Depressive-like phenotype induced by AAV-mediated overexpression of human α-synuclein in midbrain dopaminergic neurons

Experimental Neurology

Volumn 273, Issue , 2015, Pages 243-252

  Caudal, D ^a   Alvarsson, A ^a   Bjorklund A ^b   Svenningsson, P ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b LUND UNIVERSITY   (Sweden)

Author keywords

Alpha synuclein; Anxiety; Corticosterone; Depression; Parkinson disease

Indexed keywords

ADENOVIRUS VECTOR; ALPHA SYNUCLEIN; BRAIN DERIVED NEUROTROPHIC FACTOR; SPINOPHILIN; CORTICOSTERONE; CORTICOTROPIN;

ADENO ASSOCIATED VIRUS; ANIMAL EXPERIMENT; ARTICLE; BRAIN REGION; CELL DENSITY; CELL LOSS; DEPRESSION; DOPAMINERGIC NERVE CELL; DORSOLATERAL STRIATUM; ELEVATED PLUS MAZE TEST; FEMALE; FORCED SWIM TEST; HYPOTHALAMUS HYPOPHYSIS SYSTEM; LOCOMOTION; MOTOR DYSFUNCTION; NERVE CELL; NERVE CELL PLASTICITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RAT; SUBSTANTIA NIGRA; SUCROSE PREFERENCE TEST; VENTRAL TEGMENTUM; ANIMAL; BLOOD; COMPLICATION; DEPENDOPARVOVIRUS; DISEASE MODEL; FOOD PREFERENCE; GENE EXPRESSION REGULATION; GENETICS; HUMAN; LONGITUDINAL STUDY; MAZE TEST; MENTAL STRESS; MESENCEPHALON; METABOLISM; PATHOLOGY; PHYSIOLOGY; PSYCHOLOGY; PSYCHOMOTOR PERFORMANCE; SPRAGUE DAWLEY RAT; SWIMMING; TIME FACTOR; TRANSGENIC RAT;

ADRENOCORTICOTROPIC HORMONE; ALPHA-SYNUCLEIN; ANIMALS; CORTICOSTERONE; DEPENDOVIRUS; DEPRESSION; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; FEMALE; FOOD PREFERENCES; GENE EXPRESSION REGULATION; HUMANS; LONGITUDINAL STUDIES; MAZE LEARNING; MESENCEPHALON; PHENOTYPE; PSYCHOMOTOR PERFORMANCE; RATS; RATS, SPRAGUE-DAWLEY; RATS, TRANSGENIC; STRESS, PSYCHOLOGICAL; SWIMMING; TIME FACTORS;

EID: 84941992072     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2015.09.002     Document Type: Article

References (98)

1. Aarsland D., Pahlhagen S., Ballard C.G., Ehrt U., Svenningsson P. Depression in Parkinson disease-epidemiology, mechanisms and management. Nat. Rev. Neurol. 2011, 8:35-47.
2. Abeliovich A., Schmitz Y., Farinas I., Choi-Lundberg D., Ho W.H., Castillo P.E., Shinsky N., Verdugo J.M., Armanini M., Ryan A., Hynes M., Phillips H., Sulzer D., Rosenthal A. Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 2000, 25:236-252.
3. Allen P.B., Ouimet C.C., Greengard P. Spinophilin, a novel protein phosphatase 1 binding protein localized to dendritic spines. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:9956-9961.
4. Allen P.B., Zachariou V., Svenningsson P., Lepore A.C., Centonze D., Costa C., Rossi S., Bender G., Chen G., Feng J., Snyder G., Bernardi G., Nestler E.J., Yan Z., Calabresi P., Greengard P. Distinct roles for spinophilin and neurabin in dopamine-mediated plasticity. Neuroscience 2006, 140:897-911.
5. Azeredo da Silveira S., Schneider B.L., Cifuentes-Diaz C., Sage D., Abbas-Terki T., Iwatsubo T., Unser M., Aebischer P. Phosphorylation does not prompt, nor prevent, the formation of alpha-synuclein toxic species in a rat model of Parkinson's disease. Hum. Mol. Genet. 2009, 18:872-887.
6. Barbiero J.K., Santiago R.M., Persike D.S., da Silva Fernandes M.J., Tonin F.S., da Cunha C., Lucio Boschen S., Lima M.M., Vital M.A. Neuroprotective effects of peroxisome proliferator-activated receptor alpha and gamma agonists in model of parkinsonism induced by intranigral 1-methyl-4-phenyl-1,2,3,6-tetrahyropyridine. Behav. Brain Res. 2014, 274:390-399.
7. Burré J., Sharma M., Südhof T.C. α-Synuclein assembles into higher-order multimers upon membrane binding to promote SNARE complex formation. Proc. Natl. Acad. Sci. U. S. A. 2014, 111:E4274-E4283.
8. Campos F.L., Carvalho M.M., Cristovão A.C., Je G., Baltazar G., Salgado A.J., Kim Y.S., Sousa N. Rodent models of Parkinson's disease: beyond the motor symptomatology. Front. Behav. Neurosci. 2013, 7(175):1-11.
9. Castro A.A., Wiemes B.P., Matheus F.C., Lapa F.R., Viola G.G., Santos A.R., Tasca C.I., Prediger R.D. Atorvastatin improves cognitive, emotional and motor impairments induced by intranasal 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine (MPTP) administration in rats, an experimental model of Parkinson's disease. Brain Res. 2013, 1513:103-116.
10. Chaudhuri K.R., Schapira A.H. Non-motor symptoms of Parkinson's disease: dopaminergic pathophysiology and treatment. Lancet Neurol. 2009, 8:464-474.
11. Chaudhuri K.R., Healy D.G., Schapira A.H. Non-motor symptoms of Parkinson's disease: diagnosis and management. Lancet Neurol. 2006, 5:235-245.
12. Chowdhury S., Shepherd J.D., Okuno H., Lyford G., Petralia R.S., Plath N., Kuhl D., Huganir R.L., Worley P.F. Arc/Arg3.1 interacts with the endocytic machinery to regulate AMPA receptor trafficking. Neuron 2006, 52:445-459.
13. Clayton D.F., George J.M. The synucleins: a family of proteins involved in synaptic function, plasticity, neurodegeneration and disease. Trends Neurosci. 1998, 21:249-254.
14. Conner J.M., Lauterborn J.C., Yan Q., Gall C.M., Varon S. Distribution of brain derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J. Neurosci. 1997, 17:2295-2313.
15. Cryan J.F., Holmes A. The ascent of mouse: advances in modelling human depression and anxiety. Nat. Rev. Drug Discov. 2005, 4:775-790.
16. Cryan J.F., Lucki I. Antidepressant-like behavioral effects mediated by 5-hydroxytryptamine 2C receptors. J. Pharmacol. Exp. Ther. 2002, 295:1120-1126.
17. Cummings J.L. Depression and Parkinson's disease. Am. J. Psychiatry 1992, 149:443-454.
18. Dauer W., Przedborski S. Parkinson's disease: mechanisms and models. Neuron 2003, 39:889-909.
19. Decressac M., Ulusoy A., Mattsson B., Georgievska B., Romero-Ramos M., Kirik D., Björklund A. GDNF fails to exert neuroprotection in a rat alpha-synuclein model of Parkinson's disease. Brain J. Neurol. 2011, 134:2302-2311.
20. Decressac M., Kadkhodaei B., Mattsson B., Laguna A., Perlmann T., Björklund A. α-Synuclein-induced down-regulation of Nurr1 disrupts GDNF signaling in nigral dopamine neurons. Sci. Transl. Med. 2012, 4(163ra156):1-5.
21. Decressac M., Mattsson B., Björklund A. Comparison of the behavioural and histological characteristics of the 6-OHDA and alpha-synuclein rat models of Parkinson's disease. Exp. Neurol. 2012, 235:306-315.
22. Decressac M., Mattsson B., Lundblad M., Weikop P., Björklund A. Progressive neurodegenerative and behavioural changes induced by AAV-mediated overexpression of alpha-synuclein in midbrain dopamine neurons. Neurobiol. Dis. 2012, 45:939-953.
23. Delaville C., Deurwaerdère P.De, Benazzouz A. Noradrenaline and Parkinson's disease. Front. Syst. Neurosci. 2011, 5:31.
24. Den Oudsten B., Van Heck G., De Vries J. Quality of life and related concepts in Parkinson's disease: a systematic review. Mov. Disord. 2007, 22:1528-1537.
25. Detke M.J., Rickels M., Lucki I. Active behaviors in the rat forced swimming test differentially produced by serotonergic and noradrenergic antidepressants. Psychopharmacology (Berlin) 1995, 121:66-72.
26. Dluzen D.E., Story G.M., Xu K., Kucera J., Walro J.M. Alterations in nigrostriatal dopaminergic function within BDNF mutant mice. Exp. Neurol. 1999, 160:500-507.
27. Donai H., Sugiura H., Ara D., Yoshimura Y., Yamagata K., Yamauchi T. Interaction of Arc with CaM kinase II and stimulation of neurite extension by Arc in neuroblastoma cells expressing CaM kinase II. Neurosci. Res. 2003, 47:399-408.
28. Drui G., Carnicella S., Carcenac C., Favier M., Bertrand A., Boulet S., Savasta M. Loss of dopaminergic nigrostriatal neurons accounts for the motivational and affective deficits in Parkinson's disease. Mol. Psychiatry 2014, 19(3):358-367.
29. Duman R.S., Aghajanian G.K. Synaptic dysfunction in depression: potential therapeutic targets. Science 2012, 338:68-72.
30. Ehringer H., Hornykiewicz O. Distribution of noradrenaline and dopamine (3-hydroxytyramine) in the human brain and their behavior in diseases of the extrapyramidal system. Klin. Wochenschr. 1960, 38:1236-1239.
31. Feany M.B., Bender W.W. A Drosophila model of Parkinson's disease. Nature 2000, 404:394-398.
32. Feeney D.M., Gonzalez A., Law W.A. Amphetamine, haloperidol, and experience interact to affect rate of recovery after motor cortex injury. Science 1982, 217:855-857.
33. Fernagut P.O., Chesselet M.F. Alpha-synuclein and transgenic mouse models. Neurobiol. Dis. 2004, 17:123-130.
34. Fitzgerald P.J., Barkus C., Feyder M., Wiedholz L.M., Chen Y.C., Karlsson R.M., Machado-Vieira R., Graybeal C., Sharp T., Zarate C., Harvey-White J., Du J., Sprengel R., Gass P., Bannerman D., Holmes A. Does gene deletion of AMPA GluA1 phenocopy features of schizoaffective disorder?. Neurobiol. Dis. 2010, 40:608-621.
35. Fosnaugh J.S., Bhat R.V., Yamagata K., Worley P., Baraban J.M. Activation of Arc, a putative "effector" immediate early gene, by cocaine in rat brain. J. Neurochem. 1995, 64:2377-2380.
36. Freichel C., Neumann M., Ballard T., Muller V., Woolley M., Ozmen L., Borroni E., Kretzschmar H.A., Haass C., Spooren W., Kahle P.J. Age-dependent cognitive decline and amygdala pathology in alpha-synuclein transgenic mice. Neurobiol. Aging 2007, 28:1421-1435.
37. Frisina P., Haroutunian V., Libow L. The neuropathological basis for depression in Parkinson's disease. Parkinsonism Relat. Disord. 2009, 15:144-148.
38. Fujimoto T., Tanaka H., Kumamaru E., Okamura K., Miki N. Arc interacts with microtubules/microtubule-associated protein 2 and attenuates microtubule- associated protein 2 immunoreactivity in the dendrites. J. Neurosci. Res. 2004, 76:51-63.
39. Fumagalli F., Racagni G., Colombo E., Riva M.A. BDNF gene expression is reduced in the frontal cortex of dopamine transporter knockout mice. Mol. Psychiatry 2003, 8:898-899.
40. Gorbatyuk O.S., Li S., Sullivan L.F., Chen W., Kondrikova G., Manfredsson F.P., Mandel R.J., Muzyczka N. The phosphorylation state of Ser-129 in human alpha-synuclein determines neurodegeneration in a rat model of Parkinson disease. Proc. Natl. Acad. Sci. U. S. A. 2008, 105:763-768.
41. Hemmerle A., Herman J., Seroog K. Stress, depression and Parkinson's disease. Exp. Neurol. 2012, 233:79-86.
42. Howells D.W., Porritt M.J., Wong J.Y., Batchelor P.E., Kalnins R., Hughes A.J., Donnan G.A. Reduced BDNF mRNA expression in the Parkinson's disease substantia nigra. Exp. Neurol. 2000, 166:127-135.
43. Huang E.J., Reichardt L.F. Neurotrophins: roles in neuronal development and function. Annu. Rev. Neurosci. 2001, 24:677-736.
44. Isacson O., Deacon T.W., Pakzaban P., Galpern W.R., Dinsmore J., Burns L.H. Transplanted xenogeneic neural cells in neurodegenerative disease models exhibit remarkable axonal target specificity and distinct growth patterns of glial and axonal fibres. Nat. Med. 1995, 1:1189-1194.
45. Jankovic J. Parkinson's disease: clinical features and diagnosis. J. Neurol. Neurosurg. Psychiatry 2008, 79:368-376.
46. Kirik D., Rosenblad C., Burger C., Lundberg C., Johansen T.E., Muzyczka N., Mandel R.J., Björklund A. Parkinson-like neurodegeneration induced by targeted overexpression of alpha-synuclein in the nigrostriatal system. J. Neurosci. 2002, 22:2780-2791.
47. Klein R.L., King M.A., Hamby M.E., Meyer E.M. Dopaminergic cell loss induced by human A30P alpha-synuclein gene transfer to the rat substantia nigra. Hum. Gene Ther. 2002, 13:605-612.
48. Kohno R., Sawada H., Kawamoto Y., Uemura K., Shibasaki H., Shimohama S. BDNF is induced by wild-type alpha-synuclein but not by the two mutants, A30P or A53T, in glioma cell line. Biochem. Biophys. Res. Commun. 2004, 318:113-118.
49. Lang A.E., Lozano A.M. Parkinson's disease: first of two parts. N. Engl. J. Med. 1998, 339:1044-1053.
50. Langston J.W. The Parkinson's complex: parkinsonism is just the tip of the iceberg. Ann. Neurol. 2006, 59:591-596.
51. Lauwers E., Debyser Z., Van Dorpe J., De Strooper B., Nuttin B., Baekelandt V. Neuropathology and neurodegeneration in rodent brain induced by lentiviral vector-mediated overexpression of alpha-synuclein. Brain Pathol. 2003, 13:364-372.
52. Lee V.M., Trojanowski J.Q. Mechanisms of Parkinson's disease linked to pathological alpha-synuclein: new targets for drug discovery. Neuron 2006, 52:33-38.
53. Lee F.J., Liu F., Pristupa Z.B., Niznik H.B. Direct binding and functional coupling of alpha-synuclein to the dopamine transporters accelerate dopamine-induced apoptosis. FASEB J. 2001, 15:916-926.
54. Lima M., Martins E., Delattre A., Proenc M., Mori M., Carabelli B. Motor and non-motor features of Parkinson's disease: a review of clinical and experimental studies. CNS Neurol. Disord. Drug Targets 2012, 11:439-449.
55. Lo Bianco C., Ridet J.L., Schneider B.L., Deglon N., Aebischer P. Alpha-synucleinopathy and selective dopaminergic neuron loss in a rat lentiviral-based model of Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:10813-10818.
56. Lucki I. The forced swimming test as a model for core and component behavioral effects of antidepressant drugs. Behav. Pharmacol. 1997, 8:523-532.
57. Lundblad M., Chesselet M., Mattsson B., Björklund A. Impaired neurotransmission caused by overexpression of alpha-synuclein in nigral dopamine neurons. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:3213-3219.
58. Lyford G.L., Yamagata K., Kaufmann W.E., Barnes C.A., Sanders L.K., Copeland N.G., Gilbert D.J., Jenkins N.A., Lanahan A.A., Worley P. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 1995, 14:433-445.
59. Magen I., Fleming S.M., Zhu C., Garcia E.C., Cardiff K.M., Dinh D., De La Rosa K., Sanchez M., Torres E.R., Masliah E., Jentsch J.D., Chesselet M.F. Cognitive deficits in a mouse model of pre-manifest Parkinson's disease. Eur. J. Neurosci. 2012, 35:870-882.
60. Marinus J., Leentjens A., Visser M., Stiggelbout A., van Hilten J. Evaluation of the hospital anxiety and depression scale in patients with Parkinson's disease. Clin. Neuropharmacol. 2002, 25:318-324.
61. Martin L.J., Pan Y., Price A.C., Sterling W., Copeland N.G., Jenkins N.A., Price D.L., Lee M.K. Parkinson's disease alpha-synuclein transgenic mice develop neuronal mitochondrial degeneration and cell death. J. Neurosci. 2006, 26:41-50.
62. Martinez-Martin P., Damian J. Parkinson disease: depression and anxiety in Parkinson disease. Nat. Rev. Neurol. 2010, 6:243-245.
63. Masliah E., Rockenstein E., Mante M., Crews L., Spencer B., Adame A., Patrick C., Trejo M., Ubhi K., Rohn T.T., Mueller-Steiner S., Seubert P., Barbour R., McConlogue L., Buttini M., Games D., Schenk D. Passive immunization reduces behavioral and neuropathological deficits in an alpha-synuclein transgenic model of Lewy body disease. PLoS One 2011, 6(e19338):1-17.
64. McEwen B.S. Glucocorticoids, depression, and mood disorders: structural remodeling in the brain. Metabolism 2005, 54:20-23.
65. Menza M., Robertson-Hoffman D., Bonapace A. Parkinson's disease and anxiety: cormorbidity and depression. Biol. Psychiatry 1993, 34:465-470.
66. Mochizuki H., Yamada M., Mizuno Y. Alpha-synuclein overexpression model. J. Neural Transm. Suppl. 2006, 70:281-284.
67. Mogi M., Togari A., Kondo T., Mizuno Y., Komure O., Kuno S., Ichinose H., Nagatsu T. Brain-derived growth factor and nerve growth factor concentrations are decreased in the substantia nigra in Parkinson's disease. Neurosci. Lett. 1999, 270:45-48.
68. Müller T., Welnic J., Muhlack S. Acute levodopa administration reduces cortisol release in patients with Parkinson's disease. J. Neural Transm. 2007, 114:347-350.
69. Muly E.C., Smith Y., Allen P., Greengard P. Subcellular distribution of spinophilin immunolabeling in primate prefrontal cortex: localization to and within dendritic spines. J. Comp. Neurol. 2004, 469:185-197.
70. Murer M.G., Yan Q., Raisman-Vozari R. Brain-derived neurotrophic factor in the control human brain, and in Alzheimer's disease and Parkinson's disease. Prog. Neurobiol. 2001, 63:71-124.
71. Parain K., Murer M.G., Yan Q., Faucheux B., Agid Y., Hirsch E., Raisman-Vozari R. Reduced expression of brain-derived neurotrophic factor protein in Parkinson's disease substantia nigra. NeuroReport 1999, 10:557-561.
72. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2007, Elsevier Academic Press, San Diego. 6th ed.
73. Perez R.G., Waymire J.C., Lin E., Liu J.J., Guo F., Zigmond M.J. A role for alpha-synuclein in the regulation of dopamine biosynthesis. J. Neurosci. 2002, 22:3090-3099.
74. Pogorelov V., Rodriguiz R., Insco M., Caron M.G., Wetsel W. Novelty seeking and stereotypic activation of behavior in mice with disruption of the Dat1 gene. Neuropsychopharmacology 2005, 30:1818-1831.
75. Porritt M.J., Batchelor P.E., Howells D.W. Inhibiting BDNF expression by antisense oligonucleotide infusion causes loss of nigral dopaminergic neurons. Exp. Neurol. 2005, 192:226-234.
76. Porsolt R.D., Le Pichon M., Jalfre M. Depression: a new animal model sensitive to antidepressant treatments. Nature 1977, 266:730-732.
77. Reijnders J.S., Ehrt U., Weber W.E., Aarsland D., Leentjens A.F. A systematic review of prevalence studies of depression in Parkinson's disease. Mov. Disord. 2008, 23:183-189.
78. Santiago R.M., Barbiero J., Gradowski R.W., Bochen S., Lima M.M., Da Cunha C., Andreatini R., Vital M.A. Induction of depressive-like behavior by intranigral 6-OHDA is directly correlated with deficits in striatal dopamine and hippocampal serotonin. Behav. Brain Res. 2014, 259:70-77.
79. Santiago R.M., Tonin F.S., Barbiero J., Zaminelli T., Boschen S.L., Andreatini R., Da Cunha C., Lima M.M., Vital M.A. The nonsteroidal antiinflammatory drug piroxicam reverses the onset of depressive-like behavior in 6-OHDA animal model of Parkinson's disease. Neuroscience 2015, 300:246-253.
80. Satoh A., Nakanishi H., Obaishi H., Wada M., Takahashi K., Satoh K., Hirao K., Nishioka H., Hata Y., Mizoguchi A., Takai Y. Neurabin-II/spinophilin. An actin filament-binding protein with one pdz domain localized at cadherin-based cell-cell adhesion sites. J. Biol. Chem. 1998, 273:3470-3475.
81. Schallert T., Woodlee M.T. Motor systems: orienting and placing. The Behavior of the Laboratory Rat: A Handbook With Tests 2005, 129-140. Oxford University Press, New York. I.Q. Whishaw, B. Kolb (Eds.).
82. Schintu N., Zhang X., Svenningsson P. Studies of depression-related states in animal models of Parkinsonism. J. Parkinson's Dis. 2012, 2:87-106.
83. Shiba M., Bower J., Maraganore D., McDonald S., Peterson B., Ahlskog J., Schiad D., Rocca W. Anxiety and depressive disorders preceding Parkinson's disease: a case control study. Mov. Disord. 2000, 15:669-677.
84. Shirayama Y., Chen A.C., Nakagawa S., Russell D.S., Duman R.S. Brain-derived neurotrophic factor produces antidepressant effects in behavioral models of depression. J. Neurosci. 2002, 22:3251-3261.
85. Siuciak J.A., Lewis D.R., Wiegand S.J., Lindsay R.M. Antidepressant-like effect of brain-derived neurotrophic factor (BDNF). Pharmacol. Biochem. Behav. 1997, 56:131-137.
86. Smith F.D., Oxford G.S., Milgram S.L. Association of the D2 dopamine receptor third cytoplasmic loop with spinophilin, a protein phosphatase-1-interacting protein. J. Biol. Chem. 1999, 274:19894-19900.
87. Soh S., Morris M., McGinley J. Determinants of health-related quality of life in Parkinson's disease: a systematic review. Parkinsonism Relat. Disord. 2011, 17:1-9.
88. Steward O., Worley P. Local synthesis of proteins at synaptic sites on dendrites: role in synaptic plasticity and memory consolidation?. Neurobiol. Learn. Mem. 2002, 78:508-527.
89. Takakusaki K. Neurophysiology of gait: from the spinal cord to the frontal lobe. Mov. Disord. 2013, 28:1483-1491.
90. Takakusaki K., Tomita N., Yano M. Substrates for normal gait and pathophysiology of gait disturbances with respect to the basal ganglia dysfunction. J. Neurol. 2008, 255:19-29.
91. Tan A., Moratalla R., Lyford G.L., Worley P., Graybiel A.M. The activity-regulated cytoskeletal associated protein Arc is expressed in different striosome matrix patterns following exposure to amphetamine and cocaine. J. Neurochem. 2000, 74:2074-2078.
92. Ulusoy A., Decressac M., Kirik D., Björklund A. Viral vector-mediated overexpression of alpha-synuclein as a progressive model of Parkinson's disease. Prog. Brain Res. 2010, 184:89-111.
93. Van der Heyden J.A., Zethof T.J., Olivier B. Stress-induced hyperthermia in singly housed mice. Physiol. Behav. 1997, 62:463-470.
94. Walsh S.L., Wagner G.C. Motor impairments after methamphetamine-induced neurotoxicity in the rat. J. Pharmacol. Exp. Ther. 1992, 263:617-626.
95. Willner P., Towell A., Sampson D., Sophokleous S., Muscat R. Reduction of sucrose preference by chronic unpredictable mild stress, and its restoration by a tricyclic antidepressant. Psychopharmacology (Berlin) 1987, 93:358-364.
96. Yamada M., Iwatsubo T., Mizuno Y., Mochizuki H. Overexpression of alphasynuclein in rat substantia nigra results in loss of dopaminergic neurons, phosphorylation of alpha-synuclein and activation of caspase-9: resemblance to pathogenetic changes in Parkinson's disease. J. Neurochem. 2004, 91:451-461.
97. Zhao C.S., Puurunen K., Schallert T., Sivenius J., Jolkkonen J. Behavioral and histological effects of chronic antipsychotic and antidepressant drug treatment in aged rats with focal ischemic brain injury. Behav. Brain Res. 2005, 158:211-220.
98. Zhou X.F., Li W.P., Zhou F.H., Zhong J.H., Mi J.X., Wu L.L., Xian C.J. Differential effects of endogenous brain-derived neurotrophic factor on the survival of axotomized sensory neurons in dorsal root ganglia: a possible role for the p75 neurotrophin receptor. Neuroscience 2005, 132:591-603.