Summary
The neuronal origin of extracellular levels of dopamine (DA), acetylcholine (ACh), glutamate (Glu), aspartate (Asp) and gamma-aminobutyric acid (GABA) simultaneously collected from the neostriatum of halothane anaesthetized rats with in vivo microdialysis was studied. The following criteria were applied (1) sensitivity to K+-depolarization; (2) sensitivity to inhibition of synaptic inactivation mechanisms; (3) sensitivity to extracellular Ca2+; (4) neuroanatomical regionality; sensitivity to selective lesions and (5) sensitivity to chemical stimulation of the characterized pathways.
It was found that: (1) Extracellular DA levels found in perfusates collected from the neostriatum fulfills all the above criteria and therefore the changes in extracellular DA levels measured with microdialysis reflect actual release from functionally active nerve terminals, and so reflect ongoing synaptic transmission. (2) Changes in neostriatal ACh levels reflect neuronal activity, provided that a ACh-esterase inhibitor is present in the perfusion medium. (3) Extracellular Glu, Asp and GABA could be measured in different perfusion media in the rat neostriatum and probably reflect metabolic as well as synaptic release. However, (4) the majority of the extracellular GABA levels found in perfusates collected from the neostriatum may reflect neuronal release, since GABA levels were increased, in a Ca2+-dependent manner, by K+-depolarization, and could be selectively decreased by an intrinsic neostriatal lesion. (5) It was not possible to clearly distinguish between the neuronal and the metabolic pools of Glu and Asp, since neostriatal Glu and Asp levels were only slightly increased by K+-depolarization, and no changes were seen after decortication. A blocker of Glu re-uptake, DHKA, had to be included in the perfusion medium in order to monitor the effect of K+-depolarization on Glu and Asp levels. Under this condition, it was found (6) that neostriatal Glu and Asp levels were significantly increased by K+-depolarization, although only increases in the Glu levels were sensitive to Ca2+ in the perfusion medium, suggesting that Glu but not Asp is released from vesicular pools. (7) Evidence is provided that selective stimulations of nigral DA cell bodies may lead to changes in release patterns from DA terminals in the ipsilateral neostriatum, which are in turn followed by discrete changes in extracellular levels of GABA and Glu in the same region. Finally, some methodological considerations are presented to clarify the contribution of neuronal release to extracellular levels of amino acid neurotransmitters in the rat neostriatum.
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References
Björklund A, Lindvall O (1984) Dopamine containing systems in the CNS. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy, vol. 2. Classical neurotransmitters in the CNS, part I. Elsevier, New York, pp 117–155
Bolam JP, Powell JF, Wu JY, Smith AD (1985) J Comp Neurol 237: 1–20
Bouyer JJ, Park DH, Joh TH, Pickel CVM (1984) Brain Res 302: 267–277
Brownstein MJ, Mroz EA, Tappaz ML, Leeman SE (1977) Brain Res 135: 315–323
Burger PM, Mehl E, Cameron PL, Maycox PR, Baumert M, Lottspeich F, De Camilli P, Jahn R (1989) Neuron 3: 715–720
Burgunder JM, Young WS (1990) J Comp Neurol 300: 26–46
Carlsson M, Carlsson A (1990) TINS 13: 272–276
Carter CJ, L'Heureux R, Scatton B (1988) J Neurochem 51: 462–468
Chéramy AR, Romo R, Godeheu G, Glowinski J (1986) Neuroscience 19: 1067–1079
Christensson-Nylander I, Herrera-Marschitz M, Staines W, Hökfelt T, Terenius L, Ungerstedt U, Cuello C, Oertel W, Goldstein M (1986) Exp Brain Res 64: 169–192
Currie DN, Kelly JS (1981) J Exp Biol 95: 181–193
Descarries L, Lemay B, Doucet G, Berger B (1987) Neuroscience 21: 807–824
Di Chiara G (1990) TIPS 11: 116–121
Drew KL, O'Connor WT, Kehr J, Ungerstedt J (1990) Eur J Pharmacol 187: 385–397
Giorguieff MF, Kemel ML, Glowinski J (1977) Neurosci Lett 6: 73–77
Girault JA, Barbeito L, Spampinato U, Gozlan H, Glowinski J, Besson MJ (1986) J Neurochem 47: 98–196
Godukhin OV, Zharikova AD, Budantsev AY (1984) Neuroscience 12: 377–383
Graybiel AM (1990) TINS 13: 244–254
Herrera-Marschitz M, Ungerstedt U (1984a) Brain Res 323: 269–278
Herrera-Marschitz M, Ungerstedt U (1984b) Eur J Pharmacol 102: 213–227
Herrera-Marschitz M (1986) Neuropharmacology and functional anatomy of the basal ganglia. Thesis, Karolinska Institute, Stockholm, p 79
Herrera-Marschitz M, Goiny M, Utsumi H, Ungerstedt U (1989) Neurosci Lett 97: 266–270
Herrera-Marschitz M, Goiny M, Utsumi H, Ferre S, Guix T, Ungerstedt U (1990a) Regulation of cortical and striatal dopamine and acetylcholine release by glutamate mechanisms assayed in vivo with microdialysis: in situ stimulation with kainate-, quisqualate- and NMDA-receptor agonist. In: Lubec G, Rosenthal GA (eds) Amino acids. Chemistry, biology and medicine. ESCOM, Wien, pp 599–604
Herrera-Marschitz M, Goiny M, Utsumi H, Ferre S, Håkansson L, Nordberg A, Ungerstedt U (1990b) Neurosci Lett 110: 172–179
Herrera-Marschitz M, Utsumi H, Ungerstedt U (1990c) J Neurol Neurosurg Psychiatry 53: 39–43
Herrera-Marschitz M (1991) Modulation of striatal dopamine and acetylcholine release by different glutamate receptors: studies with in vivo microdialysis. In: Bernardi G, Carpenter MB, Di Chiara G, Morelli M, Stanzione P (eds) The basal ganglia III. Advances in behavioral biology, vol 39. Plenum Press, New York, pp 357–362
Herrling PL (1985) Neuroscience 14: 417–426
Hornykiewicz O (1973) Br Med Bull 29: 172–178
Hurd J (1989) In vivo brain pharmacology of cocaine, amphetamine and related drugs: a microdialysis study. Thesis, Karolinska Institute, Stockholm, p 68
Hökfelt T, Mårtensson R, Björklund A, Kleinau S, Goldstein M (1984) Distribution maps of tyrosine-hydroxylase-immunoreactive neurons in the rat brain. In: Björklund A, Hökfelt T (eds) Handbook of chemical neuroanatomy, vol 2: Classical neurotransmitters in the CNS, part I. Elsevier, New York, pp 277–379
Imperato A, Di Chiara G (1984) J Neurosci 4: 966–977
Johnston GAR. Sue M. Kemmedy E, Twitchin B (1979) J Neurochem 32: 121–127
Kehr J, Ungerstedt U (1988) J Neurochem 51: 1308–1310
Kim JS, Bak IJ, Hassler R, Okada Y (1971) Exp Brain Res 14: 95–104
Klawans HL, Goetz C, Westeimer R (1972) Dis Nerv Syst 33: 711–719
Kubota Y, Inagaki S, Kito S, Wu JY (1987a) Brain Res 406: 147–156
Kubota Y, Inagaki S, Shimada S, Kito S, Eckenstein TF, Tohyama M (1987b) Brain Res 413: 179–184
König JFR, Klippel RA (1963) The rat brain. A stereotaxic atlas of the forebrain and lower parts of the brain stem. Krieger, New York, p 162
Lindefors N (1987) Brain tachykinins and their interaction with dopaminergic transmission. Thesis, Karolinska Institute, Stockholm, p 34
Maysinger D, Herrera-Marschitz M, Carlsson A, Garofalo L, Cuello AC, Ungerstedt (1988) Brain Res 461: 355–360
McGeer PL, McGeer EG (1975) Brain Res 91: 331–335
McGeer EG, Staines WA, McGeer PL (1984) Can J Neurosci [Suppl]: 89–99
McGeorge AJ, Faull RLM (1989) Neuroscience 29: 503–537
Meana JJ, Herrera-Marschitz M, Brodin E, Hökfelt T, Ungerstedt U (1991) Amino Acids 1: 365–373
Moghaddam B, Bunney BS (1989) J Neurochem 53: 652–654
O'Connor WT, Lindefors N, Brene S, Herrera-Marschitz M, Persson H, Ungerstedt U (1991a) Neurosci Lett 128: 66–70
O'Connor WT, Herrera-Marschitz M, Lindefors N, Osborne PG, Drew KL, Reid M, Ungerstedt U (1991b) Dopamine-GABA interactions in the neostriatum. In: Rollema H, Westerink B, Drijfhout WJ (eds) Monitoring molecules in neuroscience. RUG, Groningen, pp 993–995
Osborne PG, O'Connor WT, Drew KL, Ungerstedt U (1990) J Neurosci Methods 34: 99–105
Osborne PG, O'Connor WT, Ungerstedt U (1991a) J Neurochem 56: 452–456
Osborne PG, O'Connor WT, Kehr J, Ungerstedt U (1991b) J Neurosci Methods 37: 93–102
Paulsen RE, Fonnum F (1989) J Neurochem 52: 1823–1829
Reid M, Herrera-Marschitz M, Hökfelt T, Terenius L, Ungerstedt U (1988) Eur J Pharmacol 147: 411–420
Reid MS (1990) Neuropharmacological circuitry of the basal ganglia studied by microdialysis. Thesis, Karolinska Institute, Stockholm, p 69
Reid M, Herrera-Marschitz M, Hökfelt T, Ohlin M, Valentino KI, Ungerstedt U (1990a) Neuroscience 36: 643–658
Reid M, Hökfelt T, Herrera-Marschitz M, Håkansson R, Feng DM, Folkers K, Goldstein M, Ungerstedt U (1990b) Brain Res 532: 175–181
Reid MS, Herrera-Marschitz M, Hökfelt T, Lindefors N, Persson H, Ungerstedt U (1990c) Exp Brain Res 82: 293–303
Reid MS, O'Connor WT, Herrera-Marschitz M, Ungerstedt U (1990d) Brain Res 519: 225–260
Reid MS, Herrera-Marschitz M, Kehr J, Ungerstedt U (1990e) Acta Physiol Scand 1440: 527–537
Roberts PJ, McBean GJ, Sharif NA, Thomas ER (1982) Brain Res 235: 83–91
Romo R, Chéramy A, Godeheu G, Glowinski J (1986a) Neuroscience 19: 1067–1079
Romo R, Chéramy A, Godeheu G, Glowinski J (1986b) Neuroscience 19: 1099–2005
Satoh K, Staines WA, Atmadja S, Fiberger HC (1983) Neuroscience 10: 1121–1136
Schwarcz R, Coyle JT (1977) Brain Res 127: 235–249
Schwarcz R, Creese I, Coyle JT, Snyder SH (1978) Nature 271: 766–768
Schwarcz R, Hökfelt T, Fuxe K, Jonsson G, Goldstein M, Terenius L (1979) Exp Brain Res 37: 199–216
Smith AD, Bolam JP (1990) TINS 13: 259–265
Somogyi P, Bolam JP, Smith AD (1981) J Comp Neurol 195: 567–584
Storm-Mathisen J, Leknes AK, Bore AT, Vaaland JL, Edminson P, Haug FMS, Ottersen OP (1983) Nature 301: 515–520
Ståhle L (1987) Pharmacological studies on behavioural changes induced by dopamine agonists in the rat: a multivariate approach. Thesis, Karolinska Institute, Stockholm, p 73
Szatkowski M, Barbour B, Attwell D (1990) Nature 348: 443–446
Tossman U, Ungerstedt U (1986) Eur J Pharmacol 123: 295–298
Tossman U (1986) Neurochemical studies of amino acids in the rat central nervous system. Thesis, Karolinska Institute, Stockholm, p 29
Tsumoto T (1990) Neurosci Res 9: 79–102
Ungerstedt U, Herrera-Marschitz M, Jungnelius U, Ståhle L, Tossman U, Zetterström T (1982) Dopamine synaptic mechanisms reflected in studies combining behavioral recordins and brain dialysis. In: Kohksaka M, Shomori T, Tsukada Y, Woodruff GN (eds) Advances in dopamine research. Advances in biosciences, vol 37. Pergamon Press, Oxford, pp 219–231
Ungerstedt U (1984) Measurement of neurotransmitter release by intracranial microdialysis. In: Marsden CA (ed) Measurement of neurotransmitter release in vivo. J Wiley, Chicester, pp 81–105
Westerink BHC, Damsma G, Rollema H, De Vries JB, Horn AS (1987) Life Sci 41: 1763–1776
Westerink BHC, Hofsteede HM, Damsma G, De Vries JB (1988) Naunyn-Schmiedeberg's Arch Pharmacol 337: 373–378
Young AM, Bradford HF (1986) J Neurochem 47: 1399–1404
Zetterström T (1986) Pharmacological analysis of central dopaminergic neurotransmission using a novel in vivo brain perfusion method. Thesis, Karolinska Institute, Stockholm, p 45
Zetterström T, Herrera-Marschitz M, Ungerstedt U (1986) Brain Res 376: 1–7
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Herrera-Marschitz, M., Meana, J.J., O'Connor, W.T. et al. Neuronal dependence of extracellular dopamine, acetylcholine, glutamate, aspartate and gamma-aminobutyric acid (GABA) measured simultaneously from rat neostriatum using in vivo microdialysis: reciprocal interactions. Amino Acids 2, 157–179 (1992). https://doi.org/10.1007/BF00806086
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DOI: https://doi.org/10.1007/BF00806086