Mouse models of cognitive deficits due to alpha-synuclein pathology

Journal of Parkinson's Disease

Volumn 1, Issue 3, 2011, Pages 217-227

  Magen, Iddo ^a   Chesselet, Marie Françoise ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

alpha synuclein; Cognition; memory; overexpression; Parkinson's disease; promoter

Indexed keywords

ALPHA SYNUCLEIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; PLATELET DERIVED GROWTH FACTOR B; PRION PROTEIN; THY 1 ANTIGEN;

BRAIN STEM; COGNITIVE DEFECT; DISEASE ASSOCIATION; DISEASE MODEL; EXPERIMENTAL MOUSE; FOREBRAIN; HIPPOCAMPUS; HUMAN; LIMBIC CORTEX; MEMORY DISORDER; NEUROPATHOLOGY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DEFICIENCY; PROTEIN EXPRESSION; PROTEIN FUNCTION; REVIEW; SPATIAL MEMORY; SUBCORTEX; TRANSGENIC MOUSE; WILD TYPE;

ALPHA-SYNUCLEIN; ANIMALS; ANTIGENS, THY-1; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASES; COGNITION DISORDERS; DISEASE MODELS, ANIMAL; HUMANS; MICE; PARKINSON DISEASE; PRIONS;

EID: 84858173709     PISSN: 18777171     EISSN: 1877718X     Source Type: Journal    
DOI: 10.3233/JPD-2011-11043     Document Type: Review

References (74)

1. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, Pike B, Root H, Rubenstein J, Boyer R, Stenroos ES, Chandrasekharappa S, Athanassiadou A, Papapetropoulos T, Johnson WG, Lazzarini AM, Duvoisin RC, Di Iorio G, Golbe LI, & Nussbaum RL (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science, 276, 2045-2047. (Pubitemid 27443610)
2. Kr̈uger R,KuhnW,M̈uller T,Woitalla D, Graeber M,K̈osel S, Przuntek H, Epplen JT, Scḧols L, & Riess O (1998) Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat Genet, 18, 106-108.
3. Zarranz JJ, Alegre J, Ǵomez-Esteban JC, Lezcano E, Ros R, Ampuero I, Vidal L, Hoenicka J, Rodriguez O, Ataŕes B, Llorens V, Gomez Tortosa E, del Ser T, Muñoz DG, & de Yebenes JG (2004) The new mutation, E46K, of alphasynuclein causes Parkinson and Lewy body dementia. Ann Neurol, 55, 164-173. (Pubitemid 38166992)
4. Spillantini MG, Crowther RA, Jakes R, Hasegawa M, & GoedertM(1998) Alpha-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with lewy bodies. Proc Natl Acad Sci USA, 95, 6469-6473. (Pubitemid 28249037)
5. Chartier-Harlin MC, Kachergus J, Roumier C, Mouroux V, Douay X, Lincoln S, Levecque C, Larvor L, Andrieux J, Hulihan M, Waucquier N, Defebvre L, Amouyel P, Farrer M, & Dest́eeA(2004) Alpha-synuclein locus duplication as a cause of familial Parkinson's disease. Lancet, 364, 1167-1169. (Pubitemid 39296604)
6. Ib́añez P, Bonnet AM, D́ebarges B, Lohmann E, Tison F, Pollak P, Agid Y, D̈urr A, & Brice A (2004) Causal relation between alpha-synuclein gene duplication and familial Parkinson's disease. Lancet, 364, 1169-1171. (Pubitemid 39296605)
7. Kr̈uger R, Kuhn W, Leenders KL, Sprengelmeyer R, M̈uller T,Woitalla D, Portman AT,Maguire RP, Veenma L, Schr̈oder U, Scḧols L, Epplen JT, Riess O, & Przuntek H (2001) Familial parkinsonism with synuclein pathology: Clinical and PET studies of A30P mutation carriers. Neurology, 56, 1355-1362. (Pubitemid 32455298)
8. Spira PJ, Sharpe DM, Halliday G, Cavanagh J, & Nicholson GA (2001) Clinical and pathological features of a Parkinsonian syndrome in a family with an Ala53Thr alpha-synuclein mutation. Ann Neurol, 49, 313-319. (Pubitemid 32202784)
9. Puschmann A, Ross OA, Vilariño-G̈uell C, Lincoln SJ, Kachergus JM, Cobb SA, Lindquist SG, Nielsen JE, Wszolek ZK, Farrer M, Widner H, van Westen D, Ḧagerstr̈om D, Markopoulou K, ChaseBA, Nilsson K, Reimer J,&NilssonC (2009) A Swedish family with de novo alpha-synuclein A53T mutation: Evidence for early cortical dysfunction. Parkinsonism Relat Disord, 15, 627-632.
10. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, Kachergus J, Hulihan M, Peuralinna T, Dutra A, Nussbaum R, Lincoln S, Crawley A, Hanson M, Maraganore D, Adler C, Cookson MR, Muenter M, Baptista M, Miller D, Blancato J, Hardy J, & Gwinn-Hardy K (2003) Alpha-Synuclein locus triplication causes Parkinson's disease. Science, 302, 841. (Pubitemid 37339619)
11. Farrer M, Kachergus J, Forno L, Lincoln S,Wang DS, Hulihan M, Maraganore D, Gwinn-Hardy K, Wszolek Z, Dickson D, & Langston JW (2004) Comparison of kindreds with parkinsonism and alpha-synuclein genomic multiplications. Ann Neurol, 55, 174-179. (Pubitemid 38166993)
12. Ikeuchi T, Kakita A, Shiga A, Kasuga K, Kaneko H, Tan CF, Idezuka J, Wakabayashi K, Onodera O, Iwatsubo T, Nishizawa M, Takahashi H, & Ishikawa A (2008) Patients homozygous and heterozygous for SNCA duplication in a family with parkinsonism and dementia. Arch Neurol, 65, 514-519. (Pubitemid 351549961)
13. Ḱeri S, Moustafa AA, Myers CE, Benedek G, & Gluck MA (2010) {alpha}-Synuclein gene duplication impairs reward learning. Proc Natl Acad Sci USA, 107, 15992-15994.
14. Ḱeri S, Nagy H, Myers CE, Benedek G, Shohamy D, & Gluck MA (2008) Risk and protective haplotypes of the alpha-synuclein gene associated with Parkinson's disease differentially affect cognitive sequence learning. Genes Brain Behav, 7, 31-36.
15. Goris A, Williams-Gray CH, Clark GR, Foltynie T, Lewis SJ, Brown J, Ban M, Spillantini MG, Compston A, Burn DJ, Chinnery PF, Barker RA, & Sawcer SJ (2007) Tau and alphasynuclein in susceptibility to, and dementia in, Parkinson's disease. Ann Neurol, 62, 145-153. (Pubitemid 47546500)
16. Watson GS,&Leverenz JB (2010) Profile of cognitive impairment in Parkinson's disease. Brain Pathol, 20, 640-645.
17. Rodriguez-OrozMC,Jahanshahi M, Krack P, Litvan I, Macias R, Bezard E, & Obeso JA (2009) Initial clinical manifestations of Parkinson's disease: Features and pathophysiological mechanisms. Lancet Neurol, 8, 1128-1139.
18. Aarsland D,&KurzMW(2010) The epidemiology of dementia associated with Parkinson's disease. Brain Pathol, 20, 633-639.
19. Docherty MJ, & Burn DJ (2010) Parkinson's disease dementia. Curr Neurol Neurosci Rep, 10, 292-298.
20. Janvin CC, Aarsland D,&Larsen JP (2005) Cognitive predictors of dementia in Parkinson's disease: A community-based, 4-year longitudinal study. J Geriatr Psychiatry Neurol, 18, 149-154. (Pubitemid 41284965)
21. Janvin CC, Larsen JP, Aarsland D, & Hugdahl K (2006) Subtypes of mild cognitive impairment in Parkinson's disease: Progression to dementia. Mov Disord, 21, 1343-1349. (Pubitemid 44613283)
22. Neumann J, Bras J, Deas E, O'Sullivan SS, Parkkinen L, Lachmann RH, Li A, Holton J, Guerreiro R, Paudel R, Segarane B, Singleton A, Lees A, Hardy J, Houlden H, Revesz T, & Wood NW (2009) Glucocerebrosidase mutations in clinical and pathologically proven Parkinson's disease. Brain, 132, 1783-1794.
23. Alcalay RN, Mejia-Santana H, Tang MX, Rakitin B, Rosado L, Ross B, Verbitsky M, Kisselev S, Louis ED, Comella CL, Colcher A, Jennings D, Nance MA, Bressman S, Scott WK, Tanner C, Mickel SF, Andrews HF,Waters CH, Fahn S, Cote LJ, Frucht SJ, Ford B, Rezak M,NovakK, Friedman JH, Pfeiffer R, Marsh L, Hiner B, Siderowf A, Ottman R, Clark LN, Marder KS, & Caccappolo E (2010) Self-report of cognitive impairment and mini-mental state examination performance in PRKN, LRRK2, and GBA carriers with early onset Parkinson's disease. J Clin Exp Neuropsychol, 32, 775-779.
24. Compta Y, Parkkinen L, O'Sullivan SS, Vandrovcova J, Holton JL, Collins C, Lashley T, Kallis C, Williams DR, de Silva R, Lees AJ, & Revesz T (2011) Lewy-and Alzheimertype pathologies in Parkinson's disease dementia: Which is more important? Brain, 134, 1493-1505.
25. Geser F, Wenning GK, Poewe W, & McKeith I (2005) How to diagnose dementia with Lewy bodies: State of the art. Mov Disord, 20(Suppl 12), S11-S20. (Pubitemid 41419550)
26. Halliday GM, Holton JL, Revesz T, & Dickson DW (2011) Neuropathology underlying clinical variability in patients with synucleinopathies. Acta Neuropathol, 122, 187-204.
27. McKeith IG, DicksonDW,Lowe J, Emre M, O'Brien JT, Feldman H, Cummings J, Duda JE, Lippa C, Perry EK, Aarsland D, Arai H, Ballard CG, Boeve B, Burn DJ, Costa D, Del Ser T, Dubois B, Galasko D, Gauthier S, Goetz CG, Gomez-Tortosa E, Halliday G, Hansen LA, Hardy J, Iwatsubo T, Kalaria RN, Kaufer D, Kenny RA, Korczyn A, Kosaka K, Lee VM, Lees A, Litvan I, Londos E, Lopez OL, Minoshima S, Mizuno Y, Molina JA, Mukaetova-Ladinska EB, Pasquier F, Perry RH, Schulz JB, Trojanowski JQ, Yamada M, & Consortiumon DLB (2005) Diagnosis and management of dementia with Lewy bodies: Third report of the DLB Consortium. Neurology, 65, 1863-1872. (Pubitemid 43970103)
28. DicksonDW, Braak H, Duda JE, Duyckaerts C, Gasser T, Halliday GM, Hardy J, Leverenz JB, Del Tredici K, Wszolek ZK, & Litvan I (2009) Neuropathological assessment of Parkinson's disease: Refining the diagnostic criteria. Lancet Neurol, 8, 1150-1157. Review.
29. KaoAW, Racine CA, Quitania LC, Kramer JH, ChristineCW, &Miller BL (2009) Cognitive and neuropsychiatric profile of the synucleopathies: Parkinson disease, dementia with Lewy bodies, and multiple system atrophy. Alzheimer Dis Assoc Disord, 23, 365-370.
30. Beach TG, Adler CH, Lue L, Sue LI, Bachalakuri J, Henry-Watson J, Sasse J, Boyer S, Shirohi S, Brooks R, Eschbacher J, White CL, 3rd, Akiyama H, Caviness J, Shill HA, Connor DJ, Sabbagh MN, & Walker DG (2009) Arizona Parkinson's Disease Consortium Unified staging system for Lewy body disorders: Correlation with nigrostriatal degeneration cognitive impairment and motor dysfunction. Acta Neuropathol, 117, 613-634.
31. Magen I, & Chesselet MF (2010) Genetic mouse models of Parkinson's disease The state of the art. Prog Brain Res, 184, 53-87. Review.
32. Kahle PJ (2008) Alpha-Synucleopathy models and human neuropathology: Similarities and differences. Acta Neuropathol, 115, 87-95. Review. (Pubitemid 350238669)
33. Abeliovich A, Schmitz Y, Fariñas I, Choi-Lundberg D, Ho WH, Castillo PE, ShinskyN,Verdugo JM, Armanini M, Ryan A, Hynes M, Phillips H, Sulzer D, & Rosenthal A (2000) Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron, 25, 239-252. (Pubitemid 30316525)
34. Zuccato C, Ciammola A, Rigamonti D, Leavitt BR, Goffredo D, Conti L, MacDonald ME, Friedlander RM, Silani V, Hayden MR, Timmusk T, Sipione S, & Cattaneo E (2001) Loss of huntingtin-mediated BDNF gene transcription in Huntington's disease. Science, 293, 493-498. (Pubitemid 32679077)
35. Specht CG, & Schoepfer R (2004) Deletion of multimerin-1 in alpha-synuclein-deficient mice. Genomics, 83, 1176-1178.
36. Stiedl O, Radulovic J, Lohmann R, Birkenfeld K, Palve M, Kammermeier J, Sananbenesi F, & Spiess J (1999) Strain and substrain differences in context-and tone-dependent fear conditioning of inbred mice. Behav Brain Res, 104, 1-12. (Pubitemid 29421629)
37. Siegmund A, Langnaese K, &Wotjak CT (2005) Differences in extinction of conditioned fear in C57BL/6 substrains are unrelated to expression of alpha-synuclein. Behav Brain Res, 157, 291-298. (Pubitemid 40082572)
38. Chen PE, Specht CG, Morris RG, & Schoepfer R (2002) Spatial learning is unimpaired in mice containing a deletion of the alpha-synuclein locus. Eur J Neurosci, 16, 154-158. (Pubitemid 35463607)
39. Senior SL, Ninkina N, Deacon R, Bannerman D, Buchman VL, Cragg SJ, & Wade-Martins R (2008) Increased striatal dopamine release and hyperdopaminergic-like behaviour in mice lacking both alpha-synuclein and gamma-synuclein. Eur J Neurosci, 27, 947-957. (Pubitemid 351365167)
40. Robertson DC, Schmidt O, Ninkina N, Jones PA, Sharkey J, & Buchman VL (2004) Developmental loss and resistance to MPTP toxicity of dopaminergic neurones in substantia nigra pars compacta of gamma-synuclein, alpha-synuclein and double alpha/gamma-synuclein null mutant mice. J Neurochem, 89, 1126-1136. (Pubitemid 38715830)
41. Rockenstein E, Mallory M, Hashimoto M, Song D, Shults CW, Lang I, & Masliah E (2002) Differential neuropathological alterations in transgenic mice expressing alpha-synuclein from the platelet-derived growth factor and Thy-1 promoters. J Neurosci Res, 68, 568-578. (Pubitemid 34575622)
42. Freichel C, Neumann M, Ballard T, M̈uller V, Woolley M, Ozmen L, Borroni E, Kretzschmar HA, Haass C, Spooren W, & Kahle PJ (2007) Age-dependent cognitive decline and amygdala pathology in alpha-synuclein transgenic mice. Neurobiol of Aging, 28, 1421-1435. (Pubitemid 47081234)
43. Schell H, Hasegawa T, Neumann M, & Kahle PJ (2009) Nuclear and neuritic distribution of serine-129 phosphorylated alpha-synuclein in transgenic mice. Neuroscience, 160, 796-804.
44. Zhou W, Milder JB, & Freed CR (2008) Transgenic mice overexpressing tyrosine-to-cysteine mutant human alphasynuclein: A progressive neurodegenerative model of diffuse Lewy body disease. J Biol Chem, 283, 9863-9870.
45. Lim Y, Kehm VM, Lee EB, Soper JH, Li C, Trojanowski JQ, &LeeVM(2011) {alpha}-Syn suppression reverses synaptic and memory defects in a mouse model of dementia with Lewy Bodies. J Neurosci, 31, 10076-10087.
46. Masliah E, Rockenstein E, Veinbergs I, Mallory M, Hashimoto M, Takeda A, SagaraY, Sisk A,&Mucke L (2000) Dopaminergic loss and inclusion body formation in alphasynuclein mice: Implications for neurodegenerative disorders. Science, 287, 1265-1269. (Pubitemid 30112148)
47. Nuber S, Petrasch-Parwez E, Winner B, Winkler J, von Ḧorsten S, Schmidt T, Boy J, Kuhn M, Nguyen HP, Teismann P, Schulz JB, Neumann M, Pichler BJ, Reischl G, Holzmann C, Schmitt I, Bornemann A, Kuhn W, Zimmermann F, Servadio A, & Riess O (2008) Neurodegeneration and motor dysfunction in a conditional model of Parkinson's disease. J Neurosci, 28, 2471-2484. (Pubitemid 351348209)
48. Hashimoto M, Rockenstein E, & Masliah E (2003) Transgenic models of alpha-synuclein pathology: Past, present, and future. Ann N Y Acad Sci, 991, 171-188. Review. (Pubitemid 36793813)
49. Masliah E, Rockenstein E, Veinbergs I, Sagara Y, Mallory M, Hashimoto M, & Mucke L (2001) Beta-amyloid peptides enhance alpha-synuclein accumulation and neuronal deficits in a transgenic mouse model linking Alzheimer's disease and Parkinson's disease. Proc Natl Acad Sci USA, 98, 12245-12250. (Pubitemid 32959858)
50. Price DL, Rockenstein E, Ubhi K, Phung V, MacLean-Lewis N, Askay D, Cartier A, Spencer B, Patrick C, Desplats P, Ellisman MH, & Masliah E (2010) Alterations in mGluR5 expression and signaling in Lewy body disease and in transgenic models of alpha-synucleopathy-implications for excitotoxicity. PLoS One, 5, e14020.
51. Winner B, Lie DC, Rockenstein E, Aigner R, Aigner L, Masliah E, Kuhn HG, & Winkler J (2004) Human wildtype alpha-synuclein impairs neurogenesis. J Neuropathol Exp Neurol, 63, 1155-1166. (Pubitemid 39492021)
52. Masliah E, Rockenstein E, Mante M, Crews L, Spencer B, Adame A, Patrick C, Trejo M, Ubhi K, Rohn TT, Mueller-Steiner S, Seubert P, Barbour R, McConlogue L, Buttini M, Games D, & Schenk D (2011) Passive immunization reduces behavioral and neuropathological deficits in an alphasynuclein transgenic model of Lewy body disease. PLoS One, 6, e19338.
53. Giasson BI, Duda JE, Quinn SM, Zhang B, Trojanowski JQ, & LeeVM(2002) Neuronal alpha-synucleopathy with severe movement disorder in mice expressing A53T human alphasynuclein. Neuron, 34, 521-533. (Pubitemid 34628750)
54. Clinton LK, Blurton-Jones M, Myczek K, Trojanowski JQ, & LaFerla FM (2010) Synergistic Interactions between Abeta, tau, and alpha-synuclein: Acceleration of neuropathology and cognitive decline. J Neurosci, 30, 7281-7289.
55. Kahle PJ, Neumann M, Ozmen L, Muller V, Jacobsen H, Schindzielorz A, Okochi M, Leimer U, van Der Putten H, Probst A, Kremmer E, Kretzschmar HA, & Haass C (2000) Subcellular localization of wild-type and Parkinson's diseaseassociated mutant alpha-synuclein in human and transgenic mouse brain. J Neurosci, 20, 6365-6373.
56. Fujiwara H, Hasegawa M, Dohmae N, Kawashima A, Masliah E, GoldbergMS,Shen J,Takio K,&IwatsuboT(2002) Alpha-Synuclein is phosphorylated in synucleopathy lesions. Nat Cell Biol, 4, 160-164.
57. Neumann M, Kahle PJ, Giasson BI, Ozmen L, Borroni E, Spooren W, M̈uller V, Odoy S, Fujiwara H, Hasegawa M, Iwatsubo T, Trojanowski JQ, Kretzschmar HA, & Haass C (2002) Misfolded proteinase K-resistant hyperphosphorylated alpha-synuclein in aged transgenic mice with locomotor deterioration and in human alpha-synucleopathies. J Clin Invest, 110, 1429-1439. (Pubitemid 35396914)
58. Braak H, Del Tredici K, R̈ub U, de Vos RA, Jansen Steur EN, & Braak E (2003) Staging of brain pathology related to sporadic Parkinson's disease. Neurobiol Aging, 24, 197-211. (Pubitemid 36007810)
59. Braak H, Del Tredici K, Bratzke H, Hamm-Clement J, Sandmann-Keil D, & R̈ub U (2002) Staging of the intracerebral inclusion body pathology associated with idiopathic Parkinson's disease (preclinical and clinical stages). J Neurol, 249(Suppl 3:III/1-5). Review.
60. Braak H, R̈ub U, & Del Tredici K (2006) Cognitive decline correlates with neuropathological stage in Parkinson's disease. J Neurol Sci, 248, 255-258. (Pubitemid 44647283)
61. Thiruchelvam MJ, Powers JM, Cory-Slechta DA, & Richfield EK (2004) Risk factors for dopaminergic neuron loss in human alpha-synuclein transgenic mice. Eur J Neurosci, 19, 845-854. (Pubitemid 38297021)
62. Richfield EK, Thiruchelvam MJ, Cory-Slechta DA,Wuertzer C, Gainetdinov RR, Caron MG, Di Monte DA, & Federoff HJ (2002) Behavioral and neurochemical effects of wild-type and mutated human alpha-synuclein in transgenic mice. Exp Neurol, 175, 35-48. (Pubitemid 34507908)
63. Tofaris GK, Garcia Reitb̈ock P, Humby T, Lambourne SL, O'Connell M, Ghetti B, Gossage H, Emson PC, Wilkinson LS, Goedert M, & Spillantini MG (2006) Pathological changes in dopaminergic nerve cells of the substantia nigra and olfactory bulb in mice transgenic for truncated human alpha-synuclein(1-120) : Implications for Lewy body disorders. J Neurosci, 26, 3942-3950. (Pubitemid 44315414)
64. Wakamatsu M, Ishii A, Iwata S, Sakagami J, Ukai Y, Ono M, Kanbe D, Muramatsu S, Kobayashi K, Iwatsubo T, & Yoshimoto M (2008) Selective loss of nigral dopamine neurons induced by overexpression of truncated human alphasynuclein in mice. Neurobiol Aging, 29, 574-585. (Pubitemid 351312826)
65. Wakamatsu M, Iwata S, Funakoshi T, & YoshimotoM(2008) Dopamine receptor agonists reverse behavioral abnormalities of alpha-synuclein transgenic mouse, a new model of Parkinson's disease. J Neurosci Res, 15, 640-646. (Pubitemid 351204477)
66. Peterson DA, Elliott C, Song DD, Makeig S, Sejnowski TJ,& Poizner H (2009) Probabilistic reversal learning is impaired in Parkinson's disease. Neuroscience, 163, 1092-1101.
67. Gurvich C, Georgiou-Karistianis N, Fitzgerald PB, Millist L, & White OB (2007) Inhibitory control and spatial working memory in Parkinson's disease. Mov Disord, 22, 1444-1450. (Pubitemid 47280630)
68. Fleming SM, Garcia E, Masliah E, Chesselet MF, & Jentsch JD (2008) Impaired reversal learning in transgenic mice overexpressing human wildtype alpha synuclein. Neurosci Abst, 341.1.
69. Magen I, Cardiff KM, Maidment NT,Masliah E, & Chesselet MF (2010) Hyperactivity and reduced anxiety in young mice over-expressing wild-type human alpha-synuclein under the Thy-1 promoter. Neurosci Abst, 750.26.
70. Li B, Arime Y, Hall FS, Uhl GR, & Sora I (2010) Impaired spatial working memory and decreased frontal cortex BDNF protein level in dopamine transporter knockout mice. Eur J Pharmacol, 628, 104-107.
71. Lam HA,Wu N, Cely I, Kelly RL, Hean S, Richter F, Magen I, Cepeda C, Ackerson LC, Walwyn W, Masliah E, Chesselet MF, Levine MS, & Maidment NT (2011) Elevated tonic extracellular dopamine concentration and altered dopamine modulation of synaptic activity precede dopamine loss in the striatum of mice overexpressing human synuclein. J Neurosci Res, 89, 1091-1102.
72. Botton PH, Costa MS, Ardais AP, Mioranzza S, Souza DO, da Rocha JB,&Porcíuncula LO (2010) Caffeine prevents disruption of memory consolidation in the inhibitory avoidance and novel object recognition tasks by scopolamine in adult mice. Behav Brain Res, 214, 254-259.
73. Yang JH, Han SJ, Ryu JH, Jang IS, & Kim DH (2009) Ginsenoside Rh2 ameliorates scopolamine-induced learning deficit in mice. Biol Pharm Bull, 32, 1710-1715.
74. Szeg̈o EM, Gerhardt E, Outeiro TF, & Kermer P (2011) Dopamine-depletion and increased-synuclein load induce degeneration of cortical cholinergic fibers in mice. J Neurol Sci, 310, 90-95.