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. 1996 Dec 15;497(Pt 3):745–751. doi: 10.1113/jphysiol.1996.sp021805

The source of physiologically stimulated glutamate efflux from the striatum of conscious rats.

M Miele 1, M G Boutelle 1, M Fillenz 1
PMCID: PMC1160970  PMID: 9003559

Abstract

1. Glutamate in the extracellular compartment of the striatum of freely moving rats was monitored at 5 min intervals using microdialysis and an enzyme-based assay. 2. Basal levels of dialysate glutamate were 3.6 +/- 0.5 microM. Local infusion through the dialysis probe of tetrodotoxin (TTX), cadmium chloride or magnesium chloride produced no reduction in basal levels of glutamate; with the latter two there was, instead, an increase. 3. Neuronal activation stimulated by induced grooming was accompanied by an increase in total glutamate efflux of 47.5 +/- 25.0% above basal level; this increase was not reduced by local infusion of TTX. 4. We propose that the TTX-insensitive release of glutamate in response to physiological stimulation is derived from glial cells and is a Ca(2+)-dependent mechanism triggered by a receptor-mediated release of Ca2+ from internal stores that spreads through the network of astrocytes.

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Selected References

These references are in PubMed. This may not be the complete list of references from this article.

  1. Attwell D., Barbour B., Szatkowski M. Nonvesicular release of neurotransmitter. Neuron. 1993 Sep;11(3):401–407. doi: 10.1016/0896-6273(93)90145-h. [DOI] [PubMed] [Google Scholar]
  2. Berners M. O., Boutelle M. G., Fillenz M. On-line measurement of brain glutamate with an enzyme/polymer-coated tubular electrode. Anal Chem. 1994 Jul 1;66(13):2017–2021. doi: 10.1021/ac00085a016. [DOI] [PubMed] [Google Scholar]
  3. Bonanno G., Pittaluga A., Fedele E., Fontana G., Raiteri M. Glutamic acid and gamma-aminobutyric acid modulate each other's release through heterocarriers sited on the axon terminals of rat brain. J Neurochem. 1993 Jul;61(1):222–230. doi: 10.1111/j.1471-4159.1993.tb03558.x. [DOI] [PubMed] [Google Scholar]
  4. Bonanno G., Raiteri M. Release-regulating presynaptic heterocarriers. Prog Neurobiol. 1994 Dec;44(5):451–462. doi: 10.1016/0301-0082(94)90006-x. [DOI] [PubMed] [Google Scholar]
  5. Boutelle M. G., Fellows L. K., Cook C. Enzyme packed bed system for the on-line measurement of glucose, glutamate, and lactate in brain microdialysate. Anal Chem. 1992 Sep 1;64(17):1790–1794. doi: 10.1021/ac00041a010. [DOI] [PubMed] [Google Scholar]
  6. Boutelle M. G., Zetterström T., Pei Q., Svensson L., Fillenz M. In vivo neurochemical effects of tail pinch. J Neurosci Methods. 1990 Sep;34(1-3):151–157. doi: 10.1016/0165-0270(90)90053-i. [DOI] [PubMed] [Google Scholar]
  7. Cornell-Bell A. H., Finkbeiner S. M., Cooper M. S., Smith S. J. Glutamate induces calcium waves in cultured astrocytes: long-range glial signaling. Science. 1990 Jan 26;247(4941):470–473. doi: 10.1126/science.1967852. [DOI] [PubMed] [Google Scholar]
  8. Dani J. W., Chernjavsky A., Smith S. J. Neuronal activity triggers calcium waves in hippocampal astrocyte networks. Neuron. 1992 Mar;8(3):429–440. doi: 10.1016/0896-6273(92)90271-e. [DOI] [PubMed] [Google Scholar]
  9. Erecińska M., Troeger M. B. Amino acid neurotransmitters in the CNS. Characteristics of the acidic amino acid exchange. FEBS Lett. 1986 Apr 7;199(1):95–99. doi: 10.1016/0014-5793(86)81231-5. [DOI] [PubMed] [Google Scholar]
  10. Erecińska M., Wantorsky D., Wilson D. F. Aspartate transport in synaptosomes from rat brain. J Biol Chem. 1983 Aug 10;258(15):9069–9077. [PubMed] [Google Scholar]
  11. Fillenz M. Physiological release of excitatory amino acids. Behav Brain Res. 1995 Nov;71(1-2):51–67. doi: 10.1016/0166-4328(95)00045-3. [DOI] [PubMed] [Google Scholar]
  12. Finkbeiner S. Calcium waves in astrocytes-filling in the gaps. Neuron. 1992 Jun;8(6):1101–1108. doi: 10.1016/0896-6273(92)90131-v. [DOI] [PubMed] [Google Scholar]
  13. Herrera-Marschitz M., You Z. B., Goiny M., Meana J. J., Silveira R., Godukhin O. V., Chen Y., Espinoza S., Pettersson E., Loidl C. F. On the origin of extracellular glutamate levels monitored in the basal ganglia of the rat by in vivo microdialysis. J Neurochem. 1996 Apr;66(4):1726–1735. doi: 10.1046/j.1471-4159.1996.66041726.x. [DOI] [PubMed] [Google Scholar]
  14. Itoh T., Saito T., Fujimura M., Watanabe S., Saito K. Restraint stress-induced changes in endogenous zinc release from the rat hippocampus. Brain Res. 1993 Aug 6;618(2):318–322. doi: 10.1016/0006-8993(93)91283-x. [DOI] [PubMed] [Google Scholar]
  15. Keefe K. A., Sved A. F., Zigmond M. J., Abercrombie E. D. Stress-induced dopamine release in the neostriatum: evaluation of the role of action potentials in nigrostriatal dopamine neurons or local initiation by endogenous excitatory amino acids. J Neurochem. 1993 Nov;61(5):1943–1952. doi: 10.1111/j.1471-4159.1993.tb09837.x. [DOI] [PubMed] [Google Scholar]
  16. Kim W. T., Rioult M. G., Cornell-Bell A. H. Glutamate-induced calcium signaling in astrocytes. Glia. 1994 Jun;11(2):173–184. doi: 10.1002/glia.440110211. [DOI] [PubMed] [Google Scholar]
  17. Lowy M. T., Gault L., Yamamoto B. K. Adrenalectomy attenuates stress-induced elevations in extracellular glutamate concentrations in the hippocampus. J Neurochem. 1993 Nov;61(5):1957–1960. doi: 10.1111/j.1471-4159.1993.tb09839.x. [DOI] [PubMed] [Google Scholar]
  18. Lönnroth P., Jansson P. A., Smith U. A microdialysis method allowing characterization of intercellular water space in humans. Am J Physiol. 1987 Aug;253(2 Pt 1):E228–E231. doi: 10.1152/ajpendo.1987.253.2.E228. [DOI] [PubMed] [Google Scholar]
  19. Miele M., Berners M., Boutelle M. G., Kusakabe H., Fillenz M. The determination of the extracellular concentration of brain glutamate using quantitative microdialysis. Brain Res. 1996 Jan 22;707(1):131–133. doi: 10.1016/0006-8993(95)01371-7. [DOI] [PubMed] [Google Scholar]
  20. Moghaddam B. Stress preferentially increases extraneuronal levels of excitatory amino acids in the prefrontal cortex: comparison to hippocampus and basal ganglia. J Neurochem. 1993 May;60(5):1650–1657. doi: 10.1111/j.1471-4159.1993.tb13387.x. [DOI] [PubMed] [Google Scholar]
  21. Morari M., O'Connor W. T., Ungerstedt U., Fuxe K. N-methyl-D-aspartic acid differentially regulates extracellular dopamine, GABA, and glutamate levels in the dorsolateral neostriatum of the halothane-anesthetized rat: an in vivo microdialysis study. J Neurochem. 1993 May;60(5):1884–1893. doi: 10.1111/j.1471-4159.1993.tb13416.x. [DOI] [PubMed] [Google Scholar]
  22. Morton D. B., Griffiths P. H. Guidelines on the recognition of pain, distress and discomfort in experimental animals and an hypothesis for assessment. Vet Rec. 1985 Apr 20;116(16):431–436. doi: 10.1136/vr.116.16.431. [DOI] [PubMed] [Google Scholar]
  23. Parpura V., Basarsky T. A., Liu F., Jeftinija K., Jeftinija S., Haydon P. G. Glutamate-mediated astrocyte-neuron signalling. Nature. 1994 Jun 30;369(6483):744–747. doi: 10.1038/369744a0. [DOI] [PubMed] [Google Scholar]
  24. Parpura V., Liu F., Brethorst S., Jeftinija K., Jeftinija S., Haydon P. G. Alpha-latrotoxin stimulates glutamate release from cortical astrocytes in cell culture. FEBS Lett. 1995 Mar 6;360(3):266–270. doi: 10.1016/0014-5793(95)00121-o. [DOI] [PubMed] [Google Scholar]
  25. Parpura V., Liu F., Jeftinija K. V., Haydon P. G., Jeftinija S. D. Neuroligand-evoked calcium-dependent release of excitatory amino acids from Schwann cells. J Neurosci. 1995 Aug;15(8):5831–5839. doi: 10.1523/JNEUROSCI.15-08-05831.1995. [DOI] [PMC free article] [PubMed] [Google Scholar]
  26. Pin J. P., Duvoisin R. The metabotropic glutamate receptors: structure and functions. Neuropharmacology. 1995 Jan;34(1):1–26. doi: 10.1016/0028-3908(94)00129-g. [DOI] [PubMed] [Google Scholar]
  27. Rowley H. L., Martin K. F., Marsden C. A. Determination of in vivo amino acid neurotransmitters by high-performance liquid chromatography with o-phthalaldehyde-sulphite derivatisation. J Neurosci Methods. 1995 Mar;57(1):93–99. doi: 10.1016/0165-0270(94)00132-z. [DOI] [PubMed] [Google Scholar]
  28. Semba J., Kito S., Toru M. Characterisation of extracellular amino acids in striatum of freely moving rats by in vivo microdialysis. J Neural Transm Gen Sect. 1995;100(1):39–52. doi: 10.1007/BF01276864. [DOI] [PubMed] [Google Scholar]
  29. Sharp T., Bramwell S. R., Grahame-Smith D. G. Release of endogenous 5-hydroxytryptamine in rat ventral hippocampus evoked by electrical stimulation of the dorsal raphe nucleus as detected by microdialysis: sensitivity to tetrodotoxin, calcium and calcium antagonists. Neuroscience. 1990;39(3):629–637. doi: 10.1016/0306-4522(90)90247-2. [DOI] [PubMed] [Google Scholar]
  30. Vahabzadeh A., Fillenz M. Comparison of stress-induced changes in noradrenergic and serotonergic neurons in the rat hippocampus using microdialysis. Eur J Neurosci. 1994 Jul 1;6(7):1205–1212. doi: 10.1111/j.1460-9568.1994.tb00619.x. [DOI] [PubMed] [Google Scholar]
  31. Westerink B. H., Hofsteede H. M., Damsma G., de Vries J. B. The significance of extracellular calcium for the release of dopamine, acetylcholine and amino acids in conscious rats, evaluated by brain microdialysis. Naunyn Schmiedebergs Arch Pharmacol. 1988 Apr;337(4):373–378. doi: 10.1007/BF00169526. [DOI] [PubMed] [Google Scholar]
  32. Westerink B. H., Tuntler J., Damsma G., Rollema H., de Vries J. B. The use of tetrodotoxin for the characterization of drug-enhanced dopamine release in conscious rats studied by brain dialysis. Naunyn Schmiedebergs Arch Pharmacol. 1987 Nov;336(5):502–507. doi: 10.1007/BF00169306. [DOI] [PubMed] [Google Scholar]
  33. Westerink B. H., de Vries J. B. On the origin of extracellular GABA collected by brain microdialysis and assayed by a simplified on-line method. Naunyn Schmiedebergs Arch Pharmacol. 1989 Jun;339(6):603–607. doi: 10.1007/BF00168650. [DOI] [PubMed] [Google Scholar]
  34. Yamamoto B. K., Davy S. Dopaminergic modulation of glutamate release in striatum as measured by microdialysis. J Neurochem. 1992 May;58(5):1736–1742. doi: 10.1111/j.1471-4159.1992.tb10048.x. [DOI] [PubMed] [Google Scholar]
  35. de Boer P., Damsma G., Fibiger H. C., Timmerman W., de Vries J. B., Westerink B. H. Dopaminergic-cholinergic interactions in the striatum: the critical significance of calcium concentrations in brain microdialysis. Naunyn Schmiedebergs Arch Pharmacol. 1990 Nov;342(5):528–534. doi: 10.1007/BF00169041. [DOI] [PubMed] [Google Scholar]

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