora S, Darwish M, Niebler GE (2006) Pharmacodynamic effects on alertness of single doses of armodafinil in healthy subjects during a nocturnal period of acute sleep loss. Curr Med Res Opin 22(1):159–167. https://doi.org/10.1185/030079906X80378 CrossRefPubMed

Dodds CM, Bullmore ET, Henson RN, Christensen S, Miller S, Smith M, Dewit O, Lawrence P, Nathan PJ (2011) Effects of donepezil on cognitive performance after sleep deprivation. Hum Psychopharmacol 26(8):578–587. https://doi.org/10.1002/hup.1248 CrossRefPubMed

Esposito R, Cilli F, Pieramico V, Ferretti A, Macchia A, Tommasi M, Saggino A, Ciavardelli D, Manna A, Navarra R, Cieri F, Stuppia L, Tartaro A, Sensi SL (2013) Acute effects of modafinil on brain resting state networks in young healthy subjects. PLoS ONE 8(7):e69224. https://doi.org/10.1371/journal.pone.0069224 CrossRefPubMedPubMedCentral

Estevez-Gonzalez A, Kulisevsky J, Boltes A, Otermin P, Garcia-Sanchez C (2003) Rey verbal learning test is a useful tool for differential diagnosis in the preclinical phase of Alzheimer’s disease: comparison with mild cognitive impairment and normal aging. Int J Geriatr Psychiatry 18(11):1021–1028. https://doi.org/10.1002/gps.1010 CrossRefPubMed

Fornito A, Zalesky A, Breakspear M (2015) The connectomics of brain disorders. Nat Rev Neurosci 16(3):159–172. https://doi.org/10.1038/nrn3901 CrossRefPubMed

Fox MD, Greicius M (2010) Clinical applications of resting state functional connectivity. Front Syst Neurosci 4:19. https://doi.org/10.3389/fnsys.2010.00019 PubMedPubMedCentral

Freedman D, Lane D (1983) A nonstochastic interpretation of reported significance levels. J Bus Econ Stat 1(4):292–298. https://doi.org/10.1080/07350015.1983.10509354

Gour N, Felician O, Didic M, Koric L, Gueriot C, Chanoine V, Confort-Gouny S, Guye M, Ceccaldi M, Ranjeva JP (2014) Functional connectivity changes differ in early and late-onset Alzheimer’s disease. Hum Brain Mapp 35:2978–2994. https://doi.org/10.1002/hbm.22379 CrossRefPubMed

Greicius MD, Supekar K, Menon V, Dougherty RF (2009) Resting-state functional connectivity reflects structural connectivity in the default mode network. Cereb Cortex 19:72–78. https://doi.org/10.1093/cercor/bhn059 CrossRefPubMed

Griffanti L, Wilcock GK, Voets N, Bonifacio G, Mackay CE, Jenkinson M, Zamboni G (2016) Donepezil enhances frontal functional connectivity in Alzheimer’s disease: a pilot study. Dement Geriatr Cogn Dis Extra 6:518–528. https://doi.org/10.1159/000450546 CrossRefPubMedPubMedCentral

Hedreen JC, Struble RG, Whitehouse PJ, Price DL (1984) Topography of the magnocellular basal forebrain system in human brain. J Neuropathol Exp Neurol 43:1–21CrossRefPubMed

Honey CJ, Sporns O, Cammoun L, Gigandet X, Thiran JP, Meuli R, Hagmann P (2009) Predicting human resting-state functional connectivity from structural connectivity. Proc Natl Acad Sci USA 106:2035–2040. https://doi.org/10.1073/pnas.0811168106 CrossRefPubMedPubMedCentral

Iannone R, Palcza J, Renger JJ, Calder N, Cerchio K, Gottesdiener K, Hargreaves R, Dijk DJ, Boyle J, Murphy MG (2010) Acute alertness-promoting effects of a novel histamine subtype-3 receptor inverse agonist in healthy sleep-deprived male volunteers. Clin Pharmacol Ther 88(6):831–839. https://doi.org/10.1038/clpt.2010.205 CrossRefPubMed

Kaufmann T, Elvsashagen T, Alnaes D, Zak N, Pedersen PO, Norbom LB, Quraishi SH, Tagliazucchi E, Laufs H, Bjornerud A, Malt UF, Andreassen OA, Roussos E, Duff EP, Smith SM, Groote IR, Westlye LT (2015) The brain functional connectome is robustly altered by lack of sleep. Neuroimage 127:324–332. https://doi.org/10.1016/j.neuroimage.2015.12.028 CrossRefPubMed

Killgore WD, Richards JM, Killgore DB, Kamimori GH, Balkin TJ (2007) The trait of Introversion-Extraversion predicts vulnerability to sleep deprivation. J Sleep Res 16:354–363. https://doi.org/10.1111/j.1365-2869.2007.00611.x CrossRefPubMed

Lanctot KL, Herrmann N, LouLou MM (2003) Correlates of response to acetylcholinesterase inhibitor therapy in Alzheimer’s disease. J Psychiatry Neurosci 28(1):13–26PubMedPubMedCentral

McShane R, Areosa Sastre A, Minakaran N (2006) Memantine for dementia. Cochrane Database Syst Rev (2):CD003154. https://doi.org/10.1002/14651858.CD003154.pub5

Porsteinsson AP, Grossberg GT, Mintzer J, Olin JT (2008) Memantine treatment in patients with mild to moderate Alzheimer’s disease already receiving a cholinesterase inhibitor: a randomized, double-blind, placebo-controlled trial. Curr Alzheimer Res 5(1):83–89CrossRefPubMed

Repantis D, Schlattmann P, Laisney O, Heuser I (2010) Modafinil and methylphenidate for neuroenhancement in healthy individuals: a systematic review. Pharmacol Res 62(3):187–206. https://doi.org/10.1016/j.phrs.2010.04.002 CrossRefPubMed

Robbins TW (2005) Chemistry of the mind: neurochemical modulation of prefrontal cortical function. J Comp Neurol 493:140–146. https://doi.org/10.1002/cne.20717 CrossRefPubMed

Sarter M, Parikh V (2005) Choline transporters, cholinergic transmission and cognition. Nat Rev Neurosci 6:48–56. https://doi.org/10.1038/nrn1588 CrossRefPubMed

Schulz H, Jobert M, Coppola R, Herrmann WM, Pantev M (1996) The use of diurnal vigilance changes in the EEG to verify vigilance-enhancing effects of memantine in a clinical pharmacological study. Neuropsychobiology 33(1):32–40CrossRefPubMed

Shirer WR, Ryali S, Rykhlevskaia E, Menon V, Greicius MD (2012) Decoding subject-driven cognitive states with whole-brain connectivity patterns. Cereb Cortex 22:158–165. https://doi.org/10.1093/cercor/bhr099 CrossRefPubMed

Silver MA, Shenhav A, D’Esposito M (2008) Cholinergic enhancement reduces spatial spread of visual responses in human early visual cortex. Neuron 60(5):904–914. https://doi.org/10.1016/j.neuron.2008.09.038 CrossRefPubMedPubMedCentral

Sole-Padulles C, Bartres-Faz D, Llado A, Bosch B, Pena-Gomez C, Castellvi M, Rami L, Bargallo N, Sanchez-Valle R, Molinuevo JL (2013) Donepezil treatment stabilizes functional connectivity during resting state and brain activity during memory encoding in Alzheimer’s disease. J Clin Psychopharmacol 33:199–205. https://doi.org/10.1097/JCP.0b013e3182825bfd CrossRefPubMed

Sporns O (2013) Structure and function of complex brain networks. Dialogues Clin Neurosci 15(3):247–262PubMedPubMedCentral

Sporns O, Tononi G, Kotter R (2005) The human connectome: a structural description of the human brain. PLoS Comput Biol 1(4):e42. https://doi.org/10.1371/journal.pcbi.0010042 CrossRefPubMedPubMedCentral

Tagliazucchi E, Laufs H (2014) Decoding wakefulness levels from typical fMRI resting-state data reveals reliable drifts between wakefulness and sleep. Neuron 82(3):695–708. https://doi.org/10.1016/j.neuron.2014.03.020 CrossRefPubMed

Tagliazucchi E, van Someren EJW (2017) The large-scale functional connectivity correlates of consciousness and arousal during the healthy and pathological human sleep cycle. NeuroImage. https://doi.org/10.1016/j.neuroimage.2017.06.026

Tagliazucchi E, von Wegner F, Morzelewski A, Brodbeck V, Borisov S, Jahnke K, Laufs H (2013) Large-scale brain functional modularity is reflected in slow electroencephalographic rhythms across the human non-rapid eye movement sleep cycle. Neuroimage 70:327–339. https://doi.org/10.1016/j.neuroimage.2012.12.073 CrossRefPubMed

Taylor DJ, McFatter RM (2003) Cognitive performance after sleep deprivation: does personality make a difference? Pers Indiv Differ 34(7):1179–1193. https://doi.org/10.1016/S0191-8869(02)00108-3 CrossRef

Tierney MC, Black SE, Szalai JP, Snow WG, Fisher RH, Nadon G, Chui HC (2001) Recognition memory and verbal fluency differentiate probable Alzheimer disease from subcortical ischemic vascular dementia. Arch Neurol 58(10):1654–1659. https://doi.org/10.1001/archneur.58.10.1654 CrossRefPubMed

Tzourio-Mazoyer N, Landeau B, Papathanassiou D, Crivello F, Etard O, Delcroix N, Mazoyer B, Joliot M (2002) Automated anatomical labeling of activations in SPM using a macroscopic anatomical parcellation of the MNI MRI single-subject brain. Neuroimage 15(1):273–289. https://doi.org/10.1006/nimg.2001.0978 CrossRefPubMed

Van Dongen HP, Baynard MD, Maislin G, Dinges DF (2004) Systematic interindividual differences in neurobehavioral impairment from sleep loss: evidence of trait-like differential vulnerability. Sleep 27:423–433PubMed

Winkler AM, Ridgway GR, Webster MA, Smith SM, Nichols TE (2014) Permutation inference for the general linear model. Neuroimage 92:381–397. https://doi.org/10.1016/j.neuroimage.2014.01.060 CrossRefPubMedPubMedCentral

Wirsich J, Perry A, Ridley B, Proix T, Golos M, Benar C, Ranjeva JP, Bartolomei F, Breakspear M, Jirsa V, Guye M (2016) Whole-brain analytic measures of network communication reveal increased structure–function correlation in right temporal lobe epilepsy. Neuroimage Clin 11:707–718. https://doi.org/10.1016/j.nicl.2016.05.010 CrossRefPubMedPubMedCentral

Xia M, Wang J, He Y (2013) BrainNet Viewer: a network visualization tool for human brain connectomics. PLoS ONE 8(7):e68910. https://doi.org/10.1371/journal.pone.0068910 CrossRefPubMedPubMedCentral

Yeo BT, Tandi J, Chee MW (2015) Functional connectivity during rested wakefulness predicts vulnerability to sleep deprivation. Neuroimage 111:147–158. https://doi.org/10.1016/j.neuroimage.2015.02.018 CrossRefPubMed

Zalesky A, Fornito A, Bullmore ET (2010) Network-based statistic: identifying differences in brain networks. Neuroimage 53(4):1197–1207. https://doi.org/10.1016/j.neuroimage.2010.06.041 CrossRefPubMed

Title: Brain Networks are Independently Modulated by Donepezil, Sleep, and Sleep Deprivation
Authors: Jonathan Wirsich
Marc Rey
Maxime Guye
Christian Bénar
Laura Lanteaume
Ben Ridley
Sylviane Confort-Gouny
Catherine Cassé-Perrot
Elisabeth Soulier
Patrick Viout
Franck Rouby
Marie-Noëlle Lefebvre
Christine Audebert
Romain Truillet
Elisabeth Jouve
Pierre Payoux
David Bartrés-Faz
Régis Bordet
Jill C. Richardson
Claudio Babiloni
Paolo Maria Rossini
Joelle Micallef
Olivier Blin
Jean-Philippe Ranjeva
The Pharmacog Consortium
Publication date: 01-05-2018
Publisher: Springer US
Published in: Brain Topography / Issue 3/2018
Print ISSN: 0896-0267
Electronic ISSN: 1573-6792
DOI: https://doi.org/10.1007/s10548-017-0608-5

At a glance: The STEP trials

Springer Medicine

Brain Networks are Independently Modulated by Donepezil, Sleep, and Sleep Deprivation

Abstract

At a glance: The STEP trials

Springer Medicine

Abstract

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