Effects of aging on the interaction between glutamate, dopamine, and GABA in striatum and nucleus accumbens of the awake rat

Journal of Neurochemistry

Volumn 73, Issue 5, 1999, Pages 2063-2072

  Segovia, Gregorio ^a   Del Arco, Alberto ^a   Mora, Francisco ^a  

^a UNIVERSIDAD COMPLUTENSE DE MADRID   (Spain)

Author keywords

Aging; Dopamine; GABA; Glutamate; L trans Pyrrolidine 3,4 dicarboxylic acid; Microdialysis; Nucleus accumbens; Striatum

Indexed keywords

4 AMINOBUTYRIC ACID; DICARBOXYLIC ACID DERIVATIVE; DOPAMINE; GLUTAMIC ACID;

ADOLESCENT; AGED; AGING; ANIMAL EXPERIMENT; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DIALYSATE; MALE; MICRODIALYSIS; MOLECULAR INTERACTION; NONHUMAN; NUCLEUS ACCUMBENS; PRIORITY JOURNAL; RAT; WAKEFULNESS;

ANIMALIA; RATTUS NORVEGICUS;

EID: 0032717249     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.1999.02063.x     Document Type: Article

References (80)

1. 3H]GBR-12935 in human putamen. Neurobiol. Aging 10, 661-664.
2. Araki T., Kato H., Shuto K., Fujiwara T., and Itoyama Y. (1997) Effect of aging on dopaminergic receptors and uptake sites in the rat brain studied by receptor autoradiography. J. Neurol. Sci. 148, 131-137.
3. Attwell D., Barbour B., and Szatkowski M. (1993) Nonvesicular release of neurotransmitter. Neuron 11, 401-407.
4. 3H]kainate studied by autoradiography in rat forebrain. Neurochem. Int. 26, 155-164.
5. Barbour B. and Häusser M. A. (1997) Intersynaptic diffusion of neurotransmitter. Trends Neurosci. 20, 377-384.
6. Bjelke B., Agnati L. F., and Fuxe K. (1991) Experimental evidence for volume transmission by analysis of host-graft interaction using intrastriatal adenohypophyseal transplants in the rat in combination with three-dimensional reconstruction, in Volume Transmission in the Brain: Novel Mechanisms for Neural Transmission (Fuxe K. and Agnati L. F., eds), pp. 463-478. Raven Press, New York.
7. Bouyer J. J., Park D. H., Joh T. H., and Pickel V. M. (1984) Chemical and structural analysis of the relation between cortical inputs and tyrosine hydroxylase-containing terminals in rat neostriatum. Brain Res. 302, 267-275.
8. Bridges R. J., Stanley M. S., Anderson M. W., Cotman C. W., and Camberlin A. R. (1991) Conformationally defined neurotransmitter analogues. Selective inhibition of glutamate uptake by one pyrrolidine-2,4-dicarboxylate diastereomer. J. Med. Chem. 34, 717-725.
9. Carlsson M. and Carlsson A. (1990) Interactions between glutamatergic and monoaminergic systems within the basal ganglia - implications for schizophrenia and Parkinson's disease. Trends Neurosci. 13, 272-276.
10. Carlsson M., Svensson A., and Carlsson A. (1992) Interactions between excitatory amino acids, catecholamines and acetylcholine in the basal ganglia, in Excitatory Amino Acids (Simon R. P., ed), pp. 189-194. Thieme, New York.
11. Castorina M., Ambrosini A. M., Pacifici L., Ramacci M. T., and Angelucci L. (1994) Age-dependent loss of NMDA receptors in hippocampus, striatum, and frontal cortex of the rat: prevention by acetyl-L-carnitine. Neurochem. Res. 19, 795-798.
12. Cepeda C., Li Z., and Levine M. S. (1996) Aging reduces neostriatal responsiveness to N-methyl-D-aspartate and dopamine: an in vitro electrophysiological study in vitro. Neuroscience 73, 733-750.
13. Chen Q., Veenman C. L., and Reiner A. (1996) Cellular expression of ionotropic glutamate receptor subunits on specific striatal neuron types and its implication for striatal vulnerability in glutamate receptor-mediated excitotoxicity. Neuroscience 73, 715-731.
14. Coleman P. D., Mora F., and Nieto-Sampedro M. (1994) Deterioration, stability and regeneration of the brain during normal aging. Institute Juan March de Estudios e Investigaciones, Centre for International Meetings on Biology, Madrid.
15. Corsi C., Pazzagli M., Bianchi L., Della Corte L., Pepeu G., and Pedata F. (1997) In vivo amino acid release from the striatum of aging rats: adenosine modulation. Neurobiol. Aging 18, 243-250.
16. Crawford C. A. and Levine M. S. (1997) Dopaminergic function in the neostriatum and nucleus accumbens of young and aged Fisher 344 rats. Neurobiol. Aging 18, 57-66.
17. David J. F., Ghozali F., Bianco C. F., Wattez A., Delaine S., Boniface B., Di Menza C., and Delacourte A. (1997) Glial reaction in the hippocampal formation is highly correlated with aging in human brain. Neurosci. Lett. 235, 53-56.
18. Del Arco A., González-Mora J. L., Armas V. R., and Mora F. (1999) Amphetamine increases extracellular concentrations of glutamate in striatum of the awake rat: involvement of high affinity transporter mechanisms. Neuropharmacology 38, 943-954.
19. Desce J. M., Godeheu G., Galli T., Artaud F., Cherámy A., and Glowinski J. (1991) Presynaptic facilitation of dopamine release through D,L-alpha-amino-3-hydroxy-5-methyl-4-isoxazole propionate receptors on synaptosomes from the rat striatum. J. Pharmacol Exp. Ther. 259, 692-698.
20. Di Chiara G., Morelli M., and Consolo S. (1994) Modulatory functions of neurotransmitters in the striatum: ACh/DA/NMDA interactions. Trends Neurosci. 17, 228-233.
21. Donzanti B. A., Hite J. F., and Yamamoto B. K. (1993) Extracellular glutamate levels increase with age in the lateral striatum: potential involvement of presynaptic D2 receptors. Synapse 13, 376-382.
22. Expósito I., Mora F., Zisapel N., and Oaknin S. (1995) The modulatory effect of melatonin on the dopamine-glutamate interaction in the anterior hypothalamus during aging. Neuroreport 6, 2399-2403.
23. Felten D. L., Felten S. Y., Fuller R. W., Romano T. D., Smalstig E. B., Wong D. T., and Clemens J. A. (1992) Chronic dietary pergolide preserves nigrostrialal neuronal integrity in aged-Fischer-344 rats. Neurobiol. Aging 13, 339-351.
24. Freund T. F., Powell J. F., and Smith A. D. (1984) Tyrosine hydroxylase-immunoreactive boutons in synaptic contact with identified striatonigral neurons, with particular reference to dendritic spines. Neuroscience 13, 1189-1215.
25. Friedemann M. N. and Gerhardt G. A. (1992) Regional effects of aging on dopaminergic function in the Fischer-344 rat. Neurobiol. Aging 13, 325-332.
26. Garris P. A., Ciolkowski E. L., Pastore P., and Wightman R. M. (1994) Efflux of dopamine from the synaptic cleft in the nucleus accumbens of the rat brain. J. Neurosci. 14, 6084-6093.
27. Gerhardt G. A. and Maloney R. E. (1999) Microdialysis studies of basal levels and stimulus-evoked overflow of dopamine and metabolites in the striatum of young and aged Fischer 344 rats. Brain Res. 816, 68-77.
28. Gonzales R. A., Brown L. M., Jones T. W., Trent R. D., Westbrook S. L., and Leslie S. W. (1991) N-Methyl-D-aspartate mediated responses decrease with age in Fischer 344 rat brain. Neurobiol. Aging 12, 219-225.
29. Goss J. R., Finch C. E., and Morgan D. G. (1991) Age-related changes in glial fibrillary acidic protein mRNA in the mouse brain. Neurobiol. Aging 12, 165-170.
30. Grace A. A. (1991) Phasic versus tonic dopamine release and the modulation of dopamine system responsivity: a hypothesis for the etiology of schizophrenia. Neuroscience 41, 1-24.
31. Greenamyre J. T. (1993) Glutamate-dopamine interactions in the basal ganglia: relationship to Parkinson's disease. J. Neural Transm. 91, 255-269.
32. Groenewegen H. J., Berendse H. W., Meredith G. E., Haber S. N., Voorn P., Wolters J. G., and Lohman A. S. M. (1991) Functional anatomy of the ventral, limbic system-innervated striatum, in The Mesolimbic Dopamine System: From Motivation to Action (Willner P. and Scheel-Krüger J., eds), pp. 19-59. Wiley, Chichester.
33. Huang R.-L., Wang C.-T., Tai M.-Y., Tsai Y.-F., and Peng M.-T. (1995) Effects of age on dopamine release in the nucleus accumbens and amphetamine-induced locomotor activity in rats. Neurosci. Lett. 200, 61-64.
34. Imperato A., Honoré T., and Jensen L. H. (1990) Dopamine release in the nucleus caudatus and in the nucleus accumbens is under glutamatergic control through non-NMDA receptors: a study in freely-moving rats. Brain Res. 530, 223-228.
35. Johnson L. R., Aylward R. L. M., Hussain Z., and Totterdell S. (1994) Input from the amygdala to the rat nucleus accumbens: its relationship with tyrosine hydroxylase immunoreactivity and identified neurons. Neuroscience 61, 851-865.
36. Joseph J. A., Roth G. S., and Strong R. (1990) The striatum, a microcosm for the examination of age-related alterations in the CNS: a selected review. Rev. Biol. Res. Aging 4, 181-199.
37. Kalivas P. W. and Duffy P. (1997) Dopamine regulation of extracellular glutamate in the nucleus accumbens. Brain Res. 761, 173-177.
38. Kametani H., Iijima S., Spangler E. L., Ingram D. K., and Joseph J. A. (1995) In vivo assessment of striatal dopamine release in the aged male Fischer 344 rat. Neurobiol. Aging 16, 639-646.
39. Kanai Y., Stelzner M., Nußberger S., Khawaja S., Hebert S. C., Smith C. P., and Hediger M. A. (1994) The neuronal and epithelial human high affinity glutamate transporter. J. Biol. Chem. 269, 20599-20606.
40. Kendrick K. M., Guevara-Guzman R., De la Riva C., Christensen J., Ostergaard K., and Emson P. C. (1996) NMDA and kainate-evoked release of nitric oxide and classical transmitters in the rat striatum: in vivo evidence that nitric oxide may play a neuroprotective role. Eur. J. Neurosci. 8, 2619-2634.
41. Konig J. R. F. and Klippel R. A. (1967) The Rat Brain. Krieger, New York.
42. Krebs M. O., Desce J. M., Kernel M. L., Gauchy C., Godeheu G., Cheramy A., and Glowinski J. (1991) Glutamatergic control of dopamine release in the rat striatum: evidence for presynaptic N-methyl-D-aspartate receptors on dopaminergic nerve terminals. J. Neurochem. 56, 81-85.
43. Lada M. W., Vickroy T. W., and Kennedy R. T. (1998) Evidence for neuronal origin and metabotropic receptor-mediated regulation of extracellular glutamate and aspartate in rat striatum in vivo following electrical stimulation of the prefrontal cortex. J. Neurochem. 70, 617-625.
44. Levi G., Gallo V., and Patrizio M. (1992) Release of exogenous and endogenous neurotransmitter amino acids from cultured astrocytes, in Progress in Brain Research, Vol. 94: Neuronal-Astrocytic Interactions (Yu A. C. H., Hertz L., Norenberg M. D., Sykova E., and Waxman S. G., eds), pp. 243-250. Elsevier, Amsterdam.
45. Magnusson K. R. and Cotman C. W. (1993) Effects of aging on NMDA and MK801 binding sites in mice. Brain Res. 604, 334-337.
46. Makman M. H. (1993) Influence of normal aging on monoamines, monoamine receptors and associated signal transduction systems, in Neuroregulatory Mechanisms in Aging (Makman M. H. and Stefano G. B., eds), pp. 47-78. Pergamon Press, Oxford.
47. Marczynski T. J. (1998) GABAergic deafferentation hypothesis of brain aging and Alzheimer's disease revisited. Brain Res. Bull. 45, 341-379.
48. Massieu L., Morales-Villagrán A., and Tapia R. (1995) Accumulation of extracellular glutamate by inhibition of its uptake is not sufficient for inducing neuronal damage: an in vivo microdialysis study. J. Neurochem. 64, 2262-2272.
49. Mora F. and Porras A. (1994) Interactions of dopamine, excitatory amino acids and inhibitory amino acids in the basal ganglia of the conscious rat, in The Basal Ganglia IV: New Ideas and Data on Structure and Function (Percheron G., McKenzie J. S., and Féger J., eds), pp. 441-447. Plenum Press, New York.
50. Morari M., O'Connor W. T., Ungerstedt U., and Fuxe K. (1993) N-Methyl-D-aspartic acid differentially regulates extracellular dopamine, GABA, and glutamate levels in the dorsolateral neostriatum of the halothane-anesthestized rat: an in vivo microdialysis study. J. Neurochem. 60, 1884-1893.
51. Obrenovitch T. P., Urenjak J., and Zilkha E. (1996) Evidence disputing the link between seizure activity and high extracellular glutamate. J. Neurochem. 66, 2446-2454.
52. Ohno M. and Watanabe S. (1995) Persistent increase in dopamine release following activation of metabotropic glutamate receptors in the rat nucleus accumbens. Neurosci. Lett. 200, 113-116.
53. Pepeu G. (1988) Acetylcholine and brain aging. Pharmacol. Res. Commun. 20, 91-97.
54. Pierce R. C. and Kalivas P. W. (1997) A circuitry model of the expression of behavioral sensitization to amphetamine-like psychostimulants. Brain Res. Rev. 25, 192-216.
55. Porras A. and Mora F. (1995) Dopamine-glutamate-GABA interactions and ageing: studies in the striatum of the conscious rat. Eur. J. Neurosci. 7, 2183-2188.
56. Porras A., Sanz B., and Mora F. (1997) Dopamine-glutamate interactions in the prefrontal cortex of the conscious rat: studies on ageing. Mech. Ageing Dev. 99, 9-17.
57. Queen A., Meeker D., Kim J.-H., and Vezina P. (1998) Dopamine is necessary for nucleus accumbens (1S,3R)-ACPD-induced locomotion. Soc. Neurosci. Abstr. 24, 585.
58. Robinson T. E. and Whishaw I. Q. (1988) Normalization of extracellular dopamine in striatum following recovery from a partial unilateral 6-OHDA lesion of the substantia nigra: a microdialysis study in freely moving rats. Brain Res. 450, 209-224.
59. Sacaan A. I., Bymaster F. P., and Schoepp D. D. (1992) Metabotropic glutamate receptor activation produces extrapyramidal motor system activation that is mediated by striatal dopamine. J. Neurochem. 59, 245-251.
60. Santiago M., Machado A., and Cano J. (1993) Effects of age and dopamine agonists and antagonists on striatal dopamine release in the rat: an in vivo microdialysis study. Mech. Ageing Dev. 67, 261-267.
61. Schneider J. S., Rothblat D. S., and DiStefano L. (1994) Volume transmission of dopamine over large distances may contribute to recovery from experimental parkinsonism. Brain Res. 643, 86-91.
62. Segovia G. and Mora F. (1998) Role of nitric oxide in modulating the release of dopamine, glutamate, and GABA in striatum of the freely moving rat. Brain Res. Bull. 45, 275-279.
63. Segovia G., Del Arco A., and Mora F. (1997a) Endogenous glutamate increases extracellular concentrations of dopamine, GABA, and taurine through NMDA and AMPA/kainate receptors in striatum of the freely moving rat: a microdialysis study. J. Neurochem. 69, 1476-1483.
64. Segovia G., Porras A., and Mora F. (1997b) Effects of 4-aminopyridine on extracellular concentrations of glutamate in striatum of the freely moving rat. Neurochem. Res. 22, 1491-1497.
65. Sesack S. R. and Pickel V. M. (1990) In the rat medial nucleus accumbens, hippocampal and catecholaminergic terminals converge on spiny neurons and are in apposition to each other. Brain Res. 527, 266-279.
66. Sesack S. R. and Pickel V. M. (1992) Prefrontal cortical efferents in the rat synapse on unlabeled neuronal targets of catecholamine terminals in the nucleus accumbens septi and dopamine neurons in the ventral tegmental area. J. Comp. Neurol. 320, 145-160.
67. 3H]dopamine uptake in rat striatum during aging. J. Neurochem. 56, 575-579.
68. Smith A. D. and Bolam J. P. (1990) The neural network of the basal ganglia as revealed by the study of synaptic connections of identified neurones. Trends Neurosci. 13, 259-265.
69. Snedecor W. G. and Cochran G. W. (1989) Statistical Methods. Iowa State University Press, Ames.
70. Svensson L., Zhang J., Johannessen K., and Engel J. A. (1994) Effect of local infusion of glutamate analogues into the nucleus accumbens of rats: an electrochemical and behavioural study. Brain Res. 643, 155-161.
71. Tarazi F. I., Campbell A., Yeghiayan S. K., and Baldessarini R. J. (1998) Localization of ionotropic glutamate receptors in caudate-putamen and nucleus accumbens septi of rat brain: comparison of NMDA, AMPA, and kainate receptors. Synapse 30, 227-235.
72. Terry R. D. (1986) Interrelations among the lesions of normal and abnormal aging of the brain, in Progress in Brain Research, Vol. 70: Aging of the Brain and Alzheimer's Disease (Swaab D. F., Fliers E., Mirmiran M., Van Gool W. A., and Van Haaren F., eds), pp. 41-48. Elsevier, Amsterdam.
73. Thomsen C., Hansen L., and Suzdak P. D. (1994) L-Glutamate uptake inhibitors may stimulate phosphoinositide hydrolysis in baby hamster kidney cells expressing mGluRla via heteroexchange with L-glutamate without direct activation of mGluR1a. J. Neurochem. 63, 2038-2047.
74. Van Horne C., Hoffer B. J., Strömberg I., and Gerhardt G. A. (1992) Clearance and diffusion of locally applied dopamine in normal and 6-hydroxydopamine-lesioned rat striatum. J. Pharmacol. Exp. Ther. 263, 1285-1292.
75. Vázquez M. T., Prados J., Puerta A. J., and Mora F. (1992) Increase of astrocyte population in the medial prefrontal cortex of the rat during aging. Eur. J. Neurosci. 5(Suppl.), 100.
76. Wardas J., Pietraszek M., Schulze G., Ossowska K., and Wolfarth S. (1997) Age-related changes in glutamate receptors: an autoradiographic analysis. Pol. J. Pharmacol. 49, 401-410.
77. Wenk G. L., Walker L. C., Price D. L., and Corks L. C. (1991) Loss of NMDA, but not GABA-A, binding in the brains of aged rats and monkeys. Neurobiol. Aging 12, 93-98.
78. Youngren K. D., Daly D. A., and Moghaddam B. (1993) Distinct actions of endogenous excitatory amino acids on the outflow of dopamine in the nucleus accumbens. J. Pharmacol. Exp. Ther. 264, 289-293.
79. Zigmond M. J., Abercrombie E. D., Berger T. W., Grace A. A., and Stricker E. M. (1990) Compensation after lesions of central dopaminergic neurons: some clinical and basic implications. Trends Neurosci. 13, 290-296.
80. Zoli M., Torri C., Ferrari R., Jansson A., Zini I., Fuxe K., and Agnati L. F. (1998) The emergence of the volume transmission concept. Brain Res. Rev. 26, 136-147.