Incomplete nigrostriatal dopaminergic cell loss and partial reductions in striatal dopamine produce akinesia, rigidity, tremor and cognitive deficits in middle-aged rats

Behavioural Brain Research

Volumn 102, Issue 1-2, 1999, Pages 1-16

  Lindner, Mark D ^a   Cain, Chris K ^a   Plone, Melissa A ^a   Frydel, Beata R ^a   Blaney, Thomas J ^a   Emerich, Dwaine F ^b   Hoane, Michael R ^a  

^a CytoTherapeutics Inc   (United States)

^b ALKERMES INC   (United States)

Author keywords

6 OHDA; Age; Nigrostriatal cell counts; Parkinsonian symptoms; Partial lesions

Indexed keywords

DOPAMINE;

AKINESIA; ARTICLE; CELL LOSS; COGNITIVE DEFECT; DOPAMINE BRAIN LEVEL; DOPAMINERGIC NERVE CELL; MALE; NERVE CELL PLASTICITY; NONHUMAN; PARKINSONISM; PRIORITY JOURNAL; RAT; RIGIDITY; TREMOR;

3,4-DIHYDROXYPHENYLACETIC ACID; AGE FACTORS; ANIMALS; BRAIN MAPPING; CORPUS STRIATUM; DEMENTIA; DOPAMINE; DYSKINESIA, DRUG-INDUCED; MALE; MAZE LEARNING; MENTAL RECALL; MOTOR SKILLS; MUSCLE RIGIDITY; NERVE DEGENERATION; OXIDOPAMINE; PARKINSON DISEASE, SECONDARY; RATS; RATS, SPRAGUE-DAWLEY; SUBSTANTIA NIGRA; TREMOR;

EID: 0033049711     PISSN: 01664328     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0166-4328(98)00160-0     Document Type: Article

References (83)

1. Abrous D.N., Dunnett S.B. Paw reaching in rats - the staircase test. Wouterlood F.G. Neuroscience Protocols, Module 3. 1994;19-29 Elsevier, Amsterdam.
2. Brown L.L., Schneider J.S., Lidsky T.I. Sensory and cognitive functions of the basal ganglia. Curr Opin Neurobiol. 7:1997;157-163.
3. Chesler E.J., Salamone J.D. Effects of acute and repeated clozapine injections on cholinomimetic-induced vacuous jaw movements. Pharmacol Biochem Behav. 54:1996;619-624.
4. Coggeshall R.E. A consideration of neural counting methods. Trends Neurosci. 15:1992;9-13.
5. Contin M., Riva R., Martinelli P., Triggs E.J., Albani F., Baruzzi A. Rate of motor response to oral levodopa and the clinical progression of Parkinson's disease. Neurology. 46:1996;1055-1058.
6. Corwin J.V., Vicedomini J.P., Nonneman A.J., Valentino L. Serial lesion effect in rat medial frontal cortex as a function of age. Neurobiol Aging. 3:1982;69-76.
7. Cousins M.S., Salamone J.D. Involvement of ventrolateral striatal dopamine in movement initiation and execution: a microdialysis and behavioral investigation. Neuroscience. 70:1996;849-859.
8. Cousins M.S., Salamone J.D. Skilled motor deficits in rats induced by ventrolateral striatal dopamine depletions: behavioral and pharmacological characterization. Brain Res. 732:1996;186-194.
9. Cousins M.S., Sokolowski J.D., Salamone J.D. Different effects of nucleus accumbens and ventrolateral striatal dopamine depletions on instrumental response selection in the rat. Pharmacol Biochem Behav. 46:1993;943-951.
10. Cousins M.S., Carriero D.L., Salamone J.D. Tremulous jaw movements induced by the acetylcholinesterase inhibitor tacrine: Effects of antiparkinsonian drugs. Eur J Pharmacol. 322:1997;137-145.
11. Croningolomb A., Corkin S., Growdon J.H. Impaired problem solving in Parkinson's disease: impact of a set-shifting deficit. Neuropsychologia. 32:1994;579-593.
12. de Castro J.M., Zrull M.C. Recovery of sensorimotor function after frontal cortex damage in rats: evidence that the serial lesion effect is due to serial recovery. Behav Neurosci. 102:1988;843-851.
13. Dru D., Walker J.B. CNS recovery of function: serial lesion effects. Adv Psychobiol. 3:1976;193-218.
14. Emerich D.F., McDermott P., Krueger P., Banks M., Zhao J., Marszalkowski J., Frydel B., Winn S.R., Sanberg P.R. Locomotion of aged rats: relationship to neurochemical but not morphological changes in nigrostriatal dopaminergic neurons. Brain Res Bull. 32:1993;477-486.
15. Emerich D.F., Plone M.A., Francis J.M., Frydel B.R., Winn S.R., Lindner M.D. Alleviation of behavioral deficits in aged rodents following implantation of encapsulated GDNF-producing fibroblasts. Brain Res. 736:1996;99-110.
16. Fairley P.C., Marshall J.F. Dopamine in the lateral caudate-putamen of the rat is essential for somatosensory orientation. Behav Neurosci. 100:1986;652-663.
17. Fearnley J.M., Lees A.J. Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain. 114:1991;2283-2301.
18. Finger S., Walbran B., Stein D.G. Brain damage and behavioral recovery: serial lesion phenomena. Brain Res. 63:1973;1-18.
19. Finn M., Jassen A., Baskin P., Salamone J.D. Tremulous characteristics of the vacuous jaw movements induced by pilocarpine and ventrolateral striatal dopamine depletions. Pharmacol Biochem Behav. 57:1997;243-249.
20. Giraudo M.D., Gayraud D., Habib M. Visuospatial ability of parkinsonians and elderly adults in location memory tasks. Brain Cognit. 34:1997;259-273.
21. Hagan J.J., Alpert J.E., Morris R.G.M., Iversen S.D. The effects of central catecholamine depletions on spatial learning in rats. Behav Brain Res. 9:1983;83-104.
22. Hornykiewicz O. Parkinson's disease and its chemotherapy. Biochem Pharmacol. 24:1975;1061-1065.
23. Hovestadt A., de Jong G.J., Meerwaldt J.D. Spatial disorientation as an early symptom of Parkinson's disease. Neurology. 37:1987;485-487.
24. Irwin I., Delanney L.E., Mcneill T., Chan P., Forno L.S., Murphy G.M., Dimonte D.A., Sandy M.S., Langston J.W. Aging and the nigrostriatal dopamine system: a non-human primate study. Neurodegeneration. 3:1994;251-265.
25. Janson A.M., Moller A. Chronic nicotine treatment counteracts nigral cell loss induced by a partial mesodiencephalic hemitransection: an analysis of the total number and mean volume of neurons and glia in substantia nigra of the male rat. Neuroscience. 57:1993;931-941.
26. Jicha G.A., Salamone J.D. Vacuous jaw movements and feeding deficits in rats with ventrolateral striatal dopamine depletion: possible relation to Parkinsonian symptoms. J Neurosci. 11:1991;3822-3829.
27. Kish S.J., Shannak K., Hornykiewicz O. Uneven pattern of dopamine loss in the striatum of patients with idiopathic Parkinson's disease. Pathophysiologic and clinical implications. New Engl J Med. 318:1988;876-880.
28. Lange K.W., Paul G.M., Naumann M., Gsell W. Dopaminergic effects on cognitive performance in patients with Parkinson's disease. J Neural Transmission Suppl. 46:1995;423-432.
29. Leenders K.L., Salmon E.P., Tyrrell P., Perani D., Brooks D.J., Sager H., Jones T., Marsden C.D., Frackowiak R.S. The nigrostriatal dopaminergic system assessed in vivo by positron emission tomography in healthy volunteer subjects and patients with Parkinson's disease. Arch Neurol. 47:1990;1290-1298.
30. Lees A.J., Smith E. Cognitive deficits in the early stages of Parkinson's disease. Brain. 106:1983;257-270.
31. Lindner M.D. Reliability, distribution, and validity of age-related cognitive deficits in the Morris water maze. Neurobiol Learn Memory. 68:1997;203-220.
32. Lindner M.D., Balch A.H., VanderMaelen C.P. Short forms of the 'reference'- and 'working-memory' Morris water maze for assessing age-related deficits. Behav Neural Biol. 58:1992;94-102.
33. Lindner M.D., Dworetzky S.I., Sampson C., Loy R. Relationship of APP mRNA transcripts and levels of NGF and low-affinity NGF receptors to behavioral measures of age-related cognitive dysfunction. J Neurosci. 14:1994;2282-2289.
34. Lindner M.D., Winn S.R., Baetge E.E., Hammang J.P., Gentile F.T., Doherty E., McDermott P.E., Frydel B., Ullman M.D., Schallert T., Emerich D.F. Implantation of encapsulated catecholamine and GDNF-producing cells in rats with unilateral dopamine depletions and parkinsonian symptoms. Exp Neurol. 132:1995;62-76.
35. Lindner M.D., Kearns C.E., Winn S.R., Frydel B., Emerich D.F. Effects of intraventricular encapsulated hNGF-secreting fibroblasts in aged rats. Cell Transplant. 5:1996;205-223.
36. Lindner M.D., Plone M.A., Francis J.M., Emerich D.F. Validation of a rodent model of Parkinson's disease: evidence of a therapeutic window for oral Sinemet. Brain Res Bull. 39:1996;367-372.
37. Lindner M.D., Plone M.A., Francis J.M., Blaney T.J., Salamone J.D., Emerich D.F. Rats with partial striatal dopamine depletions exhibit robust and long-lasting behavioral deficits in a simple fixed-ratio bar-pressing task. Behav Brain Res. 86:1997;25-40.
38. Lindner M.D., Plone M.A., Mullins T.D., Winn S.R., Chandonait S.E., Stott J.A., Blaney T.J., Sherman S.S., Emerich D.F. Somatic delivery of catecholamines in the striatum attenuate parkinsonian symptoms and widen the therapeutic window of oral Sinemet in rats. Exp Neurol. 145:1997;130-140.
39. Lindner M.D., Plone M.A., Schallert T., Emerich D.F. Blind rats are not profoundly impaired in the reference memory Morris water maze and cannot be clearly discriminated from rats with cognitive deficits in the cued platform task. Cognitive Brain Res. 5:1997;329-333.
40. Lindner M.D., Plone M.A., Cain C.K., Frydel B., Francis J.M., Emerich D.F., Sutton R.L. Dissociable long-term cognitive deficits after frontal versus sensorimotor cortical contusions. J Neurotrauma. 15:1998;199-216.
41. Lloyd K.G. CNS compensation to dopamine neuron loss in Parkinson's disease. Adv Exp Med Biol. 90:1977;255-266.
42. Ma S.Y., Rinne J.O., Collan Y., Roytta M., Rinne U.K. A quantitative morphometrical study of neuron degeneration in the substantia nigra in Parkinson's disease. J Neurol Sci. 140:1996;40-45.
43. Marshall J.F., Drew M.C., Neve K.A. Recovery of function after mesotelencephalic dopaminergic injury in senescence. Brain Res. 259:1983;249-260.
44. Mayorga A.J., Carriero D.L., Cousins M.S., Gianutsos G., Salamone J.D. Tremulous jaw movements produced by acute tacrine administration: Possible relation to Parkinsonian side effects. Pharmacol Biochem Behav. 56:1997;273-279.
45. Montoya C.P., Astell S., Dunnett S.B. Effects of nigral and striatal grafts on skilled forelimb use in the rat. Prog Brain Res. 82:1990;459-466.
46. Montoya C.P., Campbell-Hope L.J., Pemberton K.D., Dunnett S.B. The 'staircase test': a measure of independent forelimb reaching and grasping abilities in rats. J Neurosci Methods. 36:1991;219-228.
47. Mortimer J.A., Pirozzolo F.J., Hansch E.C., Webster D.D. Relationship of motor symptoms to intellectual deficits in Parkinson's disease. Neurology. 32:1982;133-137.
48. Moy S.S. Impaired acquisition and operant responding after neonatal dopamine depletion in rats. Pharmacol Biochem Behav. 52:1995;433-441.
49. Owen A.M., James M., Leigh P.N., Summers B.A., Marsden C.D., Quinn N.P., Lange K.W., Robbins T.W. Fronto-striatal cognitive deficits at different stages of Parkinson's disease. Brain. 115:1992;1727-1751.
50. Owen A.M., Beksinska M., James M., Leigh P.N., Summers B.A., Marsden C.D., Quinn N.P., Sahakian B.J., Robbins T.W. Visuospatial memory deficits at different stages of Parkinson's disease. Neuropsychologia. 31:1993;627-644.
51. Owen A.M., Iddon J.L., Hodges J.R., Summers B.A., Robbins T.W. Spatial and non-spatial working memory at different stages of Parkinson's disease. Neuropsychologia. 35:1997;519-532.
52. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates. 2nd edn:1986;Academic Press, Orlando, FL.
53. Pillon B., Ertle S., Deweer B., Sarazin M., Agid Y., Dubois B. Memory for spatial location is affected in Parkinson's disease. Neuropsychologia. 34:1996;77-85.
54. Pillon B., Ertle S., Deweer B., Bonnet A.M., Vidailhet M., Dubois B. Memory for spatial location in 'de novo' parkinsonian patients. Neuropsychologia. 35:1997;221-228.
55. Postle B.R., Locascio J.J., Corkin S., Growdon J.H. The time course of spatial and object learning in Parkinson's disease. Neuropsychologia. 35:1997;1413-1422.
56. Rabey J.M., Bass H., Bonuccelli U., Brooks D., Klotz P., Korczyn A.D., Kraus P., Martinezmartin P., Morrish P., Vansauten W., Vanhilten B. Evaluation of the short Parkinson's evaluation scale: a new friendly scale for the evaluation of Parkinson's disease in clinical drug trials. Clin Neuropharmacol. 20:1997;322-337.
57. Ranje C., Ungerstedt U. Lack of acquisition in dopamine denervated animals tested in an underwater Y-maze. Brain Res. 134:1977;95-111.
58. Ransmayr G., Schmidhuber-Eiler B., Karamat E., Engler-Plorer S., Poewe W., Leidlmair K. Visuoperception and visuospatial and visuorotational performance in Parkinson's disease. J Neurol. 235:1987;99-101.
59. Robbins T.W., Giardini V., Jones G.H., Reading P., Sahakian B.J. Effects of dopamine depletion from the caudate-putamen and nucleus accumbens septi on the acquisition and performance of a conditional discrimination task. Behav Brain Res. 38:1990;243-261.
60. Sabol K.E., Neill D.B., Wages S.A., Church W.H., Justice J.B. Dopamine depletion in a striatal subregion disrupts performance of a skilled motor task in the rat. Brain Res. 335:1985;33-43.
61. Sagar H.J., Sullivan E.V., Gabrieli J.D., Corkin S., Growdon J.H. Temporal ordering and short-term memory deficits in Parkinson's disease. Brain. 111:1988;525-539.
62. Saint-Cyr J.A., Taylor A.E., Lang A.E. Procedural learning and neostriatal dysfunction in man. Brain. 111:1988;941-959.
63. Salamone J., Baskin P. Vacuous jaw movements induced by acute reserpine and low-dose apomorphine: Possible model of parkinsonian tremor. Pharmacol Biochem Behav. 53:1996;179-183.
64. Salamone J.D., Kurth P.A., McCullough L.D., Sokolowski J.D., Cousins M.S. The role of brain dopamine in response initiation: effects of haloperidol and regionally specific dopamine depletions on the local rate of instrumental responding. Brain Res. 628:1993;218-226.
65. Salamone J.D., Mahan K., Rogers S. Ventrolateral striatal dopamine depletions impair feeding and food handling in rats. Pharmacol Biochem Behav. 44:1993;605-610.
66. Schallert T. Sensorimotor impairment and recovery of function in brain-damaged rats: reappearance of symptoms during old age. Behav Neurosci. 97:1983;159-164.
67. Schallert T. Aging-dependent emergence of sensorimotor dysfunction in rats recovered from dopamine depletion sustained early in life. Ann New York Acad Sci. 515:1988;108-120.
68. Schallert T., De Ryck M., Whishaw I.Q., Ramirez V.D., Teitelbaum P. Excessive bracing reactions and their control by atropine and L-DOPA in an animal analog of Parkinsonism. Exp Neurol. 64:1979;33-43.
69. Schallert T., Jones T.A., Norton D. A clinically relevant unilateral rat model of Parkinsonian akinesia. J Neural Transplant Plast. 3:1992;332-333.
70. Scherman D., Desnos C., Darchen F., Pollak P., Javoy-Agid F., Agid Y. Striatal dopamine deficiency in Parkinson's disease: role of aging. Ann Neurol. 26:1989;551-557.
71. Schneider J.S., Popecoleman A. Cognitive deficits precede motor deficits in a slowly progressing model of parkinsonism in the monkey. Neurodegeneration. 4:1995;245-255.
72. Schneider J.S., Sun Z.Q., Roeltgen D.P. Effects of dopamine agonists on delayed response performance in chronic low-dose MPTP-treated monkeys. Pharmacol Biochem Behav. 48:1994;235-240.
73. Schneider J.S., Sun Z.Q., Roeltgen D.P. Effects of dihydrexidine, a full dopamine D-1 receptor agonist, on delayed response performance in chronic low dose MPTP-treated monkeys. Brain Res. 663:1994;140-144.
74. Steinpreis R.E., Salamone J.D. The effects of acute haloperidol and reserpine administration on vacuous jaw movements in three different age groups of rats. Pharmacol Biochem Behav. 46:1993;405-409.
75. Taylor J.R., Elsworth J.D., Roth R.H., Sladek J.R. Jr, Redmond D.E. Jr Cognitive and motor deficits in the acquisition of an object retrieval/detour task in MPTP-treated monkeys. Brain. 113:1990;617-637.
76. Tsai C.H., Lu C.S., Hua M.S., Lo W.L., Lo S.K. Cognitive dysfunction in early onset parkinsonism. Acta Neurol Scand. 89:1994;9-14.
77. Wermuth L., Knudsen L., Boldsen J. A study of cognitive functions in young Parkinsonian patients. Acta Neurol Scand. 93:1996;21-24.
78. Whishaw I.Q., Dunnett S.B. Dopamine depletion, stimulation or blockade in the rat disrupts spatial navigation and locomotion dependent upon beacon or distal cues. Behav Brain Res. 18:1985;11-29.
79. Whishaw I.Q., Funk D.R., Hawryluk S.J., Karbashewski E.D. Absence of sparing of spatial navigation, skilled forelimb and tongue use and limb posture in the rat after neonatal dopamine depletion. Physiol Behav. 40:1987;247-253.
80. Wolfarth S., Konieczny J., Smialowska M., Schulze G., Ossowska K. Influence of 6-hydroxydopamine lesion of the dopaminergic nigrostriatal pathway on the muscle tone and electromyographic activity measured during passive movements. Neuroscience. 74:1996;985-996.
81. Zigmond M.J. Do compensatory processes underlie the pre-clinical phase of neurodegenerative disease? Insights from an animal model of parkinsonism. Neurobiol Dis. 4:1997;247-253.
82. Zigmond M.J., Berger T.W., Grace A.A., Stricker E.M. Compensatory responses to nigrostriatal bundle injury. Studies with 6-hydroxydopamine in an animal model of parkinsonism. Mol Chem Neuropathol. 10:1989;185-200.
83. Zigmond M.J., Stricker E.M. Parkinson's disease: studies with an animal model. Life Sci. 35:1984;5-18.