Generic placeholder image

CNS & Neurological Disorders - Drug Targets

Editor-in-Chief

ISSN (Print): 1871-5273
ISSN (Online): 1996-3181

Review Article

Mechanisms Involved in Neuroprotective Effects of Transcranial Magnetic Stimulation

Author(s): Javier Caballero-Villarraso*, Francisco J. Medina, Begoña M. Escribano, Eduardo Agüera, Abel Santamaría, Alvaro Pascual-Leone and Isaac Túnez*

Volume 21, Issue 7, 2022

Published on: 09 August, 2021

Page: [557 - 573] Pages: 17

DOI: 10.2174/1871527320666210809121922

Price: $65

Open Access Journals Promotions 2
conference banner
Abstract

Transcranial Magnetic Stimulation (TMS) is widely used in neurophysiology to study cortical excitability. Research over the last few decades has highlighted its added value as a potential therapeutic tool in the treatment of a broad range of psychiatric disorders. More recently, a number of studies have reported beneficial and therapeutic effects for TMS in neurodegenerative conditions and strokes. Yet, despite its recognised clinical applications and considerable research using animal models, the molecular and physiological mechanisms through which TMS exerts its beneficial and therapeutic effects remain unclear. They are thought to involve biochemical-molecular events affecting membrane potential and gene expression. In this aspect, the dopaminergic system plays a special role. This is the most directly and selectively modulated neurotransmitter system, producing an increase in the flux of dopamine (DA) in various areas of the brain after the application of repetitive TMS (rTMS). Other neurotransmitters, such as glutamate and gamma-aminobutyric acid (GABA) have shown a paradoxical response to rTMS. In this way, their levels increased in the hippocampus and striatum but decreased in the hypothalamus and remained unchanged in the mesencephalon. Similarly, there are sufficient evidence that TMS up-regulates the gene expression of BDNF (one of the main brain neurotrophins). Something similar occurs with the expression of genes such as c-Fos and zif268 that encode trophic and regenerative action neuropeptides. Consequently, the application of TMS can promote the release of molecules involved in neuronal genesis and maintenance. This capacity may mean that TMS becomes a useful therapeutic resource to antagonize processes that underlie the previously mentioned neurodegenerative conditions.

Keywords: Neurochemical mechanisms, biochemical pathways, cell processes, neuroplasticity, transcranial magnetic stimulation, psychiatric disorders.

Graphical Abstract
[1]
Rossi S, Hallett M, Rossini PM, Pascual-Leone A. Safety, ethical considerations, and application guidelines for the use of transcranial magnetic stimulation in clinical practice and research. Clin Neurophysiol 2009; 120(12): 2008-39.
[http://dx.doi.org/10.1016/j.clinph.2009.08.016] [PMID: 19833552]
[2]
Torres CV, López-Manzanares L, Pulido-Rivas P, Iza-Vallejo B, Pérez S, Navas-García M. Bases of deep brain stimulation. Rev Neurol 2020; 70(8): 293-9.
[PMID: 32242336]
[3]
Antal A, Alekseichuk I, Bikson M, et al. Low intensity transcranial electric stimulation: Safety, ethical, legal regulatory and application guidelines. Clin Neurophysiol 2017; 128(9): 1774-809.
[http://dx.doi.org/10.1016/j.clinph.2017.06.001] [PMID: 28709880]
[4]
Impey D, de la Salle S, Knott V. Assessment of anodal and cathodal transcranial direct current stimulation (tDCS) on MMN-indexed auditory sensory processing. Brain Cogn 2016; 105: 46-54.
[http://dx.doi.org/10.1016/j.bandc.2016.03.006] [PMID: 27054908]
[5]
Medina FJ, Túnez I. Mechanisms and pathways underlying the therapeutic effect of transcranial magnetic stimulation. Rev Neurosci 2013; 24(5): 507-25.
[http://dx.doi.org/10.1515/revneuro-2013-0024] [PMID: 24077617]
[6]
Agüera E, Caballero-Villarraso J, Feijóo M, et al. Clinical and neurochemical effects of transcranial magnetic stimulation (tms) in multiple sclerosis: a study protocol for a randomized clinical trial. Front Neurol 2020; 11: 750.
[http://dx.doi.org/10.3389/fneur.2020.00750] [PMID: 32849212]
[7]
Lefaucheur JP. Principles of therapeutic use of transcranial and epidural cortical stimulation. Clin Neurophysiol 2008; 119(10): 2179-84.
[http://dx.doi.org/10.1016/j.clinph.2008.07.007] [PMID: 18762449]
[8]
Sebastián JL, Muñoz-San Marin S, Sancho-Ruiz M, Miranda JM. Medición de radiaciones en seres vivos. Investig Cienc 2006; 353: 46-55.
[9]
McHughen SA, Pearson-Fuhrhop K, Ngo VK, Cramer SC. Intense training overcomes effects of the Val66Met BDNF polymorphism on short-term plasticity. Exp Brain Res 2011; 213(4): 415-22.
[http://dx.doi.org/10.1007/s00221-011-2791-z] [PMID: 21769545]
[10]
Mori F, Ribolsi M, Kusayanagi H, et al. Genetic variants of the NMDA receptor influence cortical excitability and plasticity in humans. J Neurophysiol 2011; 106(4): 1637-43.
[http://dx.doi.org/10.1152/jn.00318.2011] [PMID: 21753020]
[11]
Mori F, Ribolsi M, Kusayanagi H, et al. TRPV1 channels regulate cortical excitability in humans. J Neurosci 2012; 32(3): 873-9.
[http://dx.doi.org/10.1523/JNEUROSCI.2531-11.2012] [PMID: 22262885]
[12]
Cirillo J, Hughes J, Ridding M, Thomas PQ, Semmler JG. Differential modulation of motor cortex excitability in BDNF Met allele carriers following experimentally induced and use-dependent plasticity. Eur J Neurosci 2012; 36(5): 2640-9.
[http://dx.doi.org/10.1111/j.1460-9568.2012.08177.x] [PMID: 22694150]
[13]
Di Lazzaro V, Manganelli F, Dileone M, et al. The effects of prolonged cathodal direct current stimulation on the excitatory and inhibitory circuits of the ipsilateral and contralateral motor cortex. J Neural Transm (Vienna) 2012; 119(12): 1499-506.
[http://dx.doi.org/10.1007/s00702-012-0845-4] [PMID: 22711234]
[14]
Wassermann EM, Lisanby SH. Therapeutic application of repetitive transcranial magnetic stimulation: a review. Clin Neurophysiol 2001; 112(8): 1367-77.
[http://dx.doi.org/10.1016/S1388-2457(01)00585-5] [PMID: 11459676]
[15]
Green RM, Pascual-Leone A, Wasserman EM. Ethical guidelines for rTMS research. IRB 1997; 19(2): 1-7.
[http://dx.doi.org/10.2307/3563539] [PMID: 11655322]
[16]
Wassermann EM. Risk and safety of repetitive transcranial magnetic stimulation: report and suggested guidelines from the International Workshop on the Safety of Repetitive Transcranial Magnetic Stimulation, June 5-7, 1996. Electroencephalogr Clin Neurophysiol 1998; 108(1): 1-16.
[http://dx.doi.org/10.1016/S0168-5597(97)00096-8] [PMID: 9474057]
[17]
Demirtas-Tatlidede A, Freitas C, Cromer JR, et al. Safety and proof of principle study of cerebellar vermal theta burst stimulation in refractory schizophrenia. Schizophr Res 2010; 124(1-3): 91-100.
[http://dx.doi.org/10.1016/j.schres.2010.08.015] [PMID: 20817483]
[18]
Rossi S, Antal A, Bestmann S, et al. basis of this article began with a Consensus Statement from the IFCN Workshop on “Present, Future of TMS: Safety, Ethical Guidelines”, Siena, October 17-20, 2018, updating through April 2020. Safety and recommendations for TMS use in healthy subjects and patient populations, with updates on training, ethical and regulatory issues: Expert Guidelines. Clin Neurophysiol 2021; 132(1): 269-306.
[http://dx.doi.org/10.1016/j.clinph.2020.10.003] [PMID: 33243615]
[19]
Maeda F, Keenan JP, Tormos JM, Topka H, Pascual-Leone A. Interindividual variability of the modulatory effects of repetitive transcranial magnetic stimulation on cortical excitability. Exp Brain Res 2000; 133(4): 425-30.
[http://dx.doi.org/10.1007/s002210000432] [PMID: 10985677]
[20]
Keller A, Miyashita E, Asanuma H. Minimal stimulus parameters and the effects of hyperpolarization on the induction of long-term potentiation in the cat motor cortex. Exp Brain Res 1991; 87(2): 295-302.
[http://dx.doi.org/10.1007/BF00231846] [PMID: 1769383]
[21]
Hoogendam JM, Ramakers GM, Di Lazzaro V. Physiology of repetitive transcranial magnetic stimulation of the human brain. Brain Stimul 2010; 3(2): 95-118.
[http://dx.doi.org/10.1016/j.brs.2009.10.005] [PMID: 20633438]
[22]
Barker AT, Jalinous R, Freeston IL. Non-invasive magnetic stimulation of human motor cortex. Lancet 1985; 1(8437): 1106-7.
[http://dx.doi.org/10.1016/S0140-6736(85)92413-4] [PMID: 2860322]
[23]
Sommer M, Tergau F, Wischer S, Paulus W. Paired-pulse repetitive transcranial magnetic stimulation of the human motor cortex. Exp Brain Res 2001; 139(4): 465-72.
[http://dx.doi.org/10.1007/s002210100791] [PMID: 11534871]
[24]
Khedr EM, Gilio F, Rothwell J. Effects of low frequency and low intensity repetitive paired pulse stimulation of the primary motor cortex. Clin Neurophysiol 2004; 115(6): 1259-63.
[http://dx.doi.org/10.1016/j.clinph.2003.08.025] [PMID: 15134692]
[25]
Thickbroom GW, Byrnes ML, Edwards DJ, Mastaglia FL. Repetitive paired-pulse TMS at I-wave periodicity markedly increases corticospinal excitability: a new technique for modulating synaptic plasticity. Clin Neurophysiol 2006; 117(1): 61-6.
[http://dx.doi.org/10.1016/j.clinph.2005.09.010] [PMID: 16326137]
[26]
Hamada M, Terao Y, Hanajima R, et al. Bidirectional long-term motor cortical plasticity and metaplasticity induced by quadripulse transcranial magnetic stimulation. J Physiol 2008; 586(16): 3927-47.
[http://dx.doi.org/10.1113/jphysiol.2008.152793] [PMID: 18599542]
[27]
Hamada M, Hanajima R, Terao Y, et al. Quadro-pulse stimulation is more effective than paired-pulse stimulation for plasticity induction of the human motor cortex. Clin Neurophysiol 2007; 118(12): 2672-82.
[http://dx.doi.org/10.1016/j.clinph.2007.09.062] [PMID: 17977788]
[28]
Stefan K, Kunesch E, Cohen LG, Benecke R, Classen J. Induction of plasticity in the human motor cortex by paired associative stimulation. Brain 2000; 123(Pt 3): 572-84.
[http://dx.doi.org/10.1093/brain/123.3.572] [PMID: 10686179]
[29]
McKay D, Brooker R, Giacomin P, Ridding M, Miles T. Time course of induction of increased human motor cortex excitability by nerve stimulation. Neuroreport 2002; 13(10): 1271-3.
[http://dx.doi.org/10.1097/00001756-200207190-00011] [PMID: 12151785]
[30]
Medina FJ, Túnez I. Huntington’s disease: the value of transcranial meganetic stimulation. Curr Med Chem 2010; 17(23): 2482-91.
[http://dx.doi.org/10.2174/092986710791556078] [PMID: 20491647]
[31]
Zimerman M, Hummel FC. Non-invasive brain stimulation: enhancing motor and cognitive functions in healthy old subjects. Front Aging Neurosci 2010; 2: 149.
[http://dx.doi.org/10.3389/fnagi.2010.00149] [PMID: 21151809]
[32]
Fregni F, Pascual-Leone A. Technology insight: noninvasive brain stimulation in neurology-perspectives on the therapeutic potential of rTMS and tDCS. Nat Clin Pract Neurol 2007; 3(7): 383-93.
[http://dx.doi.org/10.1038/ncpneuro0530] [PMID: 17611487]
[33]
Cárdenas-Morales L, Nowak DA, Kammer T, Wolf RC, Schönfeldt-Lecuona C. Mechanisms and applications of theta-burst rTMS on the human motor cortex. Brain Topogr 2010; 22(4): 294-306.
[http://dx.doi.org/10.1007/s10548-009-0084-7] [PMID: 19288184]
[34]
Cho SS, Strafella AP. rTMS of the left dorsolateral prefrontal cortex modulates dopamine release in the ipsilateral anterior cingulate cortex and orbitofrontal cortex. PLoS One 2009; 4(8): 6725.
[http://dx.doi.org/10.1371/journal.pone.0006725] [PMID: 19696930]
[35]
Yang Y, Li L, Wang YG, et al. Acute neuroprotective effects of extremely low-frequency electromagnetic fields after traumatic brain injury in rats. Neurosci Lett 2012; 516(1): 15-20.
[http://dx.doi.org/10.1016/j.neulet.2012.03.022] [PMID: 22484017]
[36]
Tasset I, Pérez-Herrera A, Medina FJ, Arias-Carrión O, Drucker- Colín R, Túnez I. Extremely low-frequency electromagnetic fields activate the antioxidant pathway Nrf2 in a Huntington’s disease- like rat model. Brain Stimul 2013; 6(1): 84-6.
[http://dx.doi.org/10.1016/j.brs.2012.03.015] [PMID: 22537865]
[37]
Tasset I, Medina FJ, Jimena I, et al. Neuroprotective effects of extremely low-frequency electromagnetic fields on a Huntington’s disease rat model: effects on neurotrophic factors and neuronal density. Neuroscience 2012; 209: 54-63.
[http://dx.doi.org/10.1016/j.neuroscience.2012.02.034] [PMID: 22406415]
[38]
Martínez-Sámano J, Torres-Durán PV, Juárez-Oropeza MA, Verdugo-Díaz L. Effect of acute extremely low frequency electromagnetic field exposure on the antioxidant status and lipid levels in rat brain. Arch Med Res 2012; 43(3): 183-9.
[http://dx.doi.org/10.1016/j.arcmed.2012.04.003] [PMID: 22560984]
[39]
Cuccurazzu B, Leone L, Podda MV, et al. Exposure to extremely low-frequency (50 Hz) electromagnetic fields enhances adult hippocampal neurogenesis in C57BL/6 mice. Exp Neurol 2010; 226(1): 173-82.
[http://dx.doi.org/10.1016/j.expneurol.2010.08.022] [PMID: 20816824]
[40]
Varró P, Szemerszky R, Bárdos G, Világi I. Changes in synaptic efficacy and seizure susceptibility in rat brain slices following extremely low-frequency electromagnetic field exposure. Bioelectromagnetics 2009; 30(8): 631-40.
[http://dx.doi.org/10.1002/bem.20517] [PMID: 19572331]
[41]
Peinemann A, Reimer B, Löer C, et al. Long-lasting increase in corticospinal excitability after 1800 pulses of subthreshold 5 Hz repetitive TMS to the primary motor cortex. Clin Neurophysiol 2004; 115(7): 1519-26.
[http://dx.doi.org/10.1016/j.clinph.2004.02.005] [PMID: 15203053]
[42]
Nyffeler T, Wurtz P, Lüscher HR, et al. Repetitive TMS over the human oculomotor cortex: comparison of 1-Hz and theta burst stimulation. Neurosci Lett 2006; 409(1): 57-60.
[http://dx.doi.org/10.1016/j.neulet.2006.09.011] [PMID: 17049743]
[43]
Abraham WC. How long will long-term potentiation last? Philos Trans R Soc Lond B Biol Sci 2003; 358(1432): 735-44.
[http://dx.doi.org/10.1098/rstb.2002.1222] [PMID: 12740120]
[44]
Arias-Carrión O. Basic mechanisms of rTMS: Implications in Parkinson’s disease. Int Arch Med 2008; 1(1): 2.
[http://dx.doi.org/10.1186/1755-7682-1-2] [PMID: 18471317]
[45]
Keck ME, Sillaber I, Ebner K, et al. Acute transcranial magnetic stimulation of frontal brain regions selectively modulates the release of vasopressin, biogenic amines and amino acids in the rat brain. Eur J Neurosci 2000; 12(10): 3713-20.
[http://dx.doi.org/10.1046/j.1460-9568.2000.00243.x] [PMID: 11029641]
[46]
Ben-Shachar D, Belmaker RH, Grisaru N, Klein E. Transcranial magnetic stimulation induces alterations in brain monoamines. J Neural Transm (Vienna) 1997; 104(2-3): 191-7.
[http://dx.doi.org/10.1007/BF01273180] [PMID: 9203081]
[47]
Taber MT, Fibiger HC. Electrical stimulation of the prefrontal cortex increases dopamine release in the nucleus accumbens of the rat: modulation by metabotropic glutamate receptors. J Neurosci 1995; 15(5 Pt 2): 3896-904.
[http://dx.doi.org/10.1523/JNEUROSCI.15-05-03896.1995] [PMID: 7751954]
[48]
You ZB, Tzschentke TM, Brodin E, Wise RA. Electrical stimulation of the prefrontal cortex increases cholecystokinin, glutamate, and dopamine release in the nucleus accumbens: an in vivo microdialysis study in freely moving rats. J Neurosci 1998; 18(16): 6492-500.
[http://dx.doi.org/10.1523/JNEUROSCI.18-16-06492.1998] [PMID: 9698337]
[49]
Kuroda Y, Motohashi N, Ito H, et al. Effects of repetitive transcranial magnetic stimulation on [11C]raclopride binding and cognitive function in patients with depression. J Affect Disord 2006; 95(1-3): 35-42.
[http://dx.doi.org/10.1016/j.jad.2006.03.029] [PMID: 16781779]
[50]
Kanno M, Matsumoto M, Togashi H, Yoshioka M, Mano Y. Effects of acute repetitive transcranial magnetic stimulation on dopamine release in the rat dorsolateral striatum. J Neurol Sci 2004; 217(1): 73-81.
[http://dx.doi.org/10.1016/j.jns.2003.08.013] [PMID: 14675613]
[51]
Strafella AP, Paus T, Fraraccio M, Dagher A. Striatal dopamine release induced by repetitive transcranial magnetic stimulation of the human motor cortex. Brain 2003; 126(Pt 12): 2609-15.
[http://dx.doi.org/10.1093/brain/awg268] [PMID: 12937078]
[52]
Funamizu H, Ogiue-Ikeda M, Mukai H, Kawato S, Ueno S. Acute repetitive transcranial magnetic stimulation reactivates dopaminergic system in lesion rats. Neurosci Lett 2005; 383(1-2): 77-81.
[http://dx.doi.org/10.1016/j.neulet.2005.04.018] [PMID: 15882931]
[53]
Godlevskii LS, Kobolev EV. The effects of L-DOPA and transcranial magnetic stimulation on behavioral reactions in kindled rats. Neurosci Behav Physiol 2005; 35(3): 313-7.
[http://dx.doi.org/10.1007/s11055-005-0065-6] [PMID: 15875494]
[54]
Börnke Ch, Schulte T, Przuntek H, Müller T. Clinical effects of repetitive transcranial magnetic stimulation versus acute levodopa challenge in Parkinson’s disease. J Neural Transm Suppl 2004; (68): 61-7.
[http://dx.doi.org/10.1007/978-3-7091-0579-5_7] [PMID: 15354390]
[55]
Ohnishi T, Hayashi T, Okabe S, et al. Endogenous dopamine release induced by repetitive transcranial magnetic stimulation over the primary motor cortex: an [11C]raclopride positron emission tomography study in anesthetized macaque monkeys. Biol Psychiatry 2004; 55(5): 484-9.
[http://dx.doi.org/10.1016/j.biopsych.2003.09.016] [PMID: 15023576]
[56]
Pogarell O, Koch W, Pöpperl G, et al. Acute prefrontal rTMS increases striatal dopamine to a similar degree as D-amphetamine. Psychiatry Res 2007; 156(3): 251-5.
[http://dx.doi.org/10.1016/j.pscychresns.2007.05.002] [PMID: 17993266]
[57]
Khedr EM, Rothwell JC, Shawky OA, Ahmed MA, Foly N, Hamdy A. Dopamine levels after repetitive transcranial magnetic stimulation of motor cortex in patients with Parkinson’s disease: preliminary results. Mov Disord 2007; 22(7): 1046-50.
[http://dx.doi.org/10.1002/mds.21460] [PMID: 17575584]
[58]
Erhardt A, Sillaber I, Welt T, Müller MB, Singewald N, Keck ME. Repetitive transcranial magnetic stimulation increases the release of dopamine in the nucleus accumbens shell of morphine-sensitized rats during abstinence. Neuropsychopharmacology 2004; 29(11): 2074-80.
[http://dx.doi.org/10.1038/sj.npp.1300493] [PMID: 15187982]
[59]
Kendell SF, Krystal JH, Sanacora G. GABA and glutamate systems as therapeutic targets in depression and mood disorders. Expert Opin Ther Targets 2005; 9(1): 153-68.
[http://dx.doi.org/10.1517/14728222.9.1.153] [PMID: 15757488]
[60]
Yue L, Xiao-lin H, Tao S. The effects of chronic repetitive transcranial magnetic stimulation on glutamate and gamma-aminobutyric acid in rat brain. Brain Res 2009; 1260: 94-9.
[http://dx.doi.org/10.1016/j.brainres.2009.01.009] [PMID: 19401169]
[61]
Fitzgerald PB, Benitez J, Oxley T, Daskalakis JZ, de Castella AR, Kulkarni J. A study of the effects of lorazepam and dextromethorphan on the response to cortical 1 Hz repetitive transcranial magnetic stimulation. Neuroreport 2005; 16(13): 1525-8.
[http://dx.doi.org/10.1097/01.wnr.0000177005.14108.f1] [PMID: 16110283]
[62]
Stagg CJ, Wylezinska M, Matthews PM, et al. Neurochemical effects of theta burst stimulation as assessed by magnetic resonance spectroscopy. J Neurophysiol 2009; 101(6): 2872-7.
[http://dx.doi.org/10.1152/jn.91060.2008] [PMID: 19339458]
[63]
Aleman A, Sommer IE, Kahn RS. Efficacy of slow repetitive transcranial magnetic stimulation in the treatment of resistant auditory hallucinations in schizophrenia: a meta-analysis. J Clin Psychiatry 2007; 68(3): 416-21.
[http://dx.doi.org/10.4088/JCP.v68n0310] [PMID: 17388712]
[64]
Fregni F, Potvin K, Dasilva D, et al. Clinical effects and brain metabolic correlates in non-invasive cortical neuromodulation for visceral pain. Eur J Pain 2011; 15(1): 53-60.
[http://dx.doi.org/10.1016/j.ejpain.2010.08.002] [PMID: 20822942]
[65]
Levkovitz Y, Harel EV, Roth Y, et al. Deep transcranial magnetic stimulation over the prefrontal cortex: evaluation of antidepressant and cognitive effects in depressive patients. Brain Stimul 2009; 2(4): 188-200.
[http://dx.doi.org/10.1016/j.brs.2009.08.002] [PMID: 20633419]
[66]
George MS, Lisanby SH, Avery D, et al. Daily left prefrontal transcranial magnetic stimulation therapy for major depressive disorder: a sham-controlled randomized trial. Arch Gen Psychiatry 2010; 67(5): 507-16.
[http://dx.doi.org/10.1001/archgenpsychiatry.2010.46] [PMID: 20439832]
[67]
Praharaj SK, Ram D, Arora M. Efficacy of high frequency (rapid) suprathreshold repetitive transcranial magnetic stimulation of right prefrontal cortex in bipolar mania: a randomized sham controlled study. J Affect Disord 2009; 117(3): 146-50.
[http://dx.doi.org/10.1016/j.jad.2008.12.020] [PMID: 19178948]
[68]
Vieyra-Reyes P, Mineur YS, Picciotto MR, Túnez I, Vidaltamayo R, Drucker-Colín R. Antidepressant-like effects of nicotine and transcranial magnetic stimulation in the olfactory bulbectomy rat model of depression. Brain Res Bull 2008; 77(1): 13-8.
[http://dx.doi.org/10.1016/j.brainresbull.2008.05.007] [PMID: 18582540]
[69]
Kanno M, Matsumoto M, Togashi H, Yoshioka M, Mano Y. Effects of acute repetitive transcranial magnetic stimulation on extracellular serotonin concentration in the rat prefrontal cortex. J Pharmacol Sci 2003; 93(4): 451-7.
[http://dx.doi.org/10.1254/jphs.93.451] [PMID: 14737016]
[70]
Gur E, Lerer B, van de Kar LD, Newman ME. Chronic rTMS induces subsensitivity of post-synaptic 5-HT1A receptors in rat hypothalamus. Int J Neuropsychopharmacol 2004; 7(3): 335-40.
[http://dx.doi.org/10.1017/S1461145703003985] [PMID: 14741057]
[71]
Levkovitz Y, Grisaru N, Segal M. Transcranial magnetic stimulation and antidepressive drugs share similar cellular effects in rat hippocampus. Neuropsychopharmacology 2001; 24(6): 608-16.
[http://dx.doi.org/10.1016/S0893-133X(00)00244-X] [PMID: 11331140]
[72]
Tasset I, Drucker-Colín R, Peña J, et al. Antioxidant-like effects and protective action of transcranial magnetic stimulation in depression caused by olfactory bulbectomy. Neurochem Res 2010; 35(8): 1182-7.
[http://dx.doi.org/10.1007/s11064-010-0172-9] [PMID: 20428940]
[73]
Kole MH, Fuchs E, Ziemann U, Paulus W, Ebert U. Changes in 5-HT1A and NMDA binding sites by a single rapid transcranial magnetic stimulation procedure in rats. Brain Res 1999; 826(2): 309-12.
[http://dx.doi.org/10.1016/S0006-8993(99)01257-3] [PMID: 10224311]
[74]
Ben-Shachar D, Gazawi H, Riboyad-Levin J, Klein E. Chronic repetitive transcranial magnetic stimulation alters beta-adrenergic and 5-HT2 receptor characteristics in rat brain. Brain Res 1999; 816(1): 78-83.
[http://dx.doi.org/10.1016/S0006-8993(98)01119-6] [PMID: 9878693]
[75]
Karege F, Perret G, Bondolfi G, Schwald M, Bertschy G, Aubry JM. Decreased serum brain-derived neurotrophic factor levels in major depressed patients. Psychiatry Res 2002; 109(2): 143-8.
[http://dx.doi.org/10.1016/S0165-1781(02)00005-7] [PMID: 11927139]
[76]
Gottschalk W, Pozzo-Miller LD, Figurov A, Lu B. Presynaptic modulation of synaptic transmission and plasticity by brain-derived neurotrophic factor in the developing hippocampus. J Neurosci 1998; 18(17): 6830-9.
[http://dx.doi.org/10.1523/JNEUROSCI.18-17-06830.1998] [PMID: 9712654]
[77]
Klintsova AY, Dickson E, Yoshida R, Greenough WT. Altered expression of BDNF and its high-affinity receptor TrkB in response to complex motor learning and moderate exercise. Brain Res 2004; 1028(1): 92-104.
[http://dx.doi.org/10.1016/j.brainres.2004.09.003] [PMID: 15518646]
[78]
Nibuya M, Morinobu S, Duman RS. Regulation of BDNF and trkB mRNA in rat brain by chronic electroconvulsive seizure and antidepressant drug treatments. J Neurosci 1995; 15(11): 7539-47.
[http://dx.doi.org/10.1523/JNEUROSCI.15-11-07539.1995] [PMID: 7472505]
[79]
Müller MB, Toschi N, Kresse AE, Post A, Keck ME. Long-term repetitive transcranial magnetic stimulation increases the expression of brain-derived neurotrophic factor and cholecystokinin mRNA, but not neuropeptide tyrosine mRNA in specific areas of rat brain. Neuropsychopharmacology 2000; 23(2): 205-15.
[http://dx.doi.org/10.1016/S0893-133X(00)00099-3] [PMID: 10882847]
[80]
Zhang X, Mei Y, Liu C, Yu S. Effect of transcranial magnetic stimulation on the expression of c-Fos and brain-derived neurotrophic factor of the cerebral cortex in rats with cerebral infarct. J Huazhong Univ Sci Technolog Med Sci 2007; 27(4): 415-8.
[http://dx.doi.org/10.1007/s11596-007-0416-3] [PMID: 17828499]
[81]
Lang UE, Hellweg R, Gallinat J, Bajbouj M. Acute prefrontal cortex transcranial magnetic stimulation in healthy volunteers: no effects on brain-derived neurotrophic factor (BDNF) concentrations in serum. J Affect Disord 2008; 107(1-3): 255-8.
[http://dx.doi.org/10.1016/j.jad.2007.08.008] [PMID: 17825920]
[82]
Cheeran B, Talelli P, Mori F, et al. A common polymorphism in the brain-derived neurotrophic factor gene (BDNF) modulates human cortical plasticity and the response to rTMS. J Physiol 2008; 586(23): 5717-25.
[http://dx.doi.org/10.1113/jphysiol.2008.159905] [PMID: 18845611]
[83]
Bocchio-Chiavetto L, Miniussi C, Zanardini R, et al. 5-HTTLPR and BDNF Val66Met polymorphisms and response to rTMS treatment in drug resistant depression. Neurosci Lett 2008; 437(2): 130-4.
[http://dx.doi.org/10.1016/j.neulet.2008.04.005] [PMID: 18450378]
[84]
Wang HY, Crupi D, Liu J, et al. Repetitive transcranial magnetic stimulation enhances BDNF-TrkB signaling in both brain and lymphocyte. J Neurosci 2011; 31(30): 11044-54.
[http://dx.doi.org/10.1523/JNEUROSCI.2125-11.2011] [PMID: 21795553]
[85]
Sun P, Wang F, Wang L, et al. Increase in cortical pyramidal cell excitability accompanies depression-like behavior in mice: a transcranial magnetic stimulation study. J Neurosci 2011; 31(45): 16464-72.
[http://dx.doi.org/10.1523/JNEUROSCI.1542-11.2011] [PMID: 22072696]
[86]
Mix ABA, Eysel UT, Funke K. The effect of chronic transcranial theta burst magnetic stimulation on an associative tactile learning rat in tha rat. Brain Stimul 2008; 1(3): 282.
[http://dx.doi.org/10.1016/j.brs.2008.06.251]
[87]
Ji RR, Schlaepfer TE, Aizenman CD, et al. Repetitive transcranial magnetic stimulation activates specific regions in rat brain. Proc Natl Acad Sci USA 1998; 95(26): 15635-40.
[http://dx.doi.org/10.1073/pnas.95.26.15635] [PMID: 9861022]
[88]
Hausmann A, Weis C, Marksteiner J, Hinterhuber H, Humpel C. Chronic repetitive transcranial magnetic stimulation enhances c- fos in the parietal cortex and hippocampus. Brain Res Mol Brain Res 2000; 76(2): 355-62.
[http://dx.doi.org/10.1016/S0169-328X(00)00024-3] [PMID: 10762712]
[89]
Aydin-Abidin S, Trippe J, Funke K, Eysel UT, Benali A. High- and low-frequency repetitive transcranial magnetic stimulation differentially activates c-Fos and zif268 protein expression in the rat brain. Exp Brain Res 2008; 188(2): 249-61.
[http://dx.doi.org/10.1007/s00221-008-1356-2] [PMID: 18385988]
[90]
Peretto P, Merighi A, Fasolo A, Bonfanti L. The subependymal layer in rodents: a site of structural plasticity and cell migration in the adult mammalian brain. Brain Res Bull 1999; 49(4): 221-43.
[http://dx.doi.org/10.1016/S0361-9230(99)00037-4] [PMID: 10424843]
[91]
Gage FH. Neurogenesis in the adult brain. J Neurosci 2002; 22(3): 612-3.
[http://dx.doi.org/10.1523/JNEUROSCI.22-03-00612.2002] [PMID: 11826087]
[92]
Alvarez-Buylla A, Lim DA. For the long run: maintaining germinal niches in the adult brain. Neuron 2004; 41(5): 683-6.
[http://dx.doi.org/10.1016/S0896-6273(04)00111-4] [PMID: 15003168]
[93]
Arias-Carrión O, Drucker-Colín R. Neurogenesis as a therapeutic strategy to regenerate central nervous system. Rev Neurol 2007; 45(12): 739-45.
[PMID: 18075989]
[94]
Arias-Carrión O, Olivares-Buñuelos T, Drucker-Colín R. Neurogenesis in the adult brain. Rev Neurol 2007; 44(9): 541-50.
[PMID: 17492613]
[95]
Jin K, Minami M, Lan JQ, et al. Neurogenesis in dentate subgranular zone and rostral subventricular zone after focal cerebral ischemia in the rat. Proc Natl Acad Sci USA 2001; 98(8): 4710-5.
[http://dx.doi.org/10.1073/pnas.081011098] [PMID: 11296300]
[96]
Arvidsson A, Collin T, Kirik D, Kokaia Z, Lindvall O. Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 2002; 8(9): 963-70.
[http://dx.doi.org/10.1038/nm747] [PMID: 12161747]
[97]
Yamashita T, Ninomiya M, Hernández Acosta P, et al. Subventricular zone-derived neuroblasts migrate and differentiate into mature neurons in the post-stroke adult striatum. J Neurosci 2006; 26(24): 6627-36.
[http://dx.doi.org/10.1523/JNEUROSCI.0149-06.2006] [PMID: 16775151]
[98]
Parent JM, Vexler ZS, Gong C, Derugin N, Ferriero DM. Rat forebrain neurogenesis and striatal neuron replacement after focal stroke. Ann Neurol 2002; 52(6): 802-13.
[http://dx.doi.org/10.1002/ana.10393] [PMID: 12447935]
[99]
Craig CG, Tropepe V, Morshead CM, Reynolds BA, Weiss S, van der Kooy D. In vivo growth factor expansion of endogenous subependymal neural precursor cell populations in the adult mouse brain. J Neurosci 1996; 16(8): 2649-58.
[http://dx.doi.org/10.1523/JNEUROSCI.16-08-02649.1996] [PMID: 8786441]
[100]
Fallon J, Reid S, Kinyamu R, et al. In vivo induction of massive proliferation, directed migration, and differentiation of neural cells in the adult mammalian brain. Proc Natl Acad Sci USA 2000; 97(26): 14686-91.
[http://dx.doi.org/10.1073/pnas.97.26.14686] [PMID: 11121069]
[101]
Kuhn HG, Winkler J, Kempermann G, Thal LJ, Gage FH. Epidermal growth factor and fibroblast growth factor-2 have different effects on neural progenitors in the adult rat brain. J Neurosci 1997; 17(15): 5820-9.
[http://dx.doi.org/10.1523/JNEUROSCI.17-15-05820.1997] [PMID: 9221780]
[102]
Zigova T, Pencea V, Wiegand SJ, Luskin MB. Intraventricular administration of BDNF increases the number of newly generated neurons in the adult olfactory bulb. Mol Cell Neurosci 1998; 11(4): 234-45.
[http://dx.doi.org/10.1006/mcne.1998.0684] [PMID: 9675054]
[103]
Shingo T, Sorokan ST, Shimazaki T, Weiss S. Erythropoietin regulates the in vitro and in vivo production of neuronal progenitors by mammalian forebrain neural stem cells. J Neurosci 2001; 21(24): 9733-43.
[http://dx.doi.org/10.1523/JNEUROSCI.21-24-09733.2001] [PMID: 11739582]
[104]
Curtis MA, Penney EB, Pearson AG, et al. Increased cell proliferation and neurogenesis in the adult human Huntington’s disease brain. Proc Natl Acad Sci USA 2003; 100(15): 9023-7.
[http://dx.doi.org/10.1073/pnas.1532244100] [PMID: 12853570]
[105]
Arias-Carrión O, Hernández-López S, Ibañez-Sandoval O, Bargas J, Hernández-Cruz A, Drucker-Colín R. Neuronal precursors within the adult rat subventricular zone differentiate into dopaminergic neurons after substantia nigra lesion and chromaffin cell transplant. J Neurosci Res 2006; 84(7): 1425-37.
[http://dx.doi.org/10.1002/jnr.21068] [PMID: 17006899]
[106]
Arias-Carrión O, Verdugo-Díaz L, Feria-Velasco A, et al. Neurogenesis in the subventricular zone following transcranial magnetic field stimulation and nigrostriatal lesions. J Neurosci Res 2004; 78(1): 16-28.
[http://dx.doi.org/10.1002/jnr.20235] [PMID: 15372495]
[107]
Drucker-Colín R, Verdugo-Díaz L, Méndez M, et al. Comparison between low frequency magnetic field stimulation and nerve growth factor treatment of cultured chromaffin cells, on neurite growth, noradrenaline release, excitable properties, and grafting in nigrostriatal lesioned rats. Mol Cell Neurosci 1994; 5(6): 485-98.
[http://dx.doi.org/10.1006/mcne.1994.1060] [PMID: 7704421]
[108]
Wang F, Geng X, Tao HY, Cheng Y. The restoration after repetitive transcranial magnetic stimulation treatment on cognitive ability of vascular dementia rats and its impacts on synaptic plasticity in hippocampal CA1 area. J Mol Neurosci 2010; 41(1): 145-55.
[http://dx.doi.org/10.1007/s12031-009-9311-7] [PMID: 19953343]
[109]
Hellmann J, Jüttner R, Roth C, et al. Repetitive magnetic stimulation of human-derived neuron-like cells activates cAMP-CREB pathway. Eur Arch Psychiatry Clin Neurosci 2012; 262(1): 87-91.
[http://dx.doi.org/10.1007/s00406-011-0217-3] [PMID: 21562895]
[110]
Schulz JB, Matthews RT, Jenkins BG, et al. Blockade of neuronal nitric oxide synthase protects against excitotoxicity in vivo. J Neurosci 1995; 15(12): 8419-29.
[http://dx.doi.org/10.1523/JNEUROSCI.15-12-08419.1995] [PMID: 8613773]
[111]
Tabrizi SJ, Workman J, Hart PE, et al. Mitochondrial dysfunction and free radical damage in the Huntington R6/2 transgenic mouse. Ann Neurol 2000; 47(1): 80-6.
[http://dx.doi.org/10.1002/1531-8249(200001)47:1<80::AID-ANA13>3.0.CO;2-K] [PMID: 10632104]
[112]
Pérez-Severiano F, Escalante B, Vergara P, Ríos C, Segovia J. Age-dependent changes in nitric oxide synthase activity and protein expression in striata of mice transgenic for the Huntington’s disease mutation. Brain Res 2002; 951(1): 36-42.
[http://dx.doi.org/10.1016/S0006-8993(02)03102-5] [PMID: 12231454]
[113]
Post A, Müller MB, Engelmann M, Keck ME. Repetitive transcranial magnetic stimulation in rats: evidence for a neuroprotective effect in vitro and in vivo. Eur J Neurosci 1999; 11(9): 3247-54.
[http://dx.doi.org/10.1046/j.1460-9568.1999.00747.x] [PMID: 10510188]
[114]
Arendash GW, Sanchez-Ramos J, Mori T, et al. Electromagnetic field treatment protects against and reverses cognitive impairment in Alzheimer’s disease mice. J Alzheimers Dis 2010; 19(1): 191-210.
[http://dx.doi.org/10.3233/JAD-2010-1228] [PMID: 20061638]
[115]
Túnez I, Drucker-Colín R, Jimena I, et al. Transcranial magnetic stimulation attenuates cell loss and oxidative damage in the striatum induced in the 3-nitropropionic model of Huntington’s disease. J Neurochem 2006; 97(3): 619-30.
[http://dx.doi.org/10.1111/j.1471-4159.2006.03724.x] [PMID: 16524377]
[116]
Túnez I, Montilla P, del Carmen Muñoz M, Medina FJ, Drucker- Colín R. Effect of transcranial magnetic stimulation on oxidative stress induced by 3-nitropropionic acid in cortical synaptosomes. Neurosci Res 2006; 56(1): 91-5.
[http://dx.doi.org/10.1016/j.neures.2006.05.012] [PMID: 16837092]
[117]
Coşkun S, Balabanli B, Canseven A, Seyhan N. Effects of continuous and intermittent magnetic fields on oxidative parameters in vivo. Neurochem Res 2009; 34(2): 238-43.
[http://dx.doi.org/10.1007/s11064-008-9760-3] [PMID: 18563561]
[118]
Torres-Duran PV, Ferreira-Hermosillo A, Juarez-Oropeza MA, Elias-Viñas D, Verdugo-Diaz L. Effects of whole body exposure to extremely low frequency electromagnetic fields (ELF-EMF) on serum and liver lipid levels, in the rat. Lipids Health Dis 2007; 6: 31.
[http://dx.doi.org/10.1186/1476-511X-6-31] [PMID: 18021407]
[119]
Ihara Y, Takata H, Tanabe Y, Nobukuni K, Hayabara T. Influence of repetitive transcranial magnetic stimulation on disease severity and oxidative stress markers in the cerebrospinal fluid of patients with spinocerebellar degeneration. Neurol Res 2005; 27(3): 310-3.
[http://dx.doi.org/10.1179/016164105X39897] [PMID: 15845214]
[120]
Agüera E, Caballero-Villarraso J, Feijóo M, et al. Impact of repetitive transcranial magnetic stimulation on neurocognition and oxidative stress in relapsing-remitting multiple sclerosis: a case report. Front Neurol 2020; 11: 817.
[http://dx.doi.org/10.3389/fneur.2020.00817] [PMID: 32903741]
[121]
Copple IM, Goldring CE, Kitteringham NR, Park BK. The Nrf2-Keap1 defence pathway: role in protection against drug-induced toxicity. Toxicology 2008; 246(1): 24-33.
[http://dx.doi.org/10.1016/j.tox.2007.10.029] [PMID: 18083283]
[122]
Calkins MJ, Johnson DA, Townsend JA, et al. The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease. Antioxid Redox Signal 2009; 11(3): 497-508.
[http://dx.doi.org/10.1089/ars.2008.2242] [PMID: 18717629]
[123]
Johnson JA, Johnson DA, Kraft AD, et al. The Nrf2-ARE pathway: an indicator and modulator of oxidative stress in neurodegeneration. Ann N Y Acad Sci 2008; 1147: 61-9.
[http://dx.doi.org/10.1196/annals.1427.036] [PMID: 19076431]
[124]
Eggler AL, Gay KA, Mesecar AD. Molecular mechanisms of natural products in chemoprevention: induction of cytoprotective enzymes by Nrf2. Mol Nutr Food Res 2008; 52(Suppl. 1): S84-94.
[http://dx.doi.org/10.1002/mnfr.200700249] [PMID: 18435489]
[125]
Li W, Khor TO, Xu C, et al. Activation of Nrf2-antioxidant signaling attenuates NFkappaB-inflammatory response and elicits apoptosis. Biochem Pharmacol 2008; 76(11): 1485-9.
[http://dx.doi.org/10.1016/j.bcp.2008.07.017] [PMID: 18694732]
[126]
Osburn WO, Kensler TW. Nrf2 signaling: an adaptive response pathway for protection against environmental toxic insults. Mutat Res 2008; 659(1-2): 31-9.
[http://dx.doi.org/10.1016/j.mrrev.2007.11.006] [PMID: 18164232]
[127]
Lin CW, Wu MJ, Liu IY, Su JD, Yen JH. Neurotrophic and cytoprotective action of luteolin in PC12 cells through ERK-dependent induction of Nrf2-driven HO-1 expression. J Agric Food Chem 2010; 58(7): 4477-86.
[http://dx.doi.org/10.1021/jf904061x] [PMID: 20302373]
[128]
Kosaka K, Mimura J, Itoh K, et al. Role of Nrf2 and p62/ZIP in the neurite outgrowth by carnosic acid in PC12h cells. J Biochem 2010; 147(1): 73-81.
[http://dx.doi.org/10.1093/jb/mvp149] [PMID: 19762340]
[129]
Feng HL, Yan L, Cui LY. Effects of repetitive transcranial magnetic stimulation on adenosine triphosphate content and microtubule associated protein-2 expression after cerebral ischemia-reperfusion injury in rat brain. Chin Med J (Engl) 2008; 121(14): 1307-12.
[http://dx.doi.org/10.1097/00029330-200807020-00012] [PMID: 18713553]
[130]
Pettigrew LC, Holtz ML, Craddock SD, Minger SL, Hall N, Geddes JW. Microtubular proteolysis in focal cerebral ischemia. J Cereb Blood Flow Metab 1996; 16(6): 1189-202.
[http://dx.doi.org/10.1097/00004647-199611000-00013] [PMID: 8898691]
[131]
Puka-Sundvall M, Wallin C, Gilland E, et al. Impairment of mitochondrial respiration after cerebral hypoxia-ischemia in immature rats: relationship to activation of caspase-3 and neuronal injury. Brain Res Dev Brain Res 2000; 125(1-2): 43-50.
[http://dx.doi.org/10.1016/S0165-3806(00)00111-5] [PMID: 11154759]
[132]
Ye H, Cotic M, Kang EE, Fehlings MG, Carlen PL. Transmembrane potential induced on the internal organelle by a time-varying magnetic field: a model study. J Neuroeng Rehabil 2010; 7: 12.
[http://dx.doi.org/10.1186/1743-0003-7-12] [PMID: 20170538]
[133]
Yang X, Song L, Liu Z. The effect of repetitive transcranial magnetic stimulation on a model rat of Parkinson’s disease. Neuroreport 2010; 21(4): 268-72.
[http://dx.doi.org/10.1097/WNR.0b013e328335b411] [PMID: 20087233]
[134]
Wang T, Pei Z, Zhang W, et al. MPP+-induced COX-2 activation and subsequent dopaminergic neurodegeneration. FASEB J 2005; 19(9): 1134-6.
[http://dx.doi.org/10.1096/fj.04-2457fje] [PMID: 15845609]
[135]
Liang X, Wu L, Wang Q, et al. Function of COX-2 and prostaglandins in neurological disease. J Mol Neurosci 2007; 33(1): 94-9.
[http://dx.doi.org/10.1007/s12031-007-0058-8] [PMID: 17901552]
[136]
Hunter RL, Dragicevic N, Seifert K, et al. Inflammation induces mitochondrial dysfunction and dopaminergic neurodegeneration in the nigrostriatal system. J Neurochem 2007; 100(5): 1375-86.
[http://dx.doi.org/10.1111/j.1471-4159.2006.04327.x] [PMID: 17254027]
[137]
Gao F, Wang S, Guo Y, et al. Protective effects of repetitive transcranial magnetic stimulation in a rat model of transient cerebral ischaemia: a microPET study. Eur J Nucl Med Mol Imaging 2010; 37(5): 954-61.
[http://dx.doi.org/10.1007/s00259-009-1342-3] [PMID: 20107794]
[138]
Fujiki M, Kobayashi H, Abe T, Kamida T. Repetitive transcranial magnetic stimulation for protection against delayed neuronal death induced by transient ischemia. J Neurosurg 2003; 99(6): 1063-9.
[http://dx.doi.org/10.3171/jns.2003.99.6.1063] [PMID: 14705735]
[139]
Yoon KJ, Lee YT, Han TR. Mechanism of functional recovery after repetitive transcranial magnetic stimulation (rTMS) in the subacute cerebral ischemic rat model: neural plasticity or anti-apoptosis? Exp Brain Res 2011; 214(4): 549-56.
[http://dx.doi.org/10.1007/s00221-011-2853-2] [PMID: 21904929]
[140]
Dileone M, Profice P, Pilato F, et al. Repetitive transcranial magnetic stimulation for ALS. CNS Neurol Disord Drug Targets 2010; 9(3): 331-4.
[http://dx.doi.org/10.2174/187152710791292620] [PMID: 20406177]
[141]
Abraham WC. Metaplasticity: tuning synapses and networks for plasticity. Nat Rev Neurosci 2008; 9(5): 387.
[http://dx.doi.org/10.1038/nrn2356] [PMID: 18401345]
[142]
Davis GW. Homeostatic control of neural activity: from phenomenology to molecular design. Annu Rev Neurosci 2006; 29: 307-23.
[http://dx.doi.org/10.1146/annurev.neuro.28.061604.135751] [PMID: 16776588]
[143]
Wankerl K, Weise D, Gentner R, Rumpf JJ, Classen J. L-type voltage-gated Ca2+ channels: a single molecular switch for long-term potentiation/long-term depression-like plasticity and activity-dependent metaplasticity in humans. J Neurosci 2010; 30(18): 6197-204.
[http://dx.doi.org/10.1523/JNEUROSCI.4673-09.2010] [PMID: 20445045]
[144]
Rioult-Pedotti MS, Friedman D, Donoghue JP. Learning-induced LTP in neocortex. Science 2000; 290(5491): 533-6.
[http://dx.doi.org/10.1126/science.290.5491.533] [PMID: 11039938]
[145]
Jung P, Ziemann U. Homeostatic and nonhomeostatic modulation of learning in human motor cortex. J Neurosci 2009; 29(17): 5597-604.
[http://dx.doi.org/10.1523/JNEUROSCI.0222-09.2009] [PMID: 19403826]
[146]
Ziemann U, Ilić TV, Pauli C, Meintzschel F, Ruge D. Learning modifies subsequent induction of long-term potentiation-like and long-term depression-like plasticity in human motor cortex. J Neurosci 2004; 24(7): 1666-72.
[http://dx.doi.org/10.1523/JNEUROSCI.5016-03.2004] [PMID: 14973238]
[147]
Malenka RC, Bear MF. LTP and LTD: an embarrassment of riches. Neuron 2004; 44(1): 5-21.
[http://dx.doi.org/10.1016/j.neuron.2004.09.012] [PMID: 15450156]
[148]
Ogiue-Ikeda M, Kawato S, Ueno S. The effect of repetitive transcranial magnetic stimulation on long-term potentiation in rat hippocampus depends on stimulus intensity. Brain Res 2003; 993(1-2): 222-6.
[http://dx.doi.org/10.1016/j.brainres.2003.09.009] [PMID: 14642850]
[149]
Bramham CR, Southard T, Sarvey JM, Herkenham M, Brady LS. Unilateral LTP triggers bilateral increases in hippocampal neurotrophin and trk receptor mRNA expression in behaving rats: evidence for interhemispheric communication. J Comp Neurol 1996; 368(3): 371-82.
[http://dx.doi.org/10.1002/(SICI)1096-9861(19960506)368:3<371::AID-CNE4>3.0.CO;2-2] [PMID: 8725345]
[150]
Morimoto K, Sato K, Sato S, Yamada N, Hayabara T. Time-dependent changes in neurotrophic factor mRNA expression after kindling and long-term potentiation in rats. Brain Res Bull 1998; 45(6): 599-605.
[http://dx.doi.org/10.1016/S0361-9230(97)00459-0] [PMID: 9566504]
[151]
Bekinschtein P, Cammarota M, Igaz LM, Bevilaqua LR, Izquierdo I, Medina JH. Persistence of long-term memory storage requires a late protein synthesis- and BDNF- dependent phase in the hippocampus. Neuron 2007; 53(2): 261-77.
[http://dx.doi.org/10.1016/j.neuron.2006.11.025] [PMID: 17224407]
[152]
Pastalkova E, Serrano P, Pinkhasova D, Wallace E, Fenton AA, Sacktor TC. Storage of spatial information by the maintenance mechanism of LTP. Science 2006; 313(5790): 1141-4.
[http://dx.doi.org/10.1126/science.1128657] [PMID: 16931766]
[153]
May A, Hajak G, Gänssbauer S, et al. Structural brain alterations following 5 days of intervention: dynamic aspects of neuroplasticity. Cereb Cortex 2007; 17(1): 205-10.
[http://dx.doi.org/10.1093/cercor/bhj138] [PMID: 16481564]
[154]
Draganski B, Gaser C, Busch V, Schuierer G, Bogdahn U, May A. Neuroplasticity: changes in grey matter induced by training. Nature 2004; 427(6972): 311-2.
[http://dx.doi.org/10.1038/427311a] [PMID: 14737157]
[155]
Ghiglieri V, Pendolino V, Sgobio C, Bagetta V, Picconi B, Calabresi P. Θ-burst stimulation and striatal plasticity in experimental parkinsonism. Exp Neurol 2012; 236(2): 395-8.
[http://dx.doi.org/10.1016/j.expneurol.2012.04.020] [PMID: 22569102]

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