N,N-dimethyltryptamine compound found in the hallucinogenic tea ayahuasca, regulates adult neurogenesis in vitro and in vivo.


Journal

Translational psychiatry
ISSN: 2158-3188
Titre abrégé: Transl Psychiatry
Pays: United States
ID NLM: 101562664

Informations de publication

Date de publication:
28 09 2020
Historique:
received: 21 04 2020
accepted: 07 09 2020
revised: 02 09 2020
entrez: 29 9 2020
pubmed: 30 9 2020
medline: 22 6 2021
Statut: epublish

Résumé

N,N-dimethyltryptamine (DMT) is a component of the ayahuasca brew traditionally used for ritual and therapeutic purposes across several South American countries. Here, we have examined, in vitro and vivo, the potential neurogenic effect of DMT. Our results demonstrate that DMT administration activates the main adult neurogenic niche, the subgranular zone of the dentate gyrus of the hippocampus, promoting newly generated neurons in the granular zone. Moreover, these mice performed better, compared to control non-treated animals, in memory tests, which suggest a functional relevance for the DMT-induced new production of neurons in the hippocampus. Interestingly, the neurogenic effect of DMT appears to involve signaling via sigma-1 receptor (S1R) activation since S1R antagonist blocked the neurogenic effect. Taken together, our results demonstrate that DMT treatment activates the subgranular neurogenic niche regulating the proliferation of neural stem cells, the migration of neuroblasts, and promoting the generation of new neurons in the hippocampus, therefore enhancing adult neurogenesis and improving spatial learning and memory tasks.

Identifiants

pubmed: 32989216
doi: 10.1038/s41398-020-01011-0
pii: 10.1038/s41398-020-01011-0
pmc: PMC7522265
doi:

Substances chimiques

Tea 0
N,N-Dimethyltryptamine WUB601BHAA

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

331

Subventions

Organisme : Ministerio de Economía y Competitividad (Ministry of Economy and Competitiveness)
ID : SAF2017-85199-P
Pays : International

Références

Soler, J. et al. Four weekly ayahuasca sessions lead to increases in “acceptance” capacities: a comparison study with a standard 8-week mindfulness training program. Front. Pharm. 9, 224 (2018).
doi: 10.3389/fphar.2018.00224
Bouso, J. C. et al. Long-term use of psychedelic drugs is associated with differences in brain structure and personality in humans. Eur. Neuropsychopharmacol. 25, 483–492 (2015).
pubmed: 25637267 doi: 10.1016/j.euroneuro.2015.01.008
Riba, J. et al. Increased frontal and paralimbic activation following ayahuasca, the pan-Amazonian inebriant. Psychopharmacology 186, 93–98 (2006).
pubmed: 16575552 doi: 10.1007/s00213-006-0358-7
Sanches, R. F. et al. Antidepressant effects of a single dose of ayahuasca in patients with recurrent depression: a SPECT Study. J. Clin. Psychopharmacol. 36, 77–81 (2016).
pubmed: 26650973 doi: 10.1097/JCP.0000000000000436
Axelrod, J. Enzymatic formation of psychotomimetic metabolites from normally occurring compounds. Science 134, 343 (1961).
pubmed: 13685339 doi: 10.1126/science.134.3475.343
Saavedra, J. M. & Axelrod, J. Psychotomimetic N-methylated tryptamines: formation in brain in vivo and in vitro. Science 175, 1365–1366 (1972).
pubmed: 5059565 doi: 10.1126/science.175.4028.1365
Su, T. P., Hayashi, T. & Vaupel, D. B. When the endogenous hallucinogenic trace amine N,N-dimethyltryptamine meets the sigma-1 receptor. Sci. Signal 2, pe12 (2009).
pubmed: 19278957 pmcid: 3155724 doi: 10.1126/scisignal.261pe12
Shen, H. W., Jiang, X. L., Winter, J. C. & Yu, A. M. Psychedelic 5-methoxy-N,N-dimethyltryptamine: metabolism, pharmacokinetics, drug interactions, and pharmacological actions. Curr. Drug Metab. 11, 659–666 (2010).
pubmed: 20942780 pmcid: 3028383 doi: 10.2174/138920010794233495
Frecska, E., Szabo, A., Winkelman, M. J., Luna, L. E. & McKenna, D. J. A possibly sigma-1 receptor mediated role of dimethyltryptamine in tissue protection, regeneration, and immunity. J. Neural. Transm. 120, 1295–1303 (2013).
pubmed: 23619992 doi: 10.1007/s00702-013-1024-y
Szabo, A., Kovacs, A., Frecska, E. & Rajnavolgyi, E. Psychedelic N,N-dimethyltryptamine and 5-methoxy-N,N-dimethyltryptamine modulate innate and adaptive inflammatory responses through the sigma-1 receptor of human monocyte-derived dendritic cells. PLoS ONE 9, e106533 (2014).
pubmed: 25171370 pmcid: 4149582
Beaton, J. M. & Morris, P. E. Ontogeny of N,N-dimethyltryptamine and related indolealkylamine levels in neonatal rats. Mech. Ageing Dev. 25, 343–347 (1984).
pubmed: 6588281
McKenna, D. & Riba, J. New world tryptamine hallucinogens and the neuroscience of ayahuasca. Curr. Top Behav. Neurosci. 36, 283–311 (2018).
Franzen, F. & Gross, H. Tryptamine, N,N-dimethyltryptamine, N,N-dimethyl-5-hydroxytryptamine and 5-methoxytryptamine in human blood and urine. Nature 206, 1052 (1965).
pubmed: 5839067 doi: 10.1038/2061052a0
Fontanilla, D. et al. The hallucinogen N,N-dimethyltryptamine (DMT) is an endogenous sigma-1 receptor regulator. Science 323, 934–937 (2009).
pubmed: 19213917 pmcid: 2947205 doi: 10.1126/science.1166127
Barker, S. A. N. N-Dimethyltryptamine (DMT), an endogenous hallucinogen: past, present, and future research to determine its role and function. Front. Neurosci. 12, 536 (2018).
pubmed: 30127713 pmcid: 6088236 doi: 10.3389/fnins.2018.00536
Dean, J. G. et al. Biosynthesis and extracellular concentrations of N,N-dimethyltryptamine (DMT) in mammalian brain. Sci. Rep. 9, 9333 (2019).
pubmed: 31249368 pmcid: 6597727 doi: 10.1038/s41598-019-45812-w
Riba, J. et al. Subjective effects and tolerability of the South American psychoactive beverage Ayahuasca in healthy volunteers. Psychopharmacol. (Berl.) 154, 85–95 (2001).
doi: 10.1007/s002130000606
Carbonaro, T. M. et al. The role of 5-HT2A, 5-HT 2C and mGlu2 receptors in the behavioral effects of tryptamine hallucinogens N,N-dimethyltryptamine and N,N-diisopropyltryptamine in rats and mice. Psychopharmacology 232, 275–284 (2015).
pubmed: 24985890 doi: 10.1007/s00213-014-3658-3
Hayashi, T. & Su, T. P. Sigma-1 receptor ligands: potential in the treatment of neuropsychiatric disorders. CNS Drugs 18, 269–284 (2004).
pubmed: 15089113 doi: 10.2165/00023210-200418050-00001
Rousseaux, C. G. & Greene, S. F. Sigma receptors [sigmaRs]: biology in normal and diseased states. J. Recept Signal Transduct. Res. 36, 327–388 (2016).
pubmed: 26056947
Weng, T. Y., Tsai, S. A. & Su, T. P. Roles of sigma-1 receptors on mitochondrial functions relevant to neurodegenerative diseases. J. Biomed. Sci. 24, 74 (2017).
pubmed: 28917260 pmcid: 5603014
Sha, S. et al. Sigma-1 receptor knockout impairs neurogenesis in dentate gyrus of adult hippocampus via down-regulation of NMDA receptors. CNS Neurosci. Ther. 19, 705–713 (2013).
pubmed: 23745740 pmcid: 6493366
Moriguchi, S. et al. Stimulation of the sigma-1 receptor by DHEA enhances synaptic efficacy and neurogenesis in the hippocampal dentate gyrus of olfactory bulbectomized mice. PLoS ONE 8, e60863 (2013).
pubmed: 23593332 pmcid: 3620380
Sha, S. et al. Sex-related neurogenesis decrease in hippocampal dentate gyrus with depressive-like behaviors in sigma-1 receptor knockout mice. Eur. Neuropsychopharmacol. 25, 1275–1286 (2015).
pubmed: 25983018
Alvarez-Buylla, A., Garcia-Verdugo, J. M. & Tramontin, A. D. A unified hypothesis on the lineage of neural stem cells. Nat. Rev. Neurosci. 2, 287–293 (2001).
pubmed: 11283751
Gage, F. H. Mammalian neural stem cells. Science 287, 1433–1438 (2000).
pubmed: 10688783
Ming, G. L. & Song, H. Adult neurogenesis in the mammalian central nervous system. Annu. Rev. Neurosci. 28, 223–250 (2005).
pubmed: 16022595
Altman, J. & Das, G. D. Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124, 319–335 (1965).
pubmed: 5861717
Kornack, D. R. & Rakic, P. Continuation of neurogenesis in the hippocampus of the adult macaque monkey. Proc. Natl Acad. Sci. USA 96, 5768–5773 (1999).
pubmed: 10318959
van Praag, H. et al. Functional neurogenesis in the adult hippocampus. Nature 415, 1030–1034 (2002).
pubmed: 11875571 doi: 10.1038/4151030a
Moreno-Jimenez, E. P. et al. Adult hippocampal neurogenesis is abundant in neurologically healthy subjects and drops sharply in patients with Alzheimer’s disease. Nat. Med. 25, 554–560 (2019).
pubmed: 30911133 doi: 10.1038/s41591-019-0375-9
Boldrini, M. et al. Human hippocampal neurogenesis persists throughout aging. Cell Stem Cell 22, 589–599. e585 (2018).
pubmed: 29625071 pmcid: 5957089 doi: 10.1016/j.stem.2018.03.015
Tobin, M. K. et al. Human hippocampal neurogenesis persists in aged adults and Alzheimer’s disease patients. Cell Stem Cell 24, 974–982. e973 (2019).
pubmed: 31130513 pmcid: 6608595 doi: 10.1016/j.stem.2019.05.003
Duque, A. & Spector, R. A balanced evaluation of the evidence for adult neurogenesis in humans: implication for neuropsychiatric disorders. Brain Struct. Funct. 224, 2281–2295 (2019).
pubmed: 31278571 pmcid: 6852840 doi: 10.1007/s00429-019-01917-6
Abrous, D. N., Koehl, M. & Le Moal, M. Adult neurogenesis: from precursors to network and physiology. Physiol. Rev. 85, 523–569 (2005).
pubmed: 15788705 doi: 10.1152/physrev.00055.2003
Hou, Y. et al. Ageing as a risk factor for neurodegenerative disease. Nat. Rev. Neurol. 15, 565–581 (2019).
pubmed: 31501588 doi: 10.1038/s41582-019-0244-7
Van Bulck, M., Sierra-Magro, A., Alarcon-Gil, J., Perez-Castillo, A. & Morales-Garcia, J. A. Novel Approaches for the treatment of Alzheimer’s and Parkinson’s disease. Int. J. Mol. Sci. 20, 719 (2019).
pmcid: 6386829 doi: 10.3390/ijms20030719 pubmed: 6386829
Scopa, C. et al. Impaired adult neurogenesis is an early event in Alzheimer’s disease neurodegeneration, mediated by intracellular Abeta oligomers. Cell Death Differ. 27, 934–948 (2020).
pubmed: 31591472 doi: 10.1038/s41418-019-0409-3
Hoglinger, G. U. et al. Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat. Neurosci. 7, 726–735 (2004).
pubmed: 15195095 doi: 10.1038/nn1265
Lie, D. C., Song, H., Colamarino, S. A., Ming, G. L. & Gage, F. H. Neurogenesis in the adult brain: new strategies for central nervous system diseases. Annu. Rev. Pharm. Toxicol. 44, 399–421 (2004).
doi: 10.1146/annurev.pharmtox.44.101802.121631
Kang, E., Wen, Z., Song, H., Christian, K. M. & Ming, G. L. Adult neurogenesis and psychiatric disorders. Cold Spring Harb. Perspect. Biol. 8, a019026 (2016).
pubmed: 26801682 pmcid: 5008067 doi: 10.1101/cshperspect.a019026
Kucharska-Mazur, J., Ratajczak, M. Z. & Samochowiec, J. Stem cells in psychiatry. Adv. Exp. Med. Biol. 1201, 159–174 (2019).
pubmed: 31898786 doi: 10.1007/978-3-030-31206-0_8
Planchez, B., Surget, A. & Belzung, C. Adult hippocampal neurogenesis and antidepressants effects. Curr. Opin. Pharm. 50, 88–95 (2020).
doi: 10.1016/j.coph.2019.11.009
Apple, D. M., Fonseca, R. S. & Kokovay, E. The role of adult neurogenesis in psychiatric and cognitive disorders. Brain Res. 1655, 270–276 (2017).
pubmed: 26801829 doi: 10.1016/j.brainres.2016.01.023
Micheli, L., Ceccarelli, M., D’Andrea, G. & Tirone, F. Depression and adult neurogenesis: positive effects of the antidepressant fluoxetine and of physical exercise. Brain Res. Bull. 143, 181–193 (2018).
pubmed: 30236533 doi: 10.1016/j.brainresbull.2018.09.002
Ly, C. et al. Psychedelics promote structural and functional neural plasticity. Cell Rep. 23, 3170–3182 (2018).
pubmed: 29898390 pmcid: 6082376 doi: 10.1016/j.celrep.2018.05.022
Li, Y. J. et al. Silibinin exerts antidepressant effects by improving neurogenesis through BDNF/TrkB pathway. Behav. Brain Res. 348, 184–191 (2018).
pubmed: 29680784 doi: 10.1016/j.bbr.2018.04.025
Park, S. C. Neurogenesis and antidepressant action. Cell Tissue Res. 377, 95–106 (2019).
pubmed: 31165247 doi: 10.1007/s00441-019-03043-5
Morales-Garcia, J. A. et al. The alkaloids of Banisteriopsis caapi, the plant source of the Amazonian hallucinogen Ayahuasca, stimulate adult neurogenesis in vitro. Sci. Rep. 7, 5309 (2017).
pubmed: 28706205 pmcid: 5509699 doi: 10.1038/s41598-017-05407-9
Kitanaka, N., Kitanaka, J. & Takemura, M. Repeated clorgyline treatment inhibits methamphetamine-induced behavioral sensitization in mice. Neurochem Res. 30, 445–451 (2005).
pubmed: 16076014
Indra, B. et al. Suppressive effect of nantenine, isolated from Nandina domestica Thunberg, on the 5-hydroxy-L-tryptophan plus clorgyline-induced head-twitch response in mice. Life Sci. 70, 2647–2656 (2002).
pubmed: 12269391
Morales-Garcia, J. A. et al. Phosphodiesterase 7 inhibition activates adult neurogenesis in hippocampus and subventricular zone in vitro and in vivo. Stem Cells 35, 458–472 (2017).
pubmed: 27538853
Morales-Garcia, J. A. et al. Phosphodiesterase 7 inhibition induces dopaminergic neurogenesis in hemiparkinsonian rats. Stem Cells Transl. Med. 4, 564–575 (2015).
pubmed: 25925836 pmcid: 4449102
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).
pubmed: 22743772
Hill, A. S., Sahay, A. & Hen, R. Increasing adult hippocampal neurogenesis is sufficient to reduce anxiety and depression-like behaviors. Neuropsychopharmacology 40, 2368–2378 (2015).
pubmed: 25833129 pmcid: 4538351
Marcussen, A. B., Flagstad, P., Kristjansen, P. E., Johansen, F. F. & Englund, U. Increase in neurogenesis and behavioural benefit after chronic fluoxetine treatment in Wistar rats. Acta Neurol. Scand. 117, 94–100 (2008).
pubmed: 18184344
Morais, M. et al. The effects of chronic stress on hippocampal adult neurogenesis and dendritic plasticity are reversed by selective MAO-A inhibition. J. Psychopharmacol. 28, 1178–1183 (2014).
pubmed: 25315831 doi: 10.1177/0269881114553646
Perera, T. D. et al. Antidepressant-induced neurogenesis in the hippocampus of adult nonhuman primates. J. Neurosci. 27, 4894–4901 (2007).
pubmed: 17475797 pmcid: 6672102 doi: 10.1523/JNEUROSCI.0237-07.2007
Osorio Fde, L. et al. Antidepressant effects of a single dose of ayahuasca in patients with recurrent depression: a preliminary report. Braz. J. Psychiatry 37, 13–20 (2015).
pubmed: 25806551 doi: 10.1590/1516-4446-2014-1496
Arai, Y. et al. Neural stem and progenitor cells shorten S-phase on commitment to neuron production. Nat. Commun. 2, 154 (2011).
pubmed: 21224845 pmcid: 3105305
Drapeau, E. et al. Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc. Natl Acad. Sci. USA 100, 14385–14390 (2003).
pubmed: 14614143
Li, Y. F. et al. Phosphodiesterase-4D knock-out and RNA interference-mediated knock-down enhance memory and increase hippocampal neurogenesis via increased cAMP signaling. J. Neurosci. 31, 172–183 (2011).
pubmed: 21209202 pmcid: 3079568
Ramirez-Amaya, V., Marrone, D. F., Gage, F. H., Worley, P. F. & Barnes, C. A. Integration of new neurons into functional neural networks. J. Neurosci. 26, 12237–12241 (2006).
pubmed: 17122048 pmcid: 6675440
Kee, N., Teixeira, C. M., Wang, A. H. & Frankland, P. W. Preferential incorporation of adult-generated granule cells into spatial memory networks in the dentate gyrus. Nat. Neurosci. 10, 355–362 (2007).
pubmed: 17277773
Trouche, S., Bontempi, B., Roullet, P. & Rampon, C. Recruitment of adult-generated neurons into functional hippocampal networks contributes to updating and strengthening of spatial memory. Proc. Natl Acad. Sci. USA 106, 5919–5924 (2009).
pubmed: 19321751
Alvarez-Buylla, A. & Lim, D. A. For the long run: maintaining germinal niches in the adult brain. Neuron 41, 683–686 (2004).
pubmed: 15003168
Wada, K. et al. Leukotriene B4 and lipoxin A4 are regulatory signals for neural stem cell proliferation and differentiation. FASEB J. 20, 1785–1792 (2006).
pubmed: 16940150
Chen, H. L. & Panchision, D. M. Concise review: bone morphogenetic protein pleiotropism in neural stem cells and their derivatives-alternative pathways, convergent signals. Stem Cells 25, 63–68 (2007).
pubmed: 16973830
Bressan, R. B. et al. EGF-FGF2 stimulates the proliferation and improves the neuronal commitment of mouse epidermal neural crest stem cells (EPI-NCSCs). Exp. Cell Res. 327, 37–47 (2014).
pubmed: 24907656
Chen, S. Q., Cai, Q., Shen, Y. Y., Cai, X. Y. & Lei, H. Y. Combined use of NGF/BDNF/bFGF promotes proliferation and differentiation of neural stem cells in vitro. Int. J. Dev. Neurosci. 38, 74–78 (2014).
pubmed: 25124373 doi: 10.1016/j.ijdevneu.2014.08.002
Yan, C. H., Levesque, M., Claxton, S., Johnson, R. L. & Ang, S. L. Lmx1a and lmx1b function cooperatively to regulate proliferation, specification, and differentiation of midbrain dopaminergic progenitors. J. Neurosci. 31, 12413–12425 (2011).
pubmed: 21880902 pmcid: 6703256 doi: 10.1523/JNEUROSCI.1077-11.2011
Pixley, S. K. CNS glial cells support in vitro survival, division, and differentiation of dissociated olfactory neuronal progenitor cells. Neuron 8, 1191–1204 (1992).
pubmed: 1610570 doi: 10.1016/0896-6273(92)90139-5
Lim, D. A. & Alvarez-Buylla, A. Interaction between astrocytes and adult subventricular zone precursors stimulates neurogenesis. Proc. Natl Acad. Sci. USA 96, 7526–7531 (1999).
pubmed: 10377448 doi: 10.1073/pnas.96.13.7526
Song, H., Stevens, C. F. & Gage, F. H. Astroglia induce neurogenesis from adult neural stem cells. Nature 417, 39–44 (2002).
pubmed: 11986659 doi: 10.1038/417039a
Corti, S. et al. Direct reprogramming of human astrocytes into neural stem cells and neurons. Exp. Cell Res. 318, 1528–1541 (2012).
pubmed: 22426197 pmcid: 3405531 doi: 10.1016/j.yexcr.2012.02.040
Heinrich, C. et al. Directing astroglia from the cerebral cortex into subtype specific functional neurons. PLoS Biol. 8, e1000373 (2010).
pubmed: 20502524 pmcid: 2872647 doi: 10.1371/journal.pbio.1000373
Heins, N. et al. Glial cells generate neurons: the role of the transcription factor Pax6. Nat. Neurosci. 5, 308–315 (2002).
pubmed: 11896398 doi: 10.1038/nn828
Niu, W. et al. In vivo reprogramming of astrocytes to neuroblasts in the adult brain. Nat. Cell Biol. 15, 1164–1175 (2013).
pubmed: 24056302 doi: 10.1038/ncb2843
Santarelli, L. et al. Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301, 805–809 (2003).
pubmed: 12907793 doi: 10.1126/science.1083328
Banasr, M., Hery, M., Printemps, R. & Daszuta, A. Serotonin-induced increases in adult cell proliferation and neurogenesis are mediated through different and common 5-HT receptor subtypes in the dentate gyrus and the subventricular zone. Neuropsychopharmacology 29, 450–460 (2004).
pubmed: 14872203 doi: 10.1038/sj.npp.1300320
Dos Santos, R. G. & Hallak, J. E. C. Therapeutic use of serotoninergic hallucinogens: a review of the evidence and of the biological and psychological mechanisms. Neurosci. Biobehav. Rev. 108, 423–434 (2020).
pubmed: 31809772 doi: 10.1016/j.neubiorev.2019.12.001
Fukunaga, K. & Moriguchi, S. Stimulation of the sigma-1 receptor and the effects on neurogenesis and depressive behaviors in mice. Adv. Exp. Med. Biol. 964, 201–211 (2017).
pubmed: 28315273 doi: 10.1007/978-3-319-50174-1_14
Hashimoto, K. Sigma-1 receptors and selective serotonin reuptake inhibitors: clinical implications of their relationship. Cent. Nerv. Syst. Agents Med. Chem. 9, 197–204 (2009).
pubmed: 20021354 doi: 10.2174/1871524910909030197
Niitsu, T., Iyo, M. & Hashimoto, K. Sigma-1 receptor agonists as therapeutic drugs for cognitive impairment in neuropsychiatric diseases. Curr. Pharm. Des. 18, 875–883 (2012).
pubmed: 22288409 doi: 10.2174/138161212799436476
Hindmarch, I. & Hashimoto, K. Cognition and depression: the effects of fluvoxamine, a sigma-1 receptor agonist, reconsidered. Hum. Psychopharmacol. 25, 193–200 (2010).
pubmed: 20373470 doi: 10.1002/hup.1106
Vadodaria, K. C. & Gage, F. H. SnapShot: adult hippocampal neurogenesis. Cell 156, 1114–1114 e1111 (2014).
pubmed: 24581504 doi: 10.1016/j.cell.2014.02.029
Lima da Cruz, R. V., Moulin, T. C., Petiz, L. L. & Leao, R. N. A single dose of 5-MeO-DMT stimulates cell proliferation, neuronal survivability, morphological and functional changes in adult mice ventral dentate gyrus. Front. Mol. Neurosci. 11, 312 (2018).
pubmed: 30233313 pmcid: 6131656 doi: 10.3389/fnmol.2018.00312

Auteurs

Jose A Morales-Garcia (JA)

Institute for Biomedical Research "A. Sols" (CSIC-UAM). Arturo Duperier 4, 28029, Madrid, Spain. jmorales@iib.uam.es.
Spanish Center for Networked Biomedical Research on Neurodegenerative Diseases (CIBERNED), c/ Valderrebollo 5, 28031, Madrid, Spain. jmorales@iib.uam.es.
Department of Cellular Biology, School of Medicine, Complutense University of Madrid, Plaza Ramón y Cajal, 28040, Madrid, Spain. jmorales@iib.uam.es.
Cellular Neurobiology Laboratory, Neurobiology Department, UCS-UCM, Hospital Universitario Ramón y Cajal, IRYCIS, Madrid, Spain. jmorales@iib.uam.es.

Javier Calleja-Conde (J)

Department of Psychobiology and Behavioural Sciences Methods, Faculty of Psychology, Complutense University of Madrid, Carretera de Humera, 28223, Madrid, Spain.

Jose A Lopez-Moreno (JA)

Department of Psychobiology and Behavioural Sciences Methods, Faculty of Psychology, Complutense University of Madrid, Carretera de Humera, 28223, Madrid, Spain.

Sandra Alonso-Gil (S)

Institute for Biomedical Research "A. Sols" (CSIC-UAM). Arturo Duperier 4, 28029, Madrid, Spain.
Spanish Center for Networked Biomedical Research on Neurodegenerative Diseases (CIBERNED), c/ Valderrebollo 5, 28031, Madrid, Spain.

Marina Sanz-SanCristobal (M)

Institute for Biomedical Research "A. Sols" (CSIC-UAM). Arturo Duperier 4, 28029, Madrid, Spain.
Spanish Center for Networked Biomedical Research on Neurodegenerative Diseases (CIBERNED), c/ Valderrebollo 5, 28031, Madrid, Spain.

Jordi Riba (J)

Department of Neuropsychology and Psychopharmacology, Faculty of Psychology and Neuroscience, Maastricht University, Maastricht, 6229 ER, The Netherlands.

Ana Perez-Castillo (A)

Institute for Biomedical Research "A. Sols" (CSIC-UAM). Arturo Duperier 4, 28029, Madrid, Spain. aperez@iib.uam.es.
Spanish Center for Networked Biomedical Research on Neurodegenerative Diseases (CIBERNED), c/ Valderrebollo 5, 28031, Madrid, Spain. aperez@iib.uam.es.
Cellular Neurobiology Laboratory, Neurobiology Department, UCS-UCM, Hospital Universitario Ramón y Cajal, IRYCIS, Madrid, Spain. aperez@iib.uam.es.

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