Nonmotor symptoms in Parkinson's disease: Investigating early-phase onset of behavioral dysfunction in the 6-hydroxydopamine-lesioned rat model

Journal of Neuroscience Research

Volumn 86, Issue 9, 2008, Pages 2050-2061

  Branchi, Igor ^a   D'Andrea, Ivana ^a   Armida, Monica ^a   Cassano, Tommaso ^b   Pèzzola, Antonella ^a   Potenza, Rosa Luisa ^a   Morgese, Maria Grazia ^b   Popoli, Patrizia ^a   Alleva, Enrico ^a  

^a ISTITUTO SUPERIORE DI SANITÀ   (Italy)

^b UNIVERSITY OF FOGGIA   (Italy)

Author keywords

Anxiety; BDNF; Depression; Dopamine; Emotional

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DOPAMINE; OXIDOPAMINE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANXIETY; ARTICLE; BEHAVIOR DISORDER; CONTROLLED STUDY; CORPUS STRIATUM; DEPRESSION; DISEASE MODEL; EMOTION; FACE VALIDITY; LEARNING; MALE; MEMORY; NERVE DEGENERATION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; SOCIAL BEHAVIOR; SYMPTOM; WISTAR RAT;

ANIMALS; BEHAVIOR, ANIMAL; DISEASE MODELS, ANIMAL; MALE; MAZE LEARNING; MOTOR ACTIVITY; OXIDOPAMINE; PARKINSONIAN DISORDERS; RATS; RATS, WISTAR; SWIMMING;

EID: 48349148611     PISSN: 03604012     EISSN: 10974547     Source Type: Journal    
DOI: 10.1002/jnr.21642     Document Type: Article

References (79)

1. Aarsland D, Larsen JP, Lim NG, Janvin C, Karlsen K, Tandberg E, Cummings JL. 1999. Range of neuropsychiatric disturbances in patients with Parkinson's disease. J Neurol Neurosurg Psychiatry 67:492-496.
2. Aid T, Kazantseva A, Piirsoo M, Palm K, Timmusk T. 2007. Mouse and rat BDNF gene structure and expression revisited. J Neurosci Res 85: 525-535.
3. Allain H, Schuck S, Mauduit N. 2000. Depression in Parkinson's disease. Br Med J 320:1287-1288.
4. Alleva E. 1993. Assessment of aggressive behaviour in rodents. In: Conn MP, editor. Methods in neuroscience. Paradigms for the study of behavior. New York: Academic Press. p 111-137.
5. Amalric M, Koob GF. 1987. Depletion of dopamine in the caudate nucleus but not in nucleus accumbens impairs reaction-time performance in rats. J Neurosci 7:2129-2134.
6. Amalric M, Moukhles H, Nieoullon A, Daszuta A. 1995. Complex deficits on reaction time performance following bilateral intrastriatal 6-OHDA infusion in the rat. Eur J Neurosci 7:972-980.
7. Bankiewicz KS, Sanchez-Pernaute R, Oiwa Y, Kohutnicka M, Cummins A, Eberling J. 1999. Preclinical models of Parkinson's disease. Curr Protoc Neurosci 1-32[suppl 9]:9.41-9.432.
8. Baquet ZC, Bickford PC, Jones KR. 2005. Brain-derived neurotrophic factor is required for the establishment of the proper number of dopaminergic neurons in the substantia nigra pars compacta. J Neurosci 25:6251-6259.
9. Bell IR, Amend D, Kaszniak AW, Schwartz GE, Peterson JM, Stini WA, Miller JW, Selhub J. 1995. Trait shyness in the elderly: evidence for an association with Parkinson's disease in family members and biochemical correlates. J Geriatr Psychiatry Neurol 8:16-22.
10. Blandini F, Nappi G, Tassorelli C, Martignoni E. 2000. Functional changes of the basal ganglia circuitry in Parkinson's disease. Prog Neurobiol 62:63-88.
11. Boeve BF. 2007. Parkinson-related dementias. Neurol Clin 25:761-781.
12. Borsini F, Meli A. 1988. Is the forced swimming test a suitable model for revealing antidepressant activity? Psychopharmacology 94:147-160.
13. Branchi I, D'Andrea I, Fiore M, Di Fausto V, Aloe L, Alleva E. 2006a. Early social enrichment shapes social behavior and nerve growth factor and brain-derived neurotrophic factor levels in the adult mouse brain. Biol Psychiatry 60:690-696.
14. Branchi I, D'Andrea I, Sietzema J, Fiore M, Di Fausto V, Aloe L, Alleva E. 2006b. Early social enrichment augments adult hippocampal BDNF levels and survival of BrdU-positive cells while increasing anxiety- and "depression"-like behavior. J Neurosci Res 83:965-973.
15. Burn DJ. 2002. Beyond the iron mask: towards better recognition and treatment of depression associated with Parkinson's disease. Mov Disord 17:445-454.
16. Chaudhuri KR, Healy DG, Schapira AH. 2006. Non-motor symptoms of Parkinson's disease: diagnosis and management. Lancet Neurol 5: 235-245.
17. Chen G, Chen KS, Knox J, Inglis J, Bernard A, Martin SJ, Justice A, McConlogue L, Games D, Freedman SB, Morris RG. 2000. A learning deficit related to age and beta-amyloid plaques in a mouse model of Alzheimer's disease. Nature 408:975-979.
18. Chiarotti F, Alleva E, Bignami G. 1987. Problems of test choice and data analysis in behavioral teratology: the case of prenatal benzodiazepines. Neurotoxicol Teratol 9:179-186.
19. de Almeida RM, Ferrari PF, Parmigiani S, Miczek KA. 2005. Escalated aggressive behavior: dopamine, serotonin and GABA. Eur J Pharmacol 526:51-64.
20. Ebert AD, Hann HJ, Bohn MC. 2007. Progressive degeneration of dopamine neurons in 6-hydroxydopamine rat model of Parkinson's disease does not involve activation of caspase-9 and caspase-3. J Neurosci Res (in press).
21. Emre M. 2003. Dementia associated with Parkinson's disease. Lancet Neurol 2:229-237.
22. File SE. 1993. The interplay of learning and anxiety in the elevated plus maze. Behav Brain Res 58:199-202.
23. File SE. 2001. Factors controlling measures of anxiety and responses to novelty in the mouse. Behav Brain Res 125:151-157.
24. File SE, Seth P. 2003. A review of 25 years of the social interaction test. Eur J Pharmacol 463:35-53.
25. 123I-FP-CIT semi-quantitative SPECT detects pre-clinical bilateral dopaminergic deficit in early Parkinson's disease with unilateral symptoms. Nucl Med Commun 26:421-426.
26. Grant KA, Shively CA, Nader MA, Ehrenkaufer RL, Line SW, Morton TE, Gage HD, Mach RH. 1998. Effect of social status on striatal dopamine D-2 receptor binding characteristics in cynomolgus monkeys assessed with positron emission tomography. Synapse 29:80-83.
27. Gualtieri CT, Schroeder SR. 1990. Pharmacotherapy for self-injurious behavior: preliminary tests of the D1 hypothesis. Prog Neuropsychopharmacol Biol Psychiatry 14(Suppl):S81-S107.
28. Hirsch E, Graybiel AM, Agid YA. 1988. Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature 334:345-348.
29. Holmes A, Rodgers RJ. 1998. Responses of Swiss-Webster mice to repeated plus maze experience: further evidence for a qualitative shift in emotional state? Pharmacol Biochem Behav 60:473-488.
30. Ichitani Y, Okamura H, Nakahara D, Nagatsu I, Ibata Y. 1994. Biochemical and immunocytochemical changes induced by intrastriatal 6-hydroxydopamine injection in the rat nigrostriatal dopamine neuron system: evidence for cell death in the substantia nigra. Exp Neurol 130:269-278.
31. Jonsson G. 1980. Chemical neurotoxins as denervation tools in neurobiology. Annu Rev Neurosci 3:169-187.
32. Lang AE, Quinn N, Brincat S, Marsden CD, Parkes JD. 1982. Pergolide in late-stage Parkinson disease. Ann Neurol 12:243-247.
33. Langston JW. 2006. The Parkinson's complex: parkinsonism is just the tip of the iceberg. Ann Neurol 59:591-596.
34. Lauterbach EC, Duvoisin RC. 1991. Anxiety disorders in familial parkinsonism. Am J Psychiatry 148:274.
35. Lee CS, Sauer H, Bjorklund A. 1996. Dopaminergic neuronal degeneration and motor impairments following axon terminal lesion by instrastriatal 6-hydroxydopamine in the rat. Neuroscience 72:641-653.
36. Lieberman A. 2006. Are dementia and depression in Parkinson's disease related? J Neurol Sci 248:138-142.
37. Lindner MD, Plone MA, Francis JM, Blaney TJ, Salamone JD, Emerich DF. 1997. Rats with partial striatal dopamine depletions exhibit robust and long-lasting behavioral deficits in a simple fixed-ratio bar-pressing task. Behav Brain Res 86:25-40.
38. Lotharius J, Brundin P. 2002. Pathogenesis of Parkinson's disease: dopamine, vesicles and alpha-synuclein. Nat Rev Neurosci 3:932-942.
39. Macht M, Schwarz R, Ellgring H. 2005. Patterns of psychological problems in Parkinson's disease. Acta Neurol Scand 111:95-101.
40. McAllister AK, Katz LC, Lo DC. 1999. Neurotrophins and synaptic plasticity. Annu Rev Neurosci 22:295-318.
41. McDougle CJ, Holmes JP, Carlson DC, Pelton GH, Cohen DJ, Price LH. 1998. A double-blind, placebo-controlled study of risperidone in adults with autistic disorder and other pervasive developmental disorders. Arch Gen Psychiatry 55:633-641.
42. McGaugh JL, Roozendaal B. 2002. Role of adrenal stress hormones in forming lasting memories in the brain. Curr Opin Neurobiol 12:205-210.
43. Menza MA, Robertson-Hoffman DE, Bonapace AS. 1993. Parkinson's disease and anxiety: comorbidity with depression. Biol Psychiatry 34:465-470.
44. Morgan D, Grant KA, Gage HD, Mach RH, Kaplan JR, Prioleau O, Nader SH, Buchheimer N, Ehrenkaufer RL, Nader MA. 2002. Social dominance in monkeys: dopamine D-2 receptors and cocaine self-administration. Nat Neurosci 5:169-174.
45. Morton DB. 2000. A systematic approach for establishing humane end-points. Ilar J 41:80-86.
46. Nilsson FM, Kessing LV, Bolwig TG. 2001. Increased risk of developing Parkinson's disease for patients with major affective disorder: a register study. Acta Psychiatr Scand 104:380-386.
47. Numan S, Seroogy KB. 1997. Increased expression of trkB mRNA in rat caudate-putamen following 6-OHDA lesions of the nigrostriatal pathway. Eur J Neurosci 9:489-495.
48. Olanow CW, Tatton WG. 1999. Etiology and pathogenesis of Parkinson's disease. Annu Rev Neurosci 22:123-144.
49. Padovani A, Costanzi C, Gilberti N, Borroni B. 2006. Parkinson's disease and dementia. Neurol Sci 27(Suppl 1):S40-S43.
50. Paxinos G, Watson C. 1982. The rat brain in stereotaxic coordinates. New York: Academic Press.
51. Petit-Demouliere B, Chenu F, Bourin M. 2005. Forced swimming test in mice: a review of antidepressant activity. Psychopharmacology 177: 245-255.
52. Porsolt RD, Le Pichon M, Jalfre M. 1977. Depression: a new animal model sensitive to antidepressant treatments. Nature 266:730-732.
53. Porsolt RD, Anton G, Blavet N, Jalfre M. 1978. Behavioural despair in rats: a new model sensitive to antidepressant treatments. Eur J Pharmacol 47:379-391.
54. Przedborski S, Levivier M, Jiang H, Ferreira M, Jackson-Lewis V, Donaldson D, Togasaki DM. 1995. Dose-dependent lesions of the dopaminergic nigrostriatal pathway induced by intrastriatal injection of 6-hydroxydopamine. Neuroscience 67:631-647.
55. Remy P, Doder M, Lees A, Turjanski N, Brooks D. 2005. Depression in Parkinson's disease: loss of dopamine and noradrenaline innervation in the limbic system. Brain 128:1314-1322.
56. Rodgers RJ, Dalvi A. 1997. Anxiety, defence and the elevated plus maze. Neurosci Biobehav Rev 21:801-810.
57. Roedter A, Winkler C, Samii M, Walter GF, Brandis A, Nikkhah G. 2001. Comparison of unilateral and bilateral intrastriatal 6-hydroxydopamine-induced axon terminal lesions: evidence for interhemispheric functional coupling of the two nigrostriatal pathways. J Comp Neurol 432:217-229.
58. Saarelainen T, Hendolin P, Lucas G, Koponen E, Sairanen M, MacDonald E, Agerman K, Haapasalo A, Nawa H, Aloyz R, Ernfors P, Castren E. 2003. Activation of the TrkB neurotrophin receptor is induced by antidepressant drugs and is required for antidepressant-induced behavioral effects. J Neurosci 23:349-357.
59. Salamone JD, Mahan K, Rogers S. 1993. Ventrolateral striatal dopamine depletions impair feeding and food handling in rats. Pharmacol Biochem Behav 44:605-610.
60. Schmidt RH, Björklund A, Stenevi U, Dunnett SB, Gage FH. 1983. Intracerebral grafting of neuronal cell suspensions. III. Activity of intrastriatal nigral suspension implants as assessed by measurements of dopamine synthesis and metabolism. Acta Physiol Scand Suppl 522:19-28.
61. Schurman AG, van den Akker M, Ensinck KT, Metsemakers JF, Knottnerus JA, Leentjens AF, Buntinx F. 2002. Increased risk of Parkinson's disease after depression: a retrospective cohort study. Neurology 58: 1501-1504.
62. Schwarting RK, Huston JP. 1996. Unilateral 6-hydroxydopamine lesions of meso-striatal dopamine neurons and their physiological sequelae. Prog Neurobiol 49:215-266.
63. Sharma V, Smith A. 2007. A case of mania following the use of pramipexole. Am J Psychiatry 164:351.
64. Singh A, Althoff R, Martineau RJ, Jacobson J. 2005. Pramipexole, ropinirole, and mania in Parkinson's disease. Am J Psychiatry 162:814-815.
65. Slaughter JR, Slaughter KA, Nichols D, Holmes SE, Martens MP. 2001. Prevalence, clinical manifestations, etiology, and treatment of depression in Parkinson's disease. J Neuropsychiatry Clin Neurosci 13:187-196.
66. Soderstrom H, Blennow K, Manhem A, Forsman A. 2001. CSF studies in violent offenders - I. 5-HIAA as a negative and HVA as a positive predictor of psychopathy. J Neural Transm 108:869-878.
67. Stefanova E. 2003. Depression in Parkinson's disease. Ann Gen Hosp Psychiatry 2(Suppl 1):S12.
68. Tiihonen J, Kuikka J, Bergstrom K, Lepola U, Koponen H, Leinonen E. 1997. Dopamine reuptake site densities in patients with social phobia. Am J Psychiatry 154:239-242.
69. van Erp AM, Miczek KA. 2000. Aggressive behavior, increased accumbal dopamine, and decreased cortical serotonin in rats. J Neurosci 20:9320-9325.
70. van Oosten RV, Cools AR. 2002. Differential effects of a small, unilateral, 6-hydroxydopamine-induced nigral lesion on behavior in high and low responders to novelty. Exp Neurol 173:245-255.
71. Vazquez A, Jimenez-Jimenez FJ, Garcia-Ruiz P, Garcia-Urra D. 1993. "Panic attacks" in Parkinson's disease. A long-term complication of levodopa therapy. Acta Neurol Scand 87:14-18.
72. Wakamatsu M, Iwata S, Funakoshi T, Yoshimoto M. 2007. Dopamine receptor agonists reverse behavioral abnormalities of alpha-synuclein transgenic mouse, a new model of Parkinson's disease. J Neurosci Res (in press).
73. Walsh K, Bennett G. 2001. Parkinson's disease and anxiety. Postgrad Med J 77:89-93.
74. Weintraub D, Moberg PJ, Duda JE, Katz IR, Stern MB. 2004. Effect of psychiatric and other nonmotor symptoms on disability in Parkinson's disease. J Am Geriatr Soc 52:784-788.
75. Wilcox RR. 1987. New statistical procedures for the social sciences. Modern solutions to basic problems. Hillsdale, NJ: Lawrence Erlbaum.
76. Yuan H, Sarre S, Ebinger G, Michotte Y. 2004. Neuroprotective and neurotrophic effect of apomorphine in the striatal 6-OHDA-lesion rat model of Parkinson's disease. Brain Res 1026:95-107.
77. Yudofsky SC, Stevens L, Silver J, Barsa J, Williams D. 1984. Propranolol in the treatment of rage and violent behavior associated with Korsakoff's psychosis. Am J Psychiatry 141:114-115.
78. Zhou J, Pliego-Rivero B, Bradford HF, Stern GM. 1996. The BDNF content of postnatal and adult rat brain: the effects of 6-hydroxydopamine lesions in adult brain. Brain Res Dev Brain Res 97: 297-303.
79. Zorner B, Wolfer DP, Brandis D, Kretz O, Zacher C, Madani R, Grunwald I, Lipp HP, Klein R, Henn FA, Gass P. 2003. Forebrain-specific trkB-receptor knockout mice: behaviorally more hyperactive than "depressive." Biol Psychiatry 54:972-982.