Summary
Unilateral degeneration of nigrostriatal dopaminergic terminals by the intranigral infusion of 6-OHDA produced a decrease in spontaneous multiple unit activity (MUA) in both the ipsilateral and contralateral striata of freely moving rats. Nigral lesions also attenuated the dexamphetamine-induced increase in MUA in the ipsilateral but not in the contralateral striatum. The magnitude of the attenuation in the ipsilateral striatum was directly proportional to the percent depletion of dopamine. Similarly degeneration of dopaminergic terminals produced by a unilateral application of 6-OHDA into the striatum lowered spontaneous MUA and completely antagonized the dexamphetamine-induced increase in MUA in the dopamine-depleted striatum. Although the spontaneous MUA in striata contralateral to a local 6-OHDA treatment was significantly reduced, the response to dexamphetamine was normal. Both striatal and nigral application of 6-OHDA produced dopamine depletion in the ipsilateral striatum and an increase in striatal dopamine levels on the contralateral side. Striatal application of 6-OHDA did not alter dopamine levels in either the olfactory tubercles, piriform cortex or cingulate cortex. It is concluded that the increase in MUA observed in the striatum following dexamphetamine treatment is critically dependent upon the release of dopamine in the striatum. These results support the concept that dopamine may have an excitatory action on some striatal neurons.
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Altar A, Neve KA, Loughlin SE, Marshall JF, Fallon JH (1983) The crossed mesostriatal projection: neurochemistry and development response to lesion. Brain Res 279: 1–8
Bannon MJ, Roth RH (1983) Pharmacology of mesocortical dopamine neurons. Pharmacol Rev 35: 53–68
Bannon MJ, Wolf ME, Roth RH (1983) Pharmacology of dopamine neurons innervating the prefrontal, cingulate and piriform cortices. Eur J Pharmacol 92: 119–125
Bartholini G (1980) Interaction of striatal dopaminergic, cholinergic and GABA-ergic neurons: relation to extrapyramidal function. Trends Pharmacol Sci 1: 138–140
Buchwald NA, Price DD, Vernon L, Hull C (1973) Caudate intracellular responses to thalamic and cortical inputs. Exp Neurol 38: 311–323
Caviness JN, Wightman RM (1982) Use of rapid superperfusion to differentiate the release of dopamine from striatal tissue induced by sympathomimetic amines from release induced by potassium. J Pharmacol Exp Ther 223: 90–96
Chiueh CC, Moore KE (1973) Release of endogenously synthesized catechols from the caudate nucleus by stimulation of the nigro-striatal pathway and by the administration of d-amphetamine. Brain Res 50: 221–225
Clemens JH, Phebus LA (1983) Changes in brain chemistry produced by dopaminergic agents: in vivo electrochemical monitoring reveals opposite changes in anesthetized vs unanesthetized rats. Brain Res 267: 183–186
Frigyesi TL, Purpura DP (1967) Electrophysiological analysis of reciprocal caudate-nigral relations. Brain Res 6: 440–456
Garcia-Rill E, Hull CD, Levine MS, Buchwald NA (1979) The spontaneous firing patterns of forebrain neurons. IV. Effects of bilateral and unilateral frontal cortical ablations on firing of caudate, globus pallidus and thalamic neurons. Brain Res 165: 23–36
Gauchy C, Bioulac B, Cheramy A, Besson MJ, Glowinski J, Vincent JD (1974) Estimation of chronic dopamine release from the caudate nucleus of the Macaca mulatta. Brain Res 77: 257–268
Glowinski J, Cheramy A, Giorguieff MF (1979) In vitro release of dopamine. In: Horn AS, Korf J, Westerink BHC (eds) The neurobiology of dopamine. Academic Press, New York, pp 199–217
Groves PM (1977) Possible mechanisms involved in the stereotyped behaviour elicited by amphetamine. Biol Psych 12: 381–387
Groves PM (1983) A theory of the functional organization of the neostriatum and the neostriatal control of voluntary movement. Brain Res Rev 5: 109–132
Groves PM, Rebec GV, Harvey JA (1975) Alteration of the effects of d-amphetamine on neuronal activity in the striatum following lesions of the nigrostriatal bundle. Neuropharmacology 14: 369–376
Groves PM, Rebec GV, Segal DS (1974) The action of d-amphetamine on spontaneous activity in the caudate nucleus and reticular formation of the rat. Behav Biol 11: 33–47
Hansen EL, McKenzie GM (1979) Dexamphetamine increases striatal neuronal firing in freely moving rats. Neuropharmacol 18: 547–552
Hassler R (1978) Striatal control of locomotion, intentional actions and of integrating and perceptive activity. J Neurol Sci 36: 187–224
Hefti F, Enz A, Malamed E (1985) Partial lesions of the nigrostriatal pathway in the rat. Acceleration of transmitter synthesis and release of surviving dopaminergic neurons by drugs. Neuropharmacology 24: 19–23
Hefti F, Melamed E, Wurtman R (1980) Partial lesions of the dopaminergic nigrostriatal system in rat brain: biochemical characterization. Brain Res 195: 123–137
Hull CD, Bernardi GA, Buchwald NA (1970) Intracellular, responses of caudate neurons to brain stem stimulation. Brain Res 22: 163–179
Hull CD, Levine MS, Buchwald NA, Heller A, Browning RA (1974) The spontaneous firing pattern of forebrain neurons. I. The effects of dopamine and non-dopamine depleting lesions on caudate unit firing patterns. Brain Res 73: 241–252
Kitai ST, Kocsis JD, Preston RJ, Sugimori M (1976) Monosynaptic inputs to caudate neurons identified by intracellular injection of horseradish peroxidase. Brain Res 109: 601–606
Levine MS, Hull CD, Buchwald NA, Garcia-Rill E, Heller A, Erinoff L (1977) The spontaneous firing patterns of forebrain neurons. III. Prevention of induced asymmetries in caudate neuronal firing rates by unilateral thalamic lesions. Brain Res 131: 215–225
Levine MS, Hull CD, Buchwald NA, Villablanca J (1974) The spontaneous firing patterns of forebrain neurons. II. Effects of unilateral caudate nuclear ablation. Brain Res 78: 411–424
Loughlin SE, Fallon JH (1984) Substantia nigra and ventral tegmental area projections to cortex: topography and collateralization. Neuroscience 11: 425–435
Marshall JF, Drew MC, Neve KA (1983) Recovery of function after mesotelencephalic dopaminergic injury in senescence. Brain Res 259: 249–260
McCown TJ, Mueller RA, Breese GR (1983) Effects of anesthetics and electrical stimulation on nigrostriatal dopaminergic neurons. J Pharmacol Exp Ther 224: 489–493
McKenzie GM, Szerb JC (1968) The effect of dihydroxyphenylalanine, pheniprazine and dextroamphetamine on the in vivo release of dopamine from the caudate nucleus. J Pharmacol Exp Ther 162: 302–308
McKenzie GM (1972) Role of the tuberculum olfactorium in stereotyped behavior induced by apomorphine in the rat. Psychopharmacologia 23: 212–219
McKenzie GM, Hansen EL (1980) Gaba agonists dissociate striatal unit activity from drug-induced stereotyped behaviour. Neuropharmacol 19: 957–962
McLennan H, York DH (1967) The action of dopamine on neurons of the caudate nucleus. J Physiol 189: 393–402
Mereu G, Casu M, Gessa GL (1983) (−)-Sulpiride activates the firing rate and tyrosine hydroxylase activity of dopaminergic neurons in unanesthetized rats. Brain Res 264: 105–110
Neve KA, Kozlouski MR, Marshall JF (1982) Plasticity of neostriatal dopamine receptors after nigrostriatal injury. Relationship to recovery of sensorimotor functions and behavioral supersensitivity. Brain Res 244: 33–34
Norcross K, Spehlmann RA (1978 a) Quantitative analysis of the excitatory and depressant effects of dopamine on the firing of caudatal neurons: electrophysiological support for the existence of two distinct dopamine-sensitive receptors. Brain Res 156: 168–174
Norcross K, Spehlmann R (1978 b) Decreased sensitivity of caudatal neurons to microiontophoretic dopamine in dopamine-depleted caudate nucleus. Brain Res 156: 175–180
Moore RY, Bloom FE (1978) Central catecholamine neuron systems: anatomy and physiology of the dopamine systems. Ann Rev Neurosci 1: 129–169
Pellegrino LJ, Cushman AJ (1967) A stereotaxic atlas of the rat brain. In: Elliot RM, Lindzey G, MacGorguodale K (eds) Century psychology series. Appleton-Century-Crafts, New York.
Philipps SR, Robson AM, Boulton AA (1982) Unstimulated and amphetamine-stimulated release of endogenous noradrenaline and dopamine from rat brain in vivo. J Neurochem 38: 1106–1109
Pycock CJ, Kerwin RW, Carter CJ (1980) Effect of lesion of cortical dopamine terminals on subcortical dopamine receptors in rats. Nature 286: 74–77
Rebec GV, Groves PM (1976) Enhancement of effects of dopaminergic agonists on neuronal activity in the caudate-putamen of the rat following long-term d-amphetamine administration. Pharmacol Biochem Behav 5: 349–357
Riddell D, Szerb JC (1971) The release in vivo of dopamine synthesized from labelled precursors in the caudate nucleus of the cat. J Neurochem 18: 989–1006
Robinson TE, Becker JB, Presty SK (1982) Behavioural sensitization is accompanied by an enhancement in amphetamine-stimulated dopamine release from striatal tissue in vitro. Eur J Pharmacol 85: 253–254
Takano Y, Sakurai Y, Kahjimoto Y, Honda K, Kamiya H (1983) Presynaptic modulation of the release of dopamine from striatal synaptosomes: differences in the effects of high K stimulation, methamphetamine and nicotinic drugs. Brain Res 279: 330–334
Trulson ME, Jacobs BL (1979) Effects of D-amphetamine on striatal unit activity and behavior in freely moving cats. Neuropharmacology 18: 735–738
Warenycia MW, McKenzie GM (1984 a) The role of afferents from the parafascicular-centromedian complex in the excitatory striatal neuronal response to dexamphetamine in freely moving animals. Prog Neuropsychopharmacol Biol Psychiatry 8: 757–760
Warenycia MW, McKenzie GM (1984 b) Immobilization of rats modifies the response of striatal neurons to dexamphetamine. Pharmacol Biochem Behav 21: 53–59
Warenycia MW, McKenzie GM, Murphy M, Szerb JC (1984) Bilateral ablation of the corticostriatal projection: behavioural, biochemical and electrophysiological correlates. Prog Neuropsychopharmacol Biol Psychiatry 8: 761–764
Wilson CJ, Chang HT, Kitai ST (1982) Origins of postsynaptic potentials evoked in identified rat neostriatal neurons by stimulation in substantia nigra. Exp Brain Res 45: 157–167
Ungerstedt U (1971) Striatal dopamine release after amphetamine or nerve degeneration revealed by rotational behaviour. Acta Physiol Scand 82 [Suppl 367]: 49–68
Zetterstrom T, Sharp T, Marsden CA, Ungerstedt U (1983) In vivo measurement of dopamine and its metabolites by intracerebral dialysis: changes after d-amphetamine. Neurochem 41: 1769–1773
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Warenycia, M.W., McKenzie, G.M. Activation of striatal neurons by dexamphetamine is antagonized by degeneration of striatal dopaminergic terminals. J. Neural Transmission 70, 217–232 (1987). https://doi.org/10.1007/BF01253599
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DOI: https://doi.org/10.1007/BF01253599