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Folia Neuropathologica
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vol. 56
Original paper

Vitamin E can compensate the density of M1 receptors in the hippocampus of scopolamine-treated rats

Ali Sayyahi, Mehrdad Jahanshahi, Hossein Amini, Hamid Sepehri

Folia Neuropathol 2018; 56 (3): 215-228
Online publish date: 2018/09/28
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M1 muscarinic receptor plays a fundamental role in memory and is closely associated with Alzheimer’s disease (AD); it has long been assumed as a therapeutic goal. By activating of the cholinergic receptor vitamin E helps with memory retention. But effects of vitamin E on density of M1 muscarinic receptor-immunoreactive (ir) neurons remain poorly understood. The present research aimed to examine the chronic administration effect of vitamin E against scopolamine-induced memory loss and the number of M1 muscarinic receptor-ir neurons of the hippocampus in male rats.

Randomly, 42 adult male Wistar rats were divided to six groups: control, Sham-saline: receiving scopolamine + saline, Sham-sesame oil: receiving scopolamine + sesame oil and three experimental groups: receiving scopolamine + vitamin E with different doses (25, 50, and 100 mg/kg/day, i.p.) for 14 days. The passive avoidance task was used for the memory test. Twenty-four hours after behavioral tests, rats’ brains were taken and fixed, and after tissue processing, sections were stained using the immunohistochemical technique for M1 muscarinic receptor-ir neurons and cresyl violet for neurons.

The injection of scopolamine to rats caused memory impairment and vitamin E treatment could ameliorate it. In the scopolamine-treated groups, the number of CA1 and CA3 pyramidal and dentate gyrus (DG) granular neurons was decreased significantly as compared to the control group. Vitamin E treatment significantly increased neuron numbers in the CA1 and CA3 areas of the hippocampus and DG area. Treatment with vitamin E for 14 days could compensate the loss of M1 muscarinic receptor-immunoreactive neuron numbers induced by scopolamine in the hippocampus. The most effective vitamin E dose was 50 mg/kg/day in this study.

In conclusion, vitamin E can compensate the neuronal loss in the hippocampal formation and also it can raise the density of M1 receptor-ir muscarinic neurons after an injection of scopolamine.

vitamin E, scopolamine, M1 muscarinic receptor, hippocampus, passive avoidance memory test

Abd-El-Fattah AA, El-Sawalhi MM, Rashed ER, El-Ghazaly MA. Possible role of vitamin E, coenzyme Q10 and rutin in protection against cerebral ischemia/reperfusion injury in irradiated rats. Int J Radiat Biol 2010; 86: 1070-1078.
Alzoubi KH, Khabour OF, Salah HA, Hasan Z. Vitamin E prevents high-fat high-carbohydrates diet-induced memory impairment: the role of oxidative stress. Physiol Behav 2013; 119: 72-78.
Anagnostaras SG, Murphy GG, Hamilton SE, Mitchell SL, Rahnama NP, Nathanson NM, Silva AJ. Selective cognitive dysfunction in acetylcholine M1 muscarinic receptor mutant mice. Nat Neurosci 2003; 6: 51-58.
Araujo JA, Studzinski CM, Milgram NW. Further evidence for the cholinergic hypothesis of aging and dementia from the canine model of aging. Prog Neuropsychopharmacol Biol Psychiatry 2005; 29: 411-422.
Arlt S, Beisiegel U, Kontush A. Lipid peroxidation in neurodegeneration: new insights into Alzheimer’s disease. Curr Opin Lipidol 2002; 13: 289-294.
Azami NS, Piri M, Oryan S, Jahanshahi M, Babapour V, Zarrindast MR. Involvement of dorsal hippocampal α-adrenergic receptors in the effect of scopolamine on memory retrieval in inhibitory avoidance task. Neurobiol Learn Mem 2010; 93: 455-462.
Babahajian A, Rasouli H, Katebi M, Sarveazad A, Soleimani M, Nobakht M. Effect of human chorionic gonadotropin and vitamine E on cellular density of CA1 hippocampal area, learning ability and memory, following ischemia – reperfusion injury in mice. J Gorgan Uni Med Sci 2014; 15: 23-28.
Baloyannis SJ. Mitochondrial alterations in Alzheimer’s disease. J Alzheimers Dis 2006; 9: 119-126.
Bassett CN, Neely MD, Sidell KR, Markesbery WR, Switt LL, Montine TJ. Cerebrospinal fluid lipoproteins are more vulnerable to oxidation in Alzheimer’s disease and are neurotoxic when oxidized ex vivo. Lipids 1999; 34: 1273-1280.
Billings LM, Oddo S, Green KN, McGaugh JL, Laferla FM. Intraneuronal Abeta causes the onset of early Alzheimer’s disease-related cognitive deficits in transgenic mice. Neuron 2005; 45: 675-688.
Bist R, Bhatt DK. The evaluation of effect of alpha-lipoic acid and vitamin E on the lipid peroxidation, gamma-amino butyric acid and serotonin level in the brain of mice (Mus musculus) acutely intoxicated with lindane. J Neurol Sci 2009; 276: 99-102.
Blanchard V, Moussaoui S, Czech C, Touchet N, Bonici B, Planche M, Canton T, Jedidi I, Gohin M, Wirths O, Bayer TA, Langui D, Duyckaerts C, Tremp G, Pradier L. Time sequence of maturation of dystrophic neurites associated with A deposits in APP/PS1 transgenic mice. Exp Neurol 2003; 184: 247-263.
Bonner TI, Buckley NJ, Young AC, Brann MR. Identification of a family of muscarinic acetylcholine receptor genes. Science 1987; 237: 527-532.
Bonner TI, Young AC, Bran MR, Buckley NJ. Cloning and expression of the human and rat m5 muscarinic acetylcholine receptor genes. Neuron 1988; 1: 403-410.
Brun A, Englund E. Regional pattern of degeneration in Alzheimer’s disease: neuronal loss and histopathological grading. Histopathology 1981; 5: 549-564.
Caulfield MP. Muscarinic receptors-characterization, coupling and function. Pharmacol Ther 1993; 58: 319-379.
Chen K, Zhang X, Wei Xp, Qu P, Liu Yx, Li Ty. Antioxidant vitamin status during pregnancy in relation to cognitive development in the first two years of life. Early Hum Dev 2009; 85: 421-427.
Chen W, Cheng X, Chen J, Yi X, Nie D, Sun X, Qin J, Tian M, Jin G, Zhang X. Lycium barbarum polysaccharides prevent memory and neurogenesis impairments in scopolamine-treated rats. PLoS One 2014; 9: e88076.
Ciobica A, Padurariu M, Bild W, Stefanescu C. Cardiovascular risk factors as potential markers for mild cognitive impairment and Alzheimer’s disease. Psychiatr Danub 2011; 23: 340-346.
Deb D, Bairy KL, Nayak V, Rao M. Comparative effect of lisinopril and fosinopril in mitigating learning and memory deficit in scopolamine-induced amnesic rats. Adv Pharmacol Sci 2015; 2015: 1-11.
Dysken MW, Sano M, Asthana S, Vertrees JE, Pallaki M, Llorente M, Love S, Schellenberg GD, McCarten JR, Malphurs J, Prieto S, Chen P, Loreck DJ, Trapp G, Bakshi RS, Mintzer JE, Heidebrink JL, Vidal-Cardona A, Arroyo LM, Cruz AR, Zachariah S, Kowall NW, Chopra MP, Craft S, Thielke S, Turvey CL, Woodman C, Monnell KA, Gordon K, Tomaska J, Segal Y, Peduzzi PN, Guarino PD. Effect of vitamin e and memantine on functional decline in Alzheimer disease: The TEAM-AD VA cooperative randomized trial. JAMA 2014; 311: 33-44.
Eftekharzadeh M, Nobakht M, Alizadeh A, Soleimani M, Hajghasem M, Kordestani Shargh B, Karkuki Osguei N, Behnam B, Samadikuchaksaraei A. The effect of intrathecal delivery of bone marrow stromal cells on hippocampal neurons in rat model of Alzheimer’s disease. Iran J Basic Med Sci 2015; 18: 520-525.
Eidi A, Eidi M, Mahmoodi G, Oryan S. Effect of vitamin E on memory retention in rats: possible involvement of cholinergic system. Eur Neuropsychopharmacol 2006; 16: 101-106.
Engin KN. Alpha-tocopherol: Looking beyond an antioxidant. Mol Vis 2009; 15: 855-860.
Farina N, Isaac MG, Clark AR, Rusted J, Tabet N. Vitamin E for Alzheimer’s dementia and mild cognitive impairment. Cochrane Database Syst Rev 2012; 11: CD002854.
Fata GL, Weber P, Mohajeri MH. Effects of vitamin E on cognitive performance during ageing and in Alzheimer’s disease. Nutrients 2014; 6: 5453-5472.
Felder CC, Bymaster FP, Ward J, DeLapp N. Therapeutic opportunities for muscarinic receptors in the central nervous system. J Med Chem 2000; 43: 4333-4353.
Fisher A. Cholinergic treatments with emphasis on m1 muscarinic agonists as potential disease-modifying agents for Alzheimer’s disease. Neurotherapeutics 2008; 5: 433-442.
Fukui K, Omoi NO, Hayasaka T, Shinnkai T, Suzuki S, Abe K, Urano S. Cognitive impairment of rats caused by oxidative stress and aging, and its prevention by vitamin E. Ann N Y Acad Sci 2002; 959: 275-284.
Gerber DJ, Sotnikova TD, Gainetdinov RR, Huang SY, Caron MG, Tonegawa S. Hyperactivity, elevated dopaminergic transmission, and response to amphetamine in M1 muscarinic acetylcholine receptor-deficient mice. Proc Natl Acad Sci 2001; 98: 15312-15317.
Giraldo E, Lloret A, Fuchsberger T, Vińa J. A and tau toxicities in Alzheimer’s are linked via oxidative stress-induced p38 activation: Protective role of vitamin E. Redox Biol 2014; 2: 873-877.
Grasby PM, Frith CD, Paulesu E, Friston KJ, Frackowiak RSJ, Dolan RJ. The effect of the muscarinic antagonist scopolamine on regional cerebral blood flow during the performance of
a memory task. Exp Brain Res 1995; 104: 337-348.
Grimm MOW, Stahlmann CP, Mett J, Haupenthal VJ, Zimmer VC, Lehmann J, Hundsdörfer B, Endres K, Grimm HS, Hartmann T. Vitamin E: Curse or benefit in Alzheimer’s disease? A systematic investigation of the impact of -, - and -tocopherol on A generation and degradation in neuroblastoma cells. J Nutr Health Aging 2015; 19: 646-654.
Grodstein F, Chen J, Willett WC. High-dose antioxidant supplements and cognitive function in community-dwelling elderly women. Am J Clin Nutr 2003; 77: 975-984.
Grundman M. Vitamin E and Alzheimer disease: the basis for additional clinical trials. Am J Clin Nutr 2000; 71: 630s-636s.
Hamilton SE, Loose MD, Qi M, Levey AI, Hille B, McKnight GS, Idzerda RL, Nathanson NM. Disruption of the m1 receptor gene ablates muscarinic receptor-dependent M current regulation and seizure activity in mice. Proc Natl Acad Sci 1997; 94: 13311-13316.
Hasanein P, Kazemian Mahtaj A. Ameliorative effect of rosmarinic acid on scopolamine-induced memory impairment in rats. Neurosci Lett 2015; 585: 23-27.
Hasanein P, Shahidi S. Effects of combined treatment with vitamins C and E on passive avoidance learning and memory in diabetic rats. Neurobiol Learn Mem 2010; 93: 472-478.
Heneka MT, Sastre M, Dumitrescu-Ozimek L, Dewachter I, Walter J, Klockgether T, Van Leuven F. Focal glial activation coincides with increased BACE1 activation and precedes amyloid plaque deposition in APP [V717I] transgenic mice. J Neuroinflammation 2005; 2: 22.
Hodges Jr DB, Lindner MD, Hogan JB, Jones KM, Markus EJ. Scopolamine induced deficits in a battery of rat cognitive tests: comparisons of sensitivity and specificity. Behav Pharmacol 2009; 20: 237-251.
Hohmann CF, Potter ED, Levey AI. Development of muscarinic receptor subtypes in the forebrain of the mouse. J Comp Neurol 1995; 358: 88-101.
Jahanshahi M, Azami NS, Nickmahzar EG. Effect of scopolamine-based amnesia on the number of astrocytes in the rat’s hippocampus. Int J Morphol 2012; 30: 388-393.
Jahanshahi M, Nickmahzar EG, Babakordi F. The effect of Ginkgo biloba extract on scopolamine-induced apoptosis in the hippocampus of rats. Anat Sci Int 2013; 88: 217-222.
Jahanshahi M, Nickmahzar EG, Seif-hoseini S, Babakordi F, Moharreri A. Scopolamine reduces the density of M1 muscarinic neurons in rats’ hippocampus. Int J Morphol 2013; 31: 1227-1232.
Jahanshahi M, Nikmahzar E, Yadollahi N, Ramazani K. Protective effects of Ginkgo biloba extract (EGB 761) on astrocytes of rat hippocampus after exposure with scopolamine. Anat Cell Biol 2012; 45: 92-96.
Jahanshahi M, Sadeghi Y, Hosseini A. Estimation of astrocyte number in different subfield of rat hippocampus. Pak J Biol Sci 2006; 9: 1595-1597.
Jeong EJ, Lee KY, Kim SH, Sung SH, Kim YC. Cognitive-enhancing and antioxidant activities of iridoid glycosides from Scrophularia buergeriana in scopolamine-treated mice. Eur J Pharmacol 2008; 588: 78-84.
Jolitha AB, Subramanyam MVV, Devi SA. Age-related responses of the rat cerebral cortex: influence of vitamin E and exercise on the cholinergic system. Biogerontology 2009; 10: 53-63.
Karimi S, Jahanshahi M, Golalipour MJ. The effect of MDMA-induced anxiety on neuronal apoptosis in adult male rats’ hippocampus. Folia Biol (Praha) 2014; 60: 187-191.
Keltner NL, Zielinski AL, Hardin MS. Biological perspectives: Drugs used for cognitive symptoms of Alzheimer’s disease. Perspect Psychiatr Care 2001; 37: 31-34.
Khodamoradi N, Komaki A, Salehi I, Shahidi S, Sarihi A. Effect of vitamin E on lead exposure-induced learning and memory impairment in rats. Physiol Behav 2015; 144: 90-94.
Komaki A, Karimi SA, Salehi I, Sarihi A, Shahidi S, Zarei M. The treatment combination of vitamins E and C and astaxanthin prevents high-fat diet induced memory deficits in rats. Pharmacol Biochem Behav 2015; 131: 98-103.
Korbo L, Amrein I, Lipp HP, Wolfer D, Regeur L, Oster S, Pakkenberg B. No evidence for loss of hippocampal neurons in non-Alzheimer dementia patients. Acta Neurol Scand 2004; 109: 132-139.
Koscik RL, Lai HJ, Laxova A, Zaremba KM, Kosorok MR, Douglas JA, Rock MJ, Splaingard ML, Farrell PM. Preventing early, prolonged vitamin E deficiency: an opportunity for better cognitive outcomes via early diagnosis through neonatal screening. J Pediatr 2005; 147: 51-56.
Kril JJ, Patel S, Harding AJ, Halliday GM. Patients with vascular dementia due to microvascular pathology have significant hippocampal neuronal loss. J Neurol Neurosurg Psychiatry 2002; 72: 747-751.
Kwon SH, Kim HC, Lee SY, Jang CG. Loganin improves learning and memory impairments induced by scopolamine in mice. Eur J Pharmacol 2009; 619: 44-49.
Lee B, Park J, Kwon S, Park MW, Oh SM, Yeom MJ, Shim I, Lee HJ, Hahm DH. Effect of wild ginseng on scopolamine-induced acetylcholine depletion in the rat hippocampus. J Pharm Pharmacol 2010; 62: 263-271.
Lee HP, Zhu X, Casadesus G, Castellani RJ, Nunomura A, Smith MA, Lee HG, Perry G. Antioxidant approaches for the treatment of Alzheimer’s disease. Expert Rev Neurother 2010; 10: 1201-1208.
Levey AI. Immunological localization of m1-m5 muscarinic acetylcholine receptors in peripheral tissues and brain. Life Sci 1993; 52: 441-448.
Levey AI, Kitt CA, Simonds WF, Price DL, Brann MR. Identification and localization of muscarinic acetylcholine receptor proteins in brain with subtype-specific antibodies. J Neurosci 1991; 11: 3218-3226.
Lloret A, Badía MC, Mora NJ, Pallardó FV, Alonso MD, Vińa J. Vitamin e paradox in Alzheimer’s disease: It does not prevent loss of cognition and may even be detrimental. J Alzheimers Dis 2009; 17: 143-149.
Mahakizadeh S, Jahanshahi M, Haidari K, Shahbazi M. Dopamine receptors gene expression in male rat hippocampus after administration of MDMA (ecstasy). Int J Morphol 2015; 33: 301-308.
Marisco PC, Carvalho FB, Rosa MM, Girardi BA, Gutierres JM, Jaques JA, Salla AP, Pimentel VC, Schetinger MR, Leal DB, Mello CF, Rubin MA. Piracetam prevents scopolamine-induced memory impairment and decrease of NTPDase, 5’-nucleotidase and adenosine deaminase activities. Neurochem Res 2013; 38: 1704-1714.
Milgram NW, Head E, Zicker SC, Ikeda-Douglas CJ, Murphey H, Muggenburg B, Siwak C, Tapp D, Cotman CW. Learning ability in aged beagle dogs is preserved by behavioral enrichment and dietary fortification: a two-year longitudinal study. Neurobiol Aging 2005; 26: 77-90.
Miyakawa T, Yamada M, Duttaroy A, Wess J. Hyperactivity and intact hippocampus-dependent learning in mice lacking the M1 muscarinic acetylcholine receptor. J Neurosci 2001; 21: 5239-5250.
Moghadami S, Jahanshahi M, Sepehri H, Amini H. Gonadectomy reduces the density of androgen receptor-immunoreactive neurons in male rat’s hippocampus: testosterone replacement compensates it. Behav Brain Funct 2016; 12: 5.
Nagata K, Nakashima-Kamimura N, Mikami T, Ohsawa I, Ohta S. Consumption of molecular hydrogen prevents the stress-induced impairments in hippocampus-dependent learning tasks during chronic physical restraint in mice. Neuropsychopharmacology 2009; 34: 501-508.
Nathanson NM. Molecular properties of the muscarinic acetylcholine receptor. Annu Rev Neurosci 1987; 10: 195-236.
Navarro A, Bandez MJ, Lopez-Cepero JM, Gómez C, Boveris A. High doses of vitamin E improve mitochondrial dysfunction in rat hippocampus and frontal cortex upon aging. Am J Physiol Regul Integr Comp Physiol 2011; 300: R827-R834.
Nesaretnam K. Multitargeted therapy of cancer by tocotrienols. Cancer Lett 2008; 269: 388-395.
Nishida Y, Yokota T, Takahashi T, Uchihara T, Jishage K-i, Mizusawa H. Deletion of vitamin E enhances phenotype of Alzheimer disease model mouse. Biochem Biophys Res Commun 2006; 350: 530-536.
Padurariu M, Ciobica A, Hritcu L, Stoica B, Bild W, Stefanescu C. Changes of some oxidative stress markers in the serum of patients with mild cognitive impairment and Alzheimer’s disease. Neurosci Lett 2010; 469: 6-10.
Padurariu M, Ciobica A, Mavroudis I, Fotiou D, Baloyannis S. Hippocampal neuronal loss in the CA1 and CA3 areas of Alzheimer’s disease patients. Psychiatr Danub 2012; 24: 152-158.
Palozza P, Simone R, Picci N, Buzzoni L, Ciliberti N, Natangelo A, Manfredini S, Vertuani S. RETRACTED: Design, synthesis, and antioxidant potency of novel -tocopherol analogues in isolated membranes and intact cells. Free Radic Biol Med 2008; 44: 1452-1464.
Palozza P, Verdecchia S, Avanzi L, Vertuani S, Serini S, Iannone A, Manfredini S. Comparative antioxidant activity of tocotrienols and the novel chromanyl-polyisoprenyl molecule FeAox-6 in isolated membranes and intact cells. Mol Cell Biochem 2006; 287: 21-32.
Petersen RC, Thomas RG, Grundman M, Bennett D, Doody R, Ferris S, Galasko D, Jin S, Kaye J, Levey A, Pfeiffer E, Sano M, van Dyck CH, Thal LJ; Alzheimer’s Disease Cooperative Study Group.. Vitamin E and donepezil for the treatment of mild cognitive impairment. N Engl J Med 2005; 352: 2379-2388.
Power AE, McIntyre CK, Litmanovich A, McGaugh JL. Cholinergic modulation of memory in the basolateral amygdala involves activation of both m1 and m2 receptors. Behav Pharmacol 2003; 14: 207-213.
Puri V, Wang X, Vardigan JD, Kuduk SD, Uslaner JM. The selective positive allosteric M1 muscarinic receptor modulator PQCA attenuates learning and memory deficits in the Tg2576 Alzheimer’s disease mouse model. Behav Brain Res 2015; 287: 96-99.
Sano M, Ernesto C, Thomas RG, Klauber MR, Schafer K, Grundman M, Woodbury P, Growdon J, Cotman CW, Pfeiffer E, Schneider LS, Thal LJ. A controlled trial of selegiline, alpha-tocopherol, or both as treatment for Alzheimer’s disease. N Engl J Med 1997; 336: 1216-1222.
Schippling S, Kontush A, Arlt S, Buhmann C, Stürenburg HJ, Mann U, Müller-Thomsen T, Beisiegel U. Increased lipoprotein oxidation in Alzheimer’s disease. Free Radic Biol Med 2000; 28: 351-360.
Seifhosseini S, Jahanshahi M, Moghimi A, Aazami NS. The effect of scopolamine on avoidance memory and hippocampal neurons in male Wistar rats. Basic Clin Neurosci 2011; 3: 9-15.
Shichiri M, Yoshida Y, Ishida N, Hagihara Y, Iwahashi H, Tamai H, Niki E.-Tocopherol suppresses lipid peroxidation and behavioral and cognitive impairments in the Ts65Dn mouse model of Down syndrome. Free Radic Biol Med 2011; 50: 1801-1811.
Shideler KK, Yan J. M1 muscarinic receptor for the development of auditory cortical function. Mol Brain 2010; 3: 29.
Shinoe T, Matsui M, Taketo MM, Manabe T. Modulation of synaptic plasticity by physiological activation of M1 muscarinic acetylcholine receptors in the mouse hippocampus. J Neurosci 2005; 25: 11194-11200.
Shiozaki K, Iseki E, Hino H, Kosaka K. Distribution of M1 muscarinic acetylcholine receptors in the hippocampus of patients with Alzheimer’s disease and dementia with Lewy bodies – an immunohistochemical study. J Neurol Sci 2001; 193: 23-28.
Simic G, Kostovic I, Winblad B, Bogdanovic N. Volume and number of neurons of the human hippocampal formation in normal aging and Alzheimer’s disease. J Comp Neurol 1997; 379: 482-494.
Spires TL, Orne JD, SantaCruz K, Pitstick R, Carlson GA, Ashe KH, Hyman BT. Region-specific dissociation of neuronal loss and neurofibrillary pathology in a mouse model of tauopathy. Am J Pathol 2006; 168: 1598-1607.
Tagami M, Yamagata K, Ikeda K, Nara Y, Fujino H, Kubota A, Numano F, Yamori Y. Vitamin E prevents apoptosis in cortical neurons during hypoxia and oxygen reperfusion. Lab Invest 1998; 78: 1415-1429.
Tagliari B, Scherer EB, Machado FR, Ferreira AGK, Dalmaz C, Wyse ATS. Antioxidants prevent memory deficits provoked by chronic variable stress in rats. Neurochem Res 2011; 36: 2373-2380.
Takatsu H, Owada K, Abe K, Nakano M, Urano S. Effect of vitamin E on learning and memory deficit in aged rats. J Nutr Sci Vitaminol 2009; 55: 389-393.
Tayebati SK, Amenta F, El-Assouad D, Zaccheo D. Muscarinic cholinergic receptor subtypes in the hippocampus of aged rats. Mech Ageing Dev 2002; 123: 521-528.
Thomé GR, Spanevello RM, Mazzanti A, Fiorenza AM, Duarte MM, da Luz SC, Pereira ME, Morsch VM, Schetinger MR, Mazzanti CM. Vitamin E decreased the activity of acetylcholinesterase and level of lipid peroxidation in brain of rats exposed to aged and diluted sidestream smoke. Nicotine Tob Res 2011; 13: 1210-1219.
Van de Pol LA, Hensel A, Barkhof F, Gertz HJ, Scheltens P, Van Der Flier WM. Hippocampal atrophy in Alzheimer disease: age matters. Neurology 2006; 66: 236-238.
VanDeMark KL, Guizzetti M, Giordano G, Costa LG. The activation of M1 muscarinic receptor signaling induces neuronal differentiation in pyramidal hippocampal neurons. J Pharmacol Exp Ther 2009; 329: 532-542.
Wess J. Molecular biology of muscarinic acetylcholine receptors. Crit Rev Neurobiol 1996; 10: 69-99.
Wess J. Muscarinic acetylcholine receptor knockout mice: novel phenotypes and clinical implications. Annu Rev Pharmacol Toxicol 2004; 44: 423-450.
West MJ, Coleman PD, Flood DG, Troncoso JC. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer’s disease. Lancet 1994; 344: 769-772.
Wirths O, Bayer TA. Neuron loss in transgenic mouse models of Alzheimer’s disease. Int J Alzheimers Dis 2010; 2010: 723782.
Wirths O, Breyhan H, Marcello A, Cotel MC, Brück W, Bayer TA. Inflammatory changes are tightly associated with neurodegeneration in the brain and spinal cord of the APP/PS1KI mouse model of Alzheimer’s disease. Neurobiol Aging 2010; 31: 747-757.
Yan BC, Park JH, Chen BH, Cho JH, Kim IH, Ahn JH, Lee JC, Hwang IK, Cho JH, Lee YL, Kang IJ, Won MH. Long-term administration of scopolamine interferes with nerve cell proliferation, differentiation and migration in adult mouse hippocampal dentate gyrus, but it does not induce cell death. Neural Regen Res 2014; 9: 1731-1739.
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