Generic placeholder image

Current Molecular Pharmacology

Editor-in-Chief

ISSN (Print): 1874-4672
ISSN (Online): 1874-4702

Review Article

Effects of Modafinil (Provigil) on Memory and Learning in Experimental and Clinical Studies: From Molecular Mechanisms to Behaviour Molecular Mechanisms and Behavioural Effects

Author(s): Mohammad Yassin Zamanian, Mahdi Najafiani Karimvandi, Marjan Nikbakhtzadeh, Elham Zahedi, Dmitry Olegovich Bokov, Małgorzata Kujawska, Mahsa Heidari and Mohammad Reza Rahmani*

Volume 16, Issue 4, 2023

Published on: 16 November, 2022

Article ID: e010922208415 Pages: 10

DOI: 10.2174/1874467215666220901122824

Price: $65

Abstract

Modafinil (MOD, 2‐diphenyl‐methyl‐sulphinil‐2‐acetamide) is a stimulant-like medicine used to treat narcolepsy. Off-label uses include improving cognitive ability in the course of other diseases. This review aims to discuss findings demonstrating the memory and learningenhancing activity of MOD in experimental and clinical studies. We included behavioral evaluations alongside the effects of MOD at the cellular and molecular level.

MOD in different animal disease models exerted beneficial effects on induced memory and learning impairment, which in some cases were accompanied by modulation of neurotransmitter pathways or neuroplastic capabilities, reducing oxidative stress, or expression of synaptic proteins. Individuals treated with MOD showed improved memory and learning skills in different conditions. These effects were associated with regulating brain activity in some participants, confirmed by functional magnetic resonance imaging.

Presented herein, data support the use of MOD in treating memory and learning deficits in various disease conditions.

Keywords: Modafinil, memory, learning, oxidative stress, hippocampus, synaptic plasticity.

[1]
Minzenberg, M.J.; Carter, C.S. Modafinil: A review of neurochemical actions and effects on cognition. Neuropsychopharmacology, 2008, 33(7), 1477-1502.
[http://dx.doi.org/10.1038/sj.npp.1301534] [PMID: 17712350]
[2]
Sahakian, B.J.; Morein-Zamir, S. Pharmacological cognitive enhancement: Treatment of neuropsychiatric disorders and lifestyle useby healthy people. Lancet Psychiatry, 2015, 2(4), 357-362.
[http://dx.doi.org/10.1016/S2215-0366(15)00004-8] [PMID: 26360089]
[3]
Peñaloza, R.A.; Sarkar, U.; Claman, D.M.; Omachi, T.A. Trends in on-label and off-label modafinil use in a nationally representative sample. JAMA Intern. Med., 2013, 173(8), 704-706.
[http://dx.doi.org/10.1001/jamainternmed.2013.2807] [PMID: 23552641]
[4]
Turner, D.C.; Clark, L.; Dowson, J.; Robbins, T.W.; Sahakian, B.J. Modafinil improves cognition and response inhibition in adult attention-deficit/hyperactivity disorder. Biol. Psychiatry, 2004, 55(10), 1031-1040.
[http://dx.doi.org/10.1016/j.biopsych.2004.02.008] [PMID: 15121488]
[5]
Ballon, J.S.; Feifel, D. A systematic review of modafinil: Potential clinical uses and mechanisms of action. J. Clin. Psychiatry, 2006, 67(4), 554-566.
[http://dx.doi.org/10.4088/JCP.v67n0406] [PMID: 16669720]
[6]
Raineri, M.; Gonzalez, B.; Goitia, B.; Garcia-Rill, E.; Krasnova, I.N.; Cadet, J.L.; Urbano, F.J.; Bisagno, V. Modafinil abrogates methamphetamine-induced neuroinflammation and apoptotic effects in the mouse striatum. PLoS One, 2012, 7(10), e46599.
[http://dx.doi.org/10.1371/journal.pone.0046599]
[7]
Brandt, M.D.; Ellwardt, E.; Storch, A. Short- and long-term treatment with modafinil differentially affects adult hippocampal neurogenesis. Neuroscience, 2014, 278, 267-275.
[http://dx.doi.org/10.1016/j.neuroscience.2014.08.014] [PMID: 25158676]
[8]
Yan, Y.D.; Chen, Y.Q.; Wang, C.Y.; Ye, C.B.; Hu, Z.Z.; Behnisch, T.; Huang, Z.L.; Yang, S.R. Chronic modafinil therapy ameliorates depressive-like behavior, spatial memory and hippocampal plasticity impairments, and sleep-wake changes in a surgical mouse model of menopause. Transl. Psychiatry, 2021, 11(1), 116.
[http://dx.doi.org/10.1038/s41398-021-01229-6] [PMID: 33558464]
[9]
Squire, L.R. Memory and brain systems: 1969-2009. J. Neurosci., 2009, 29(41), 12711-12716.
[http://dx.doi.org/10.1523/JNEUROSCI.3575-09.2009] [PMID: 19828780]
[10]
Zlotnik, G.; Vansintjan, A. Memory: An extended definition. Front. Psychol., 2019, 10, 2523.
[http://dx.doi.org/10.3389/fpsyg.2019.02523] [PMID: 31787916]
[11]
Camina, E.; Güell, F. The neuroanatomical, neurophysiological and psychological basis of memory: Current models and their origins. Front. Pharmacol., 2017, 8, 438.
[http://dx.doi.org/10.3389/fphar.2017.00438] [PMID: 28713278]
[12]
Zhang, W.; Guo, L.; Liu, D.; Xu, G. The dynamic properties of a brain network during working memory based on the algorithm of cross-frequency coupling. Cogn. Neurodynamics, 2020, 14(2), 215-228.
[http://dx.doi.org/10.1007/s11571-019-09562-9] [PMID: 32226563]
[13]
Yan, W.W.; Yao, L.H.; Chen, C.; Wang, H.X.; Li, C.H.; Huang, J.N.; Xiao, P.; Liu, C.Y. Effects of modafinil on behavioral learning and hippocampal synaptic transmission in rats. Int. Neurourol. J., 2015, 19(4), 220-227.
[http://dx.doi.org/10.5213/inj.2015.19.4.220] [PMID: 26739176]
[14]
Scoriels, L.; Jones, P.B.; Sahakian, B.J. Modafinil effects on cognition and emotion in schizophrenia and its neurochemical modulation in the brain. Neuropharmacology, 2013, 64, 168-184.
[http://dx.doi.org/10.1016/j.neuropharm.2012.07.011] [PMID: 22820555]
[15]
Kaser, M.; Deakin, J.B.; Michael, A.; Zapata, C.; Bansal, R.; Ryan, D.; Cormack, F.; Rowe, J.B.; Sahakian, B.J. Modafinil improves episodic memory and working memory cognition in patients with remitted depression: A double-blind, randomized, placebo-controlled study. Biol. Psychiatry Cogn. Neurosci. Neuroimaging, 2017, 2(2), 115-122.
[http://dx.doi.org/10.1016/j.bpsc.2016.11.009] [PMID: 28299368]
[16]
Frakey, L.L.; Salloway, S.; Buelow, M.; Malloy, P. A randomized, double-blind, placebo-controlled trial of modafinil for the treatment of apathy in individuals with mild-to-moderate Alzheimer’s disease. J. Clin. Psychiatry, 2012, 73(6), 796-801.
[http://dx.doi.org/10.4088/JCP.10m06708] [PMID: 22687392]
[17]
Kumar, M.; Maqbool, S. Memory improvement by modafinil at cost of metabolic hazards? A study to decipher the benefits and risks of modafinil in rats. Neurotoxicology, 2020, 78, 106-115.
[http://dx.doi.org/10.1016/j.neuro.2020.02.014] [PMID: 32126242]
[18]
Murillo-Rodríguez, E.; Barciela Veras, A.; Barbosa Rocha, N.; Budde, H.; Machado, S. An overview of the clinical uses, pharmacology, and safety of modafinil. ACS Chem. Neurosci., 2018, 9(2), 151-158.
[http://dx.doi.org/10.1021/acschemneuro.7b00374] [PMID: 29115823]
[19]
Lin, J.S.; Roussel, B.; Gaspar, A.; Zhao, Y.; Hou, Y.; Schmidt, M.; Jouvet, A.; Jouvet, M. The unfinished journey with modafinil and discovery of a novel population of modafinil-immunoreactive neurons. Sleep Med., 2018, 49, 40-52.
[http://dx.doi.org/10.1016/j.sleep.2018.06.008] [PMID: 30172629]
[20]
Kaviani, E.; Rahmani, M.; Kaeidi, A.; Shamsizadeh, A.; Allahtavakoli, M.; Mozafari, N.; Fatemi, I. Protective effect of atorvastatin on d-galactose-induced aging model in mice. Behav. Brain Res., 2017, 334, 55-60.
[http://dx.doi.org/10.1016/j.bbr.2017.07.029] [PMID: 28750834]
[21]
Spiegel, K.; Tasali, E.; Leproult, R.; Van Cauter, E. Effects of poor and short sleep on glucose metabolism and obesity risk. Nat. Rev. Endocrinol., 2009, 5(5), 253-261.
[http://dx.doi.org/10.1038/nrendo.2009.23] [PMID: 19444258]
[22]
Garcia, V.A.; Hirotsu, C.; Matos, G.; Alvarenga, T.; Pires, G.N.; Kapczinski, F.; Schröder, N.; Tufik, S.; Andersen, M.L. Modafinil ameliorates cognitive deficits induced by maternal separation and sleep deprivation. Behav. Brain Res., 2013, 253, 274-279.
[http://dx.doi.org/10.1016/j.bbr.2013.07.029] [PMID: 23906765]
[23]
Garcia, V.A.; Souza de Freitas, B.; Busato, S.B.; D’avila Portal, B.C.; Piazza, F.C.; Schröder, N. Differential effects of modafinil on memory in naïve and memory-impaired rats. Neuropharmacology, 2013, 75, 304-311.
[http://dx.doi.org/10.1016/j.neuropharm.2013.07.038] [PMID: 23958446]
[24]
Zamanian, M.; Shamsizadeh, A.; Esmaeili Nadimi, A.; Hajizadeh, M.; Allahtavakoli, F.; Rahmani, M.; Kaeidi, A.; Safari Khalegh, H.; Allahtavakoli, M. Short-term effects of troxerutin (vitamin P4) on muscle fatigue and gene expression of Bcl-2 and Bax in the hepatic tissue of rats. Can. J. Physiol. Pharmacol., 2017, 95(6), 708-713.
[http://dx.doi.org/10.1139/cjpp-2016-0653] [PMID: 28187266]
[25]
Ornell, F.; Valvassori, S.S.; Steckert, A.V.; Deroza, P.F.; Resende, W.R.; Varela, R.B.; Quevedo, J. Modafinil effects on behavior and oxidative damage parameters in brain of wistar rats. Behav. Neurol., 2014, 2014, 1-7.
[http://dx.doi.org/10.1155/2014/917246] [PMID: 25431526]
[26]
Kristofova, M.; Aher, Y.D.; Ilic, M.; Radoman, B.; Kalaba, P.; Dragacevic, V.; Aher, N.Y.; Leban, J.; Korz, V.; Zanon, L.; Neuhaus, W.; Wieder, M.; Langer, T.; Urban, E.; Sitte, H.H.; Hoeger, H.; Lubec, G.; Aradska, J. A daily single dose of a novel modafinil analogue CE-123 improves memory acquisition and memory retrieval. Behav. Brain Res., 2018, 343, 83-94.
[http://dx.doi.org/10.1016/j.bbr.2018.01.032] [PMID: 29410048]
[27]
Shanmugasundaram, B.; Aher, Y.D.; Aradska, J.; Ilic, M.; Daba Feyissa, D.; Kalaba, P.; Aher, N.Y.; Dragacevic, V.; Saber Marouf, B.; Langer, T.; Sitte, H.H.; Hoeger, H.; Lubec, G.; Korz, V. R-Modafinil exerts weak effects on spatial memory acquisition and dentate gyrus synaptic plasticity. PLoS One, 2017, 12(6), e0179675.
[http://dx.doi.org/10.1371/journal.pone.0179675] [PMID: 28644892]
[28]
Dudchenko, P.A. An overview of the tasks used to test working memory in rodents. Neurosci. Biobehav. Rev., 2004, 28(7), 699-709.
[http://dx.doi.org/10.1016/j.neubiorev.2004.09.002] [PMID: 15555679]
[29]
Yoon, T.; Okada, J.; Jung, M.W.; Kim, J.J. Prefrontal cortex and hippocampus subserve different components of working memory in rats. Learn. Mem., 2008, 15(3), 97-105.
[http://dx.doi.org/10.1101/lm.850808] [PMID: 18285468]
[30]
Bezu, M.; Shanmugasundaram, B.; Lubec, G.; Korz, V. Repeated application of Modafinil and Levodopa reveals a drug-independent precise timing of spatial working memory modulation. Behav. Brain Res., 2016, 312, 9-13.
[http://dx.doi.org/10.1016/j.bbr.2016.06.003] [PMID: 27268456]
[31]
Shibani, F.; Sahamsizadeh, A.; Fatemi, I.; Allahtavakoli, M.; Hasanshahi, J.; Rahmani, M.; Azin, M.; Hassanipour, M.; Mozafari, N.; Kaeidi, A. Effect of oleuropein on morphine-induced hippocampus neurotoxicity and memory impairments in rats. Naunyn Schmiedebergs Arch. Pharmacol., 2019, 392(11), 1383-1391.
[http://dx.doi.org/10.1007/s00210-019-01678-3] [PMID: 31236657]
[32]
Antunes, M.; Biala, G. The novel object recognition memory: Neurobiology, test procedure, and its modifications. Cogn. Process., 2012, 13(2), 93-110.
[http://dx.doi.org/10.1007/s10339-011-0430-z] [PMID: 22160349]
[33]
Clarke, J.R.; Cammarota, M.; Gruart, A.; Izquierdo, I.; Delgado-García, J.M. Plastic modifications induced by object recognition memory processing. Proc. Natl. Acad. Sci. USA, 2010, 107(6), 2652-2657.
[http://dx.doi.org/10.1073/pnas.0915059107] [PMID: 20133798]
[34]
Sahu, S.; Kauser, H.; Ray, K.; Kishore, K.; Kumar, S.; Panjwani, U. Caffeine and modafinil promote adult neuronal cell proliferation during 48h of total sleep deprivation in rat dentate gyrus. Exp. Neurol., 2013, 248, 470-481.
[http://dx.doi.org/10.1016/j.expneurol.2013.07.021] [PMID: 23920241]
[35]
Wadhwa, M.; Sahu, S.; Kumari, P.; Kauser, H.; Ray, K.; Panjwani, U. Caffeine and modafinil given during 48h sleep deprivation modulate object recognition memory and synaptic proteins in the hippocampus of the rat. Behav. Brain Res., 2015, 294, 95-101.
[http://dx.doi.org/10.1016/j.bbr.2015.08.002] [PMID: 26255702]
[36]
Murphy, H.M.; Ekstrand, D.; Tarchick, M.; Wideman, C.H. Modafinil as a cognitive enhancer of spatial working memory in rats. Physiol. Behav., 2015, 142, 126-130.
[http://dx.doi.org/10.1016/j.physbeh.2015.02.003] [PMID: 25656691]
[37]
Ling, W.; Rawson, R.; Shoptaw, S.; Ling, W. Management of methamphetamine abuse and dependence. Curr. Psychiatry Rep., 2006, 8(5), 345-354.
[http://dx.doi.org/10.1007/s11920-006-0035-x] [PMID: 16968614]
[38]
Reichel, C.M.; See, R.E. Modafinil effects on reinstatement of methamphetamine seeking in a rat model of relapse. Psychopharmacology, 2010, 210(3), 337-346.
[http://dx.doi.org/10.1007/s00213-010-1828-5] [PMID: 20352413]
[39]
Holtz, N.A.; Lozama, A.; Prisinzano, T.E.; Carroll, M.E. Reinstatement of methamphetamine seeking in male and female rats treated with modafinil and allopregnanolone. Drug Alcohol Depend., 2012, 120(1-3), 233-237.
[http://dx.doi.org/10.1016/j.drugalcdep.2011.07.010] [PMID: 21820819]
[40]
Reichel, C.M.; Gilstrap, M.G.; Ramsey, L.A.; See, R.E. Modafinil restores methamphetamine induced object-in-place memory deficits in rats independent of glutamate N -methyl- d -aspartate receptor expression. Drug Alcohol Depend., 2014, 134, 115-122.
[http://dx.doi.org/10.1016/j.drugalcdep.2013.09.018] [PMID: 24120858]
[41]
Kalechstein, A.D.; De La Garza, R., II; Newton, T.F. Modafinil administration improves working memory in methamphetamine-dependent individuals who demonstrate baseline impairment. Am. J. Addict., 2010, 19(4), 340-4.
[http://dx.doi.org/10.1111/j.1521-0391.2010.00052.x] [PMID: 20653641]
[42]
Kalechstein, A.D.; Mahoney, J.J., III; Yoon, J.H.; Bennett, R.; De La Garza, R. II Modafinil, but not escitalopram, improves working memory and sustained attention in long-term, high-dose cocaine users. Neuropharmacology, 2013, 64, 472-478.
[http://dx.doi.org/10.1016/j.neuropharm.2012.06.064] [PMID: 22796108]
[43]
Béracochéa, D.; Celerier, A.; Peres, M.; Pierard, C. Enhancement of learning processes following an acute modafinil injection in mice. Pharmacol. Biochem. Behav., 2003, 76(3-4), 473-479.
[http://dx.doi.org/10.1016/j.pbb.2003.09.007] [PMID: 14643846]
[44]
Béracochéa, D.; Cagnard, B.; Célérier, A.; le Merrer, J.; Pérès, M.; Piérard, C. First evidence of a delay-dependent working memory-enhancing effect of modafinil in mice. Neuroreport, 2001, 12(2), 375-378.
[http://dx.doi.org/10.1097/00001756-200102120-00038] [PMID: 11209953]
[45]
Fernandes, H.A.; Zanin, K.A.; Patti, C.L.; Wuo-Silva, R.; Carvalho, R.C.; Fernandes-Santos, L.; Bittencourt, L.R.A.; Tufik, S.; Frussa-Filho, R. Inhibitory effects of modafinil on emotional memory in mice. Neuropharmacology, 2013, 64, 365-370.
[http://dx.doi.org/10.1016/j.neuropharm.2012.06.058] [PMID: 22771974]
[46]
Pierard, C.; Liscia, P.; Chauveau, F.; Coutan, M.; Corio, M.; Krazem, A.; Beracochea, D. Differential effects of total sleep deprivation on contextual and spatial memory: Modulatory effects of modafinil. Pharmacol. Biochem. Behav., 2011, 97(3), 399-405.
[http://dx.doi.org/10.1016/j.pbb.2010.09.016] [PMID: 20883715]
[47]
Moreira, K.M.; Ferreira, T.L.; Hipolide, D.C.; Fornari, R.V.; Tufik, S.; Oliveira, M.G.M. Modafinil prevents inhibitory avoidance memory deficit induced by sleep deprivation in rats. Sleep, 2010, 33(7), 990-993.
[http://dx.doi.org/10.1093/sleep/33.7.990] [PMID: 20614860]
[48]
Wisor, J.P.; Nishino, S.; Sora, I.; Uhl, G.H.; Mignot, E.; Edgar, D.M. Dopaminergic role in stimulant-induced wakefulness. J. Neurosci., 2001, 21(5), 1787-1794.
[http://dx.doi.org/10.1523/JNEUROSCI.21-05-01787.2001] [PMID: 11222668]
[49]
Ferraro, L.; Antonelli, T.; O’Connor, W.T.; Tanganelli, S.; Rambert, F.A.; Fuxe, K. Modafinil: An antinarcoleptic drug with a different neurochemical profile to d-amphetamine and dopamine uptake blockers. Biol. Psychiatry, 1997, 42(12), 1181-1183.
[http://dx.doi.org/10.1016/S0006-3223(97)00353-3] [PMID: 9426889]
[50]
D’Hooge, R.; De Deyn, P.P. Applications of the Morris water maze in the study of learning and memory. Brain Res. Brain Res. Rev., 2001, 36(1), 60-90.
[http://dx.doi.org/10.1016/S0165-0173(01)00067-4] [PMID: 11516773]
[51]
Clark, R.E.; Broadbent, N.J.; Squire, L.R. Hippocampus and remote spatial memory in rats. Hippocampus, 2005, 15(2), 260-272.
[http://dx.doi.org/10.1002/hipo.20056] [PMID: 15523608]
[52]
Shuman, T.; Wood, S.C.; Anagnostaras, S.G. Modafinil and memory: Effects of modafinil on Morris water maze learning and Pavlovian fear conditioning. Behav. Neurosci., 2009, 123(2), 257-266.
[http://dx.doi.org/10.1037/a0014366] [PMID: 19331449]
[53]
Piérard, C.; Liscia, P.; Philippin, J.; Mons, N.; Lafon, T.; Chauveau, F.; Vanbeers, P.; Drouet, I.; Serra, A.; Jouanin, J.; Béracochéa, D. Modafinil restores memory performance and neural activity impaired by sleep deprivation in mice. Pharmacol. Biochem. Behav., 2007, 88(1), 55-63.
[http://dx.doi.org/10.1016/j.pbb.2007.07.006] [PMID: 17698177]
[54]
Béracochéa, D.; Liscia, P.; Tronche, C.; Chauveau, F.; Jouanin, J.C.; Piérard, C. Stress modulation of the memory retrograde-enhancing effects of the awakening drug modafinil in mice. Psychopharmacology, 2008, 196(1), 1-13.
[http://dx.doi.org/10.1007/s00213-007-0915-8] [PMID: 17934722]
[55]
Piérard, C.; Liscia, P.; Valleau, M.; Drouet, I.; Chauveau, F.; Huart, B.; Bonneau, D.; Jouanin, J.C.; Beaumont, M.; Béracochéa, D. Modafinil-induced modulation of working memory and plasma corticosterone in chronically-stressed mice. Pharmacol. Biochem. Behav., 2006, 83(1), 1-8.
[http://dx.doi.org/10.1016/j.pbb.2005.11.018] [PMID: 16439006]
[56]
Boutrel, B.; Koob, G.F. What keeps us awake: The neuropharmacology of stimulants and wakefulness-promoting medications. Sleep, 2004, 27(6), 1181-1194.
[http://dx.doi.org/10.1093/sleep/27.6.1181] [PMID: 15532213]
[57]
Pigeau, R.; Naitoh, P.; Buguet, A.; McCANN, C.; Baranski, J.; Taylor, M.; Thompson, M.; Mack, I. Modafinil, d-amphetamine and placebo during 64 hours of sustained mental work. I. Effects on mood, fatigue, cognitive performance and body temperature. J. Sleep Res., 1995, 4(4), 212-228.
[http://dx.doi.org/10.1111/j.1365-2869.1995.tb00172.x] [PMID: 10607161]
[58]
Turner, D.C.; Robbins, T.W.; Clark, L.; Aron, A.R.; Dowson, J.; Sahakian, B.J. Cognitive enhancing effects of modafinil in healthy volunteers. Psychopharmacology, 2003, 165(3), 260-269.
[http://dx.doi.org/10.1007/s00213-002-1250-8] [PMID: 12417966]
[59]
Müller, U.; Steffenhagen, N.; Regenthal, R.; Bublak, P. Effects of modafinil on working memory processes in humans. Psychopharmacology, 2004, 177(1-2), 161-169.
[http://dx.doi.org/10.1007/s00213-004-1926-3] [PMID: 15221200]
[60]
Thorpy, M.J. Recently approved and upcoming treatments for narcolepsy. CNS Drugs, 2020, 34(1), 9-27.
[http://dx.doi.org/10.1007/s40263-019-00689-1] [PMID: 31953791]
[61]
Fulda, S.; Schulz, H. Cognitive dysfunction in sleep disorders. Sleep Med. Rev., 2001, 5(6), 423-445.
[http://dx.doi.org/10.1053/smrv.2001.0157] [PMID: 12531152]
[62]
Hood, B.; Bruck, D. Sleepiness and performance in narcolepsy. J. Sleep Res., 1996, 5(2), 128-134.
[http://dx.doi.org/10.1046/j.1365-2869.1996.00018.x] [PMID: 8795814]
[63]
Ellis, C.M.; Monk, C.; Simmons, A.; Lemmens, G.; Williams, S.C.R.; Brammer, M.; Bullmore, E.; Parkes, J.D. Functional magnetic resonance imaging neuroactivation studies in normal subjects and subjects with the narcoleptic syndrome. Actions of modafinil. J. Sleep Res., 1999, 8(2), 85-93.
[http://dx.doi.org/10.1046/j.1365-2869.1999.00142.x] [PMID: 10389090]
[64]
Allen, M.D.; Hedges, D.W.; Farrer, T.J.; Larson, M.J. Assessment of brain activity during memory encoding in a narcolepsy patient on and off modafinil using normative fMRI data. Neurocase, 2012, 18(1), 13-25.
[http://dx.doi.org/10.1080/13554794.2010.547508] [PMID: 21985031]
[65]
Béracochéa, D.; Celerier, A.; Borde, N.; Valleau, M.; Peres, M.; Pierard, C. Improvement of learning processes following chronic systemic administration of modafinil in mice. Pharmacol. Biochem. Behav., 2002, 73(3), 723-728.
[http://dx.doi.org/10.1016/S0091-3057(02)00877-8] [PMID: 12151049]
[66]
Rao, Y.; Xiao, P.; Xu, S. Effects of intrahippocampal aniracetam treatment on Y-maze avoidance learning performance and behavioral long-term potentiation in dentate gyrus in rat. Neurosci. Lett., 2001, 298(3), 183-186.
[http://dx.doi.org/10.1016/S0304-3940(00)01744-4] [PMID: 11165437]
[67]
Kleschevnikov, A.M.; Belichenko, P.V.; Faizi, M.; Jacobs, L.F.; Htun, K.; Shamloo, M.; Mobley, W.C. Deficits in cognition and synaptic plasticity in a mouse model of Down syndrome ameliorated by GABAB receptor antagonists. J. Neurosci., 2012, 32(27), 9217-9227.
[http://dx.doi.org/10.1523/JNEUROSCI.1673-12.2012] [PMID: 22764230]
[68]
Shanmugasundaram, B.; Korz, V.; Fendt, M.; Braun, K.; Lubec, G. Differential effects of wake promoting drug modafinil in aversive learning paradigms. Front. Behav. Neurosci., 2015, 9, 220.
[http://dx.doi.org/10.3389/fnbeh.2015.00220] [PMID: 26347629]
[69]
Burgos, H.; Castillo, A.; Flores, O.; Puentes, G.; Morgan, C.; Gatica, A.; Cofré, C.; Hernández, A.; Laurido, C.; Constandil, L. Effect of modafinil on learning performance and neocortical long-term potentiation in rats. Brain Res. Bull., 2010, 83(5), 238-244.
[http://dx.doi.org/10.1016/j.brainresbull.2010.08.010] [PMID: 20800665]
[70]
Ghahremani, D.G.; Tabibnia, G.; Monterosso, J.; Hellemann, G.; Poldrack, R.A.; London, E.D. Effect of modafinil on learning and task-related brain activity in methamphetamine-dependent and healthy individuals. Neuropsychopharmacology, 2011, 36(5), 950-959.
[http://dx.doi.org/10.1038/npp.2010.233] [PMID: 21289606]
[71]
Gilleen, J.; Michalopoulou, P.G.; Reichenberg, A.; Drake, R.; Wykes, T.; Lewis, S.W.; Kapur, S. Modafinil combined with cognitive training is associated with improved learning in healthy volunteers--a randomised controlled trial. Eur. Neuropsychopharmacol., 2014, 24(2014), 529-539.
[72]
Grady, S.; Aeschbach, D.; Wright, K.P., Jr; Czeisler, C.A. Effect of modafinil on impairments in neurobehavioral performance and learning associated with extended wakefulness and circadian misalignment. Neuropsychopharmacology, 2010, 35(9), 1910-1920.
[http://dx.doi.org/10.1038/npp.2010.63] [PMID: 20505660]

Rights & Permissions Print Cite
© 2024 Bentham Science Publishers | Privacy Policy