Aging of the rat mesostriatal system: Differences between the nigrostriatal and the mesolimbic compartments

Experimental Neurology

Volumn 204, Issue 1, 2007, Pages 147-161

  Cruz Muros, Ignacio ^a   Afonso Oramas, Domingo ^a   Abreu, Pedro ^a   Barroso Chinea, Pedro ^a   Rodríguez, Manuel ^a   González, M Carmen ^a   Hernández, Tomás González ^a  

^a UNIVERSIDAD DE LA LAGUNA   (Spain)

Author keywords

Alpha synuclein; Amyloid precursor protein; Differential vulnerability; Dopaminergic; Elderly; Parkinson's disease

Indexed keywords

ALPHA SYNUCLEIN; AMYLOID; AROMATIC LEVO AMINO ACID DECARBOXYLASE; DOPAMINE; LEVODOPA; TYROSINE 3 MONOOXYGENASE;

AGING; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DEGENERATION; DOPAMINE METABOLISM; DOPAMINERGIC DEGENERATION; DOPAMINERGIC SYSTEM; ENZYME ACTIVITY; LIMBIC CORTEX; MALE; NERVE FIBER DEGENERATION; NIGRONEOSTRIATAL SYSTEM; NONHUMAN; NUCLEOTIDE SEQUENCE; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN AGGREGATION; RAT; STRIATE CORTEX;

AGING; ALPHA-SYNUCLEIN; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; AXONS; CORPUS STRIATUM; DOPA DECARBOXYLASE; DOPAMINE; LEVODOPA; LIMBIC SYSTEM; MALE; NERVE DEGENERATION; PHOSPHORYLATION; RATS; RATS, SPRAGUE-DAWLEY; SUBSTANTIA NIGRA; TYROSINE 3-MONOOXYGENASE;

EID: 33847255845     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2006.10.004     Document Type: Article

References (107)

1. Abreu P., Santana C., Hernandez G., Calzadilla C.H., and Alonso R. Day-night rhythm of rat pineal tyrosine hydroxylase activity as determined by HPLC with amperometric detection. J. Neurochem. 48 (1987) 665-668
2. Bannon M.J., Poosch M.S., Xia Y., Goebel D.J., Cassin B., and Kapatos G. Dopamine transporter mRNA content in human substantia nigra decreases precipitously with age. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 7095-7099
3. Barili P., De Carolis G., Zaccheo D., and Amenta F. Sensitivity to ageing of the limbic dopaminergic system: a review. Mech. Ageing Dev. 106 (1998) 57-92
4. Beeson J.G., Shelton E.R., Chan H.W., and Gage F.H. Age and damage induced changes in amyloid protein precursor immunohistochemistry in the rat brain. J. Comp. Neurol. 342 (1994) 69-77
5. Beeson J.G., Shelton E.R., Chan H.W., and Gage F.H. Differential distribution of amyloid protein precursor immunoreactivity in the rat brain studied by using five different antibodies. J. Comp. Neurol. 342 (1994) 78-96
6. Bennett M.C. The role of alpha-synuclein in neurodegenerative diseases. Pharmacol. Ther. 105 (2005) 311-331
7. Bernheimer H., Birkmayer W., Hornykiewicz O., Jellinger K., and Seitelberger F. Brain dopamine and the syndromes of Parkinson and Huntington. Clinical, morphological and neurochemical correlations. J. Neurol. Sci. 20 (1973) 415-455
8. Bevilaqua L.R., Graham M.E., Dunkley P.R., von Nagy-Felsobuki E.I., and Dickson P.W. Phosphorylation of Ser(19) alters the conformation of tyrosine hydroxylase to increase the rate of phosphorylation of Ser(40). J. Biol. Chem. 276 (2001) 40411-40416
9. Brooks D.J., Ibanez V., Sawle G.V., Quinn N., Lees A.J., Mathias C.J., Bannister R., Marsden C.D., and Frackowiak R.S. Differing patterns of striatal 18F-dopa uptake in Parkinson's disease, multiple system atrophy, and progressive supranuclear palsy. Ann. Neurol. 28 (1990) 547-555
10. Brown A.S., and Gershon S. Dopamine and depression. J. Neural Transm.: Gen. Sect. 91 (1993) 75-109
11. Burns R.S., Chiueh C.C., Markey S.P., Ebert M.H., Jacobowitz D.M., and Kopin I.J. A primate model of parkinsonism: selective destruction of dopaminergic neurons in the pars compacta of the substantia nigra by N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine. Proc. Natl. Acad. Sci. U. S. A. 80 (1983) 4546-4550
12. Cabello C.R., Thune J.J., Pakkenberg H., and Pakkenberg B. Ageing of substantia nigra in humans: cell loss may be compensated by hypertrophy. Neuropathol. Appl. Neurobiol. 28 (2002) 283-291
13. Calne D.B., and Langston J.W. Aetiology of Parkinson's disease. Lancet 2 (1983) 1457-1459
14. Carfagna N., Trunzo F., and Moretti A. Brain catecholamine content and turnover in aging rats. Exp. Gerontol. 20 (1985) 265-269
15. Chiueh C.C., Burns R.S., Markey S.P., Jacobowitz D.M., and Kopin I.J. Primate model of parkinsonism: selective lesion of nigrostriatal neurons by 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine produces an extrapyramidal syndrome in rhesus monkeys. Life Sci. 36 (1985) 213-218
16. Christenson J.G., Dairman W., and Udenfriend S. Preparation and properties of a homogeneous aromatic l-amino acid decarboxylase from hog kidney. Arch. Biochem. Biophys. 141 (1970) 356-367
17. Cordes M., Snow B.J., Cooper S., Schulzer M., Pate B.D., Ruth T.J., and Calne D.B. Age-dependent decline of nigrostriatal dopaminergic function: a positron emission tomographic study of grandparents and their grandchildren. Ann. Neurol. 36 (1994) 667-670
18. Cottrell B.A., Galvan V., Banwait S., Gorostiza O., Lombardo C.R., Williams T., Schilling B., Peel A., Gibson B., Koo E.H., Link C.D., and Bredesen D.E. A pilot proteomic study of amyloid precursor interactors in Alzheimer's disease. Ann. Neurol. 58 (2005) 277-289
19. Dahlström A., and Fuxe K. Evidence for the existence of monoamine-containing neurons in the central nervous system: I. Demonstration of monoamines in the cell bodies of brain stem neurons. Acta Physiol. Scand. 62 Suppl. 232 (1964) 1-55
20. Damier P., Hirsch E.C., Agid Y., and Graybiel A.M. The substantia nigra of the human brain: II. Patterns of loss of dopamine-containing neurons in Parkinson's disease. Brain 122 Pt 8 (1999) 1437-1448
21. Diederich N.J., Moore C.G., Leurgans S.E., Chmura T.A., and Goetz C.G. Parkinson disease with old-age onset: a comparative study with subjects with middle-age onset. Arch. Neurol. 60 (2003) 529-533
22. Dunkley P.R., Bobrovskaya L., Graham M.E., von Nagy-Felsobuki E.I., and Dickson P.W. Tyrosine hydroxylase phosphorylation: regulation and consequences. J. Neurochem. 91 (2004) 1025-1043
23. Emerich D.F., McDermott P., Krueger P., Banks M., Zhao J., Marszalkowski J., Frydel B., Winn S.R., and 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
24. Fallon J.H., and Moore R.Y. Catecholamine innervation of the basal forebrain: IV. Topography of the dopamine projection to the basal forebrain and neostriatum. J. Comp. Neurol. 180 (1978) 545-580
25. Fearnley J.M., and Lees A.J. Ageing and Parkinson's disease: substantia nigra regional selectivity. Brain 114 Pt 5 (1991) 2283-2301
26. Frank C., Pari G., and Rossiter J.P. Approach to diagnosis of Parkinson disease. Can. Fam. Physician 52 (2006) 862-868
27. Friedemann M.N., and Gerhardt G.A. Regional effects of aging on dopaminergic function in the Fischer-344 rat. Neurobiol. Aging 13 (1992) 325-332
28. Gerhardt G.A., Cass W.A., Yi A., Zhang Z., and Gash D.M. Changes in somatodendritic but not terminal dopamine regulation in aged rhesus monkeys. J. Neurochem. 80 (2002) 168-177
29. German D.C., Manaye K.F., Sonsalla P.K., and Brooks B.A. Midbrain dopaminergic cell loss in Parkinson's disease and MPTP-induced parkinsonism: sparing of calbindin-D28k-containing cells. Ann. N. Y. Acad. Sci. 648 (1992) 42-62
30. Gibb W.R., and Lees A.J. Anatomy, pigmentation, ventral and dorsal subpopulations of the substantia nigra, and differential cell death in Parkinson's disease. J. Neurol. Neurosurg. Psychiatry 54 (1991) 388-396
31. Godefroy F., Bassant M.H., Lamour Y., and Weil-Fugazza J. Effect of aging on dopamine metabolism in the rat cerebral cortex: a regional analysis. J. Neural Transm.: Gen. Sect. 83 (1991) 13-24
32. Goldstein M., Lee K.Y., Lew J.Y., Harada K., Wu J., Haycock J.W., Hokfelt T., and Deutch A.Y. Antibodies to a segment of tyrosine hydroxylase phosphorylated at serine 40. J. Neurochem. 64 (1995) 2281-2287
33. Gonzalez-Hernandez T., and Rodriguez M. Compartmental organization and chemical profile of dopaminergic and GABAergic neurons in the substantia nigra of the rat. J. Comp. Neurol. 421 (2000) 107-135
34. Gonzalez-Hernandez T., Barroso-Chinea P., De La Cruz Muros I., Del Mar Perez-Delgado M., and Rodriguez M. Expression of dopamine and vesicular monoamine transporters and differential vulnerability of mesostriatal dopaminergic neurons. J. Comp. Neurol. 479 (2004) 198-215
35. Gunawardena S., and Goldstein L.S. Disruption of axonal transport and neuronal viability by amyloid precursor protein mutations in Drosophila. Neuron 32 (2001) 389-401
36. Gupta M., Stoler M.H., Fossom L.H., and Tank A.W. Tyrosine hydroxylase mRNA in the dopaminergic neurons of young adult and aged mice by in situ hybridization. Neurosci. Lett. 119 (1990) 49-52
37. Harada N., Nishiyama S., Satoh K., Fukumoto D., Kakiuchi T., and Tsukada H. Age-related changes in the striatal dopaminergic system in the living brain: a multiparametric PET study in conscious monkeys. Synapse 45 (2002) 38-45
38. Harman D. Aging: a theory based on free radical and radiation chemistry. J. Gerontol. 11 (1956) 298-300
39. Haycock J.W., and Wakade A.R. Activation and multiple-site phosphorylation of tyrosine hydroxylase in perfused rat adrenal glands. J. Neurochem. 58 (1992) 57-64
40. Haycock J.W., Becker L., Ang L., Furukawa Y., Hornykiewicz O., and Kish S.J. Marked disparity between age-related changes in dopamine and other presynaptic dopaminergic markers in human striatum. J. Neurochem. 87 (2003) 574-585
41. Hebert M.A., and Gerhardt G.A. Age-related changes in the capacity, rate, and modulation of dopamine uptake within the striatum and nucleus accumbens of Fischer 344 rats: an in vivo electrochemical study. J. Pharmacol. Exp. Ther. 288 (1999) 879-887
42. Hirsch E., Graybiel A.M., and Agid Y.A. Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature 334 (1988) 345-348
43. Hof P.R., and Morrison J.H. The aging brain: morphomolecular senescence of cortical circuits. Trends Neurosci. 27 (2004) 607-613
44. Hung H.C., and Lee E.H. The mesolimbic dopaminergic pathway is more resistant than the nigrostriatal dopaminergic pathway to MPTP and MPP+ toxicity: role of BDNF gene expression. Brain Res. Mol. Brain Res. 41 (1996) 14-26
45. Irwin I., DeLanney L.E., McNeill T., Chan P., Forno L.S., Murphy Jr. G.M., Di Monte D.A., Sandy M.S., and Langston J.W. Aging and the nigrostriatal dopamine system: a non-human primate study. Neurodegeneration 3 (1994) 251-265
46. Joel D., and Weiner I. The connections of the dopaminergic system with the striatum in rats and primates: an analysis with respect to the functional and compartmental organization of the striatum. Neuroscience 96 (2000) 451-474
47. Kamenetz F., Tomita T., Hsieh H., Seabrook G., Borchelt D., Iwatsubo T., Sisodia S., and Malinow R. APP processing and synaptic function. Neuron 37 (2003) 925-937
48. Kang U.J., Park D.H., Wessel T., Baker H., and Joh T.H. Dopa-decarboxylation in the striata of rats with unilateral substantia nigra lesions. Neurosci. Lett. 147 (1992) 53-57
49. Kish S.J., Shannak K., Rajput A., Deck J.H., and Hornykiewicz O. Aging produces a specific pattern of striatal dopamine loss: implications for the etiology of idiopathic Parkinson's disease. J. Neurochem. 58 (1992) 642-648
50. Kish S.J., Zhong X.H., Hornykiewicz O., and Haycock J.W. Striatal 3,4-dihydroxyphenylalanine decarboxylase in aging: disparity between postmortem and positron emission tomography studies?. Ann. Neurol. 38 (1995) 260-264
51. Kubis N., Faucheux B.A., Ransmayr G., Damier P., Duyckaerts C., Henin D., Forette B., Le Charpentier Y., Hauw J.J., Agid Y., and Hirsch E.C. Preservation of midbrain catecholaminergic neurons in very old human subjects. Brain 123 Pt 2 (2000) 366-373
52. Kuhlmann T., Lingfeld G., Bitsch A., Schuchardt J., and Bruck W. Acute axonal damage in multiple sclerosis is most extensive in early disease stages and decreases over time. Brain 125 (2002) 2202-2212
53. Lau F.C., Shukitt-Hale B., and Joseph J.A. The beneficial effects of fruit polyphenols on brain aging. Neurobiol. Aging 26 Suppl. 1 (2005) 128-132
54. Lee K.Y., Lew J.Y., Tang D., Schlesinger D.H., Deutch A.Y., and Goldstein M. Antibodies to a synthetic peptide corresponding to a Ser-40-containing segment of tyrosine hydroxylase: activation and immunohistochemical localization of tyrosine hydroxylase. J. Neurochem. 53 (1989) 1238-1244
55. Leenders K.L., Palmer A.J., Quinn N., Clark J.C., Firnau G., Garnett E.S., Nahmias C., Jones T., and Marsden C.D. Brain dopamine metabolism in patients with Parkinson's disease measured with positron emission tomography. J. Neurol. Neurosurg. Psychiatry 49 (1986) 853-860
56. Levitt M., Spector S., Sjoerdsma A., and Udenfriend S. Elucidation of the rate-limiting step in norepinephrine biosynthesis in the perfused guinea-pig heart. J. Pharmacol. Exp. Ther. 148 (1965) 1-8
57. Machado A., Cano J., and Santiago M. The change with age in biogenic amines and their metabolites in the striatum of the rat. Arch. Gerontol. Geriatr. 5 (1986) 333-342
58. Marshall J.F., and Rosenstein A.J. Age-related decline in rat striatal dopamine metabolism is regionally homogeneous. Neurobiol. Aging 11 (1990) 131-137
59. Martin W.R., Palmer M.R., Patlak C.S., and Calne D.B. Nigrostriatal function in humans studied with positron emission tomography. Ann. Neurol. 26 (1989) 535-542
60. Masliah E., Mallory M., Hansen L., DeTeresa R., and Terry R.D. Quantitative synaptic alterations in the human neocortex during normal aging. Neurology 43 (1993) 192-197
61. McGeer P.L., McGeer E.G., and Suzuki J.S. Aging and extrapyramidal function. Arch. Neurol. 34 (1977) 33-35
62. McKenzie K.J., McLellan D.R., Gentleman S.M., Maxwell W.L., Gennarelli T.A., and Graham D.I. Is beta-APP a marker of axonal damage in short-surviving head injury?. Acta Neuropathol. (Berl. ) 92 (1996) 608-613
63. McNeill T.H., and Koek L.L. Differential effects of advancing age on neurotransmitter cell loss in the substantia nigra and striatum of C57BL/6N mice. Brain Res. 521 (1990) 107-117
64. McRitchie D.A., Hardman C.D., and Halliday G.M. Cytoarchitectural distribution of calcium binding proteins in midbrain dopaminergic regions of rats and humans. J. Comp. Neurol. 364 (1996) 121-150
65. Miguez J.M., Aldegunde M., Paz-Valinas L., Recio J., and Sanchez-Barcelo E. Selective changes in the contents of noradrenaline, dopamine and serotonin in rat brain areas during aging. J. Neural. Transm. 106 (1999) 1089-1098
66. Muller, P.Y., Janovjak, H., Miserez, A.R.,Dobbie, Z., 2002. Processing of gene expression data generated by quantitative real-time RT-PCR, BioTechniques 32, 1372-1374, 1376, 1378-1379.
67. Nieoullon A., and Coquerel A. Dopamine: a key regulator to adapt action, emotion, motivation and cognition. Curr. Opin. Neurol. 16 Suppl. 2 (2003) S3-S9
68. Norris E.H., Giasson B.I., and Lee V.M. Alpha-synuclein: normal function and role in neurodegenerative diseases. Curr. Top. Dev. Biol. 60 (2004) 17-54
69. Pakkenberg H., Andersen B.B., Burns R.S., and Pakkenberg B. A stereological study of substantia nigra in young and old rhesus monkeys. Brain Res. 693 (1995) 201-206
70. Pania, L.,Gessab, G.L., 2002. Dopaminergic deficit and mood disorders, Int Clin Psychopharmacol 17 Suppl 4, S1-7; discussion S7.
71. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates (1998), Academic Press, Orlando, FL
72. Povlishock J.T., and Kontos H.A. The role of oxygen radicals in the pathobiology of traumatic brain injury. Hum. Cell 5 (1992) 345-353
73. Rapp P.R., and Gallagher M. Preserved neuron number in the hippocampus of aged rats with spatial learning deficits. Proc. Natl. Acad. Sci. U. S. A. 93 (1996) 9926-9930
74. Rasmussen T., Schliemann T., Sorensen J.C., Zimmer J., and West M.J. Memory impaired aged rats: no loss of principal hippocampal and subicular neurons. Neurobiol. Aging 17 (1996) 143-147
75. Reeves S., Bench C., and Howard R. Ageing and the nigrostriatal dopaminergic system. Int. J. Geriatr. Psychiatry 17 (2002) 359-370
76. Remy P., Doder M., Lees A., Turjanski N., and Brooks D. Depression in Parkinson's disease: loss of dopamine and noradrenaline innervation in the limbic system. Brain 128 (2005) 1314-1322
77. Rodriguez M., Barroso-Chinea P., Abdala P., Obeso J., and Gonzalez-Hernandez T. Dopamine cell degeneration induced by intraventricular administration of 6-hydroxydopamine in the rat: similarities with cell loss in Parkinson's disease. Exp. Neurol. 169 (2001) 163-181
78. Roediger B., and Armati P.J. Oxidative stress induces axonal beading in cultured human brain tissue. Neurobiol. Dis. 13 (2003) 222-229
79. Ross C.A., and Poirier M.A. Protein aggregation and neurodegenerative disease. Nat. Med. 10 (2004) S10-S17 (Suppl.)
80. Russo C., Venezia V., Repetto E., Nizzari M., Violani E., Carlo P., and Schettini G. The amyloid precursor protein and its network of interacting proteins: physiological and pathological implications. Brain Res. Brain Res. Rev. 48 (2005) 257-264
81. Saito Y., Ruberu N.N., Sawabe M., Arai T., Kazama H., Hosoi T., Yamanouchi H., and Murayama S. Lewy body-related alpha-synucleinopathy in aging. J. Neuropathol. Exp. Neurol. 63 (2004) 742-749
82. Salamone J.D. The involvement of nucleus accumbens dopamine in appetitive and aversive motivation. Behav. Brain Res. 61 (1994) 117-133
83. Sawle G.V., Colebatch J.G., Shah A., Brooks D.J., Marsden C.D., and Frackowiak R.S. Striatal function in normal aging: implications for Parkinson's disease. Ann. Neurol. 28 (1990) 799-804
84. Schipper H.M. Brain iron deposition and the free radical-mitochondrial theory of ageing. Ageing Res. Rev. 3 (2004) 265-301
85. Schuligoi R., Fernandez J., Heavens R.P., and Sirinathsinghji D.J. Decreased tyrosine hydroxylase mRNA but not cholecystokinin mRNA in the pars compacta of the substantia nigra and ventral tegmental area of aged rats. Brain Res. Mol. Brain Res. 19 (1993) 333-338
86. Sofroniew M.V. Neuronal responses to axotomy. In: Koerdower J. (Ed). CNS regeneration (1999), Academic Press, San Diego 3-26
87. Spillantini M.G., Schmidt M.L., Lee V.M., Trojanowski J.Q., Jakes R., and Goedert M. Alpha-synuclein in Lewy bodies. Nature 388 (1997) 839-840
88. Squier T.C. Oxidative stress and protein aggregation during biological aging. Exp. Gerontol. 36 (2001) 1539-1550
89. Stanford J.A., Vorontsova E., Surgener S.P., Gerhardt G.A., and Fowler S.C. Aged Fischer 344 rats exhibit altered orolingual motor function: relationships with nigrostriatal neurochemical measures. Neurobiol. Aging 24 (2003) 259-266
90. Sutherland C., Alterio J., Campbell D.G., Le Bourdelles B., Mallet J., Haavik J., and Cohen P. Phosphorylation and activation of human tyrosine hydroxylase in vitro by mitogen-activated protein (MAP) kinase and MAP-kinase-activated kinases 1 and 2. Eur. J. Biochem. 217 (1993) 715-722
91. Thal D.R., Del Tredici K., and Braak H. Neurodegeneration in normal brain aging and disease. Sci. Aging Knowledge Environ. (2004) e26
92. Thobois S., Jahanshahi M., Pinto S., Frackowiak R., and Limousin-Dowsey P. PET and SPECT functional imaging studies in Parkinsonian syndromes: from the lesion to its consequences. NeuroImage 23 (2004) 1-16
93. Toledo-Aral J.J., Mendez-Ferrer S., Pardal R., Echevarria M., and Lopez-Barneo J. Trophic restoration of the nigrostriatal dopaminergic pathway in long-term carotid body-grafted parkinsonian rats. J. Neurosci. 23 (2003) 141-148
94. Toska K., Kleppe R., Armstrong C.G., Morrice N.A., Cohen P., and Haavik J. Regulation of tyrosine hydroxylase by stress-activated protein kinases. J. Neurochem. 83 (2002) 775-783
95. Tsai H.W., Shui H.A., Liu H.S., Tai M.Y., and Tsai Y.F. Monoamine levels in the nucleus accumbens correlate with male sexual behavior in middle-aged rats. Pharmacol. Biochem. Behav. 83 (2006) 265-270
96. Udenfriend S., Zaltzman-Nirenberg P., Gordon R., and Spector S. Evaluation of the biochemical effects produced in vivo by inhibitors of the three enzymes involved in norepinephrine biosynthesis. Mol. Pharmacol. 2 (1966) 95-105
97. Uemura E. Age-related changes in the subiculum of Macaca mulatta: synaptic density. Exp. Neurol. 87 (1985) 403-411
98. Venero J.L., Machado A., and Cano J. Turnover of dopamine and serotonin and their metabolites in the striatum of aged rats. J. Neurochem. 56 (1991) 1940-1948
99. Viani P., Cervato G., Fiorilli A., and Cestaro B. Age-related differences in synaptosomal peroxidative damage and membrane properties. J. Neurochem. 56 (1991) 253-258
100. Voogt J.L., Arbogast L.A., Quadri S.K., and Andrews G. Tyrosine hydroxylase messenger RNA in the hypothalamus, substantia nigra and adrenal medulla of old female rats. Brain Res. Mol. Brain Res. 8 (1990) 55-62
101. Watanabe H. Differential decrease in the rate of dopamine synthesis in several dopaminergic neurons of aged rat brain. Exp. Gerontol. 22 (1987) 17-25
102. West M.J. Stereological methods for estimating the total number of neurons and synapses: issues of precision and bias. Trends Neurosci. 22 (1999) 51-61
103. West M.J., Coleman P.D., Flood D.G., and Troncoso J.C. Differences in the pattern of hippocampal neuronal loss in normal ageing and Alzheimer's disease. Lancet 344 (1994) 769-772
104. White N.J., and Barnes T.R. Senile parkinsonism, a study of current treatment. Age Ageing 10 (1981) 81-86
105. Williams R.W., and Rakic P. Three-dimensional counting: an accurate and direct method to estimate numbers of cells in sectioned material. J. Comp. Neurol. 278 (1988) 344-352
106. Wolf M.E., LeWitt P.A., Bannon M.J., Dragovic L.J., and Kapatos G. Effect of aging on tyrosine hydroxylase protein content and the relative number of dopamine nerve terminals in human caudate. J. Neurochem. 56 (1991) 1191-1200
107. Xu Z.Q., Lew J.Y., Harada K., Aman K., Goldstein M., Deutch A., Haycock J.W., and Hokfelt T. Immunohistochemical studies on phosphorylation of tyrosine hydroxylase in central catecholamine neurons using site- and phosphorylation state-specific antibodies. Neuroscience 82 (1998) 727-738