Abstract
In rats vertically implanted with concentric dialysis probes in the medial prefrontal cortex and in the medial nucleus accumbens, morphine, ethanol and nicotine failed to modify extracellular dopamine in the medial prefrontal cortex at doses that were fully effective in raising extracellular dopamine in the nucleus accumbens. Conversely, the aversive/anxiogenic drugs picrotoxin, pentylenetetrazol and FG 7142, administered at subconvulsant doses, increased extracellular dopamine in the medial prefrontal cortex but failed to do so in the nucleus accumbens. Systemic administration of low doses of the 5HT3 antagonist ICS 205930, previously reported to prevent the increase of extracellular dopamine in the nucleus accumbens elicited by morphine, nicotine, ethanol and haloperidol (Carboni et al. 1989) as well as by stress (Imperato et al. 1990), also prevented the increase of extracellular dopamine elicited in the prefrontal cortex by anxiogenic drugs. Therefore, mesocortical and mesolimbic dopamine neurons show clear-cut differences in the reactivity to drugs of abuse and to aversive drugs but are both modulated by a facilitatory serotonergic input mediated by 5HT3 receptors.
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References
Abercrombie EA, Keefe KA, DiFrischia DA, Zigmond MJ (1989) Differential effect of stress on in vivo dopamine release in striatum, nucleus accumbens and medial frontal cortex. J Neurochem 52:1655–1658
Acquas E, Di Chiara G (1994) D1 receptor blockade stereospecifically impairs the acquisition of drug-conditioned place preference and place aversion. Behav Pharmacol 5:555–569
Acquas E, Carboni E, Leone P, Di Chiara G (1989) SCH 23390 blocks drug-conditioned place-preference and place-aversion: anhedonia (lack of reward) or apathy (lack of motivation) after dopamine-receptor blockade? Psychopharmacology 99:151–155
Beninger RJ (1983) The role of dopamine in locomotor activity and learning. Brain Res 6:173–196
Bradberry CW, Lory JD, Roth RH (1991) The anxiogenic β-carboline FG 7142 selectively increases dopamine releases in rat prefrontal cortex as measured by microdialysis. J Neurochem 56:748–752
Brazell MP, Mitchell SN, Joseph MH, Gray JA (1990) Acute administration of nicotine increases the in vivo extracellular levels of dopamine, 3,4-dihydroxyphenylacetic acid and ascorbic acid preferentially in the nucleus accumbens of the rat: comparison with caudate-putamen. Neuropharmacology 29:1177–1185
Carboni E, Acquas E, Frau R, Di Chiara G (1989) Differential inhibitory effects of a 5-HT3 antagonist on drug-induced stimulation of dopamine release. Eur J Pharmacol 164:515–519
Corda MG, Blaker WD, Mendelson WB, Guidotti A, Costa E (1983) β-Carbolines enhance shock-induced suppression of drinking in rats. Proc Natl Acad Sci USA 80:2072–2076
Di Chiara G (1995) The role of dopamine in drug abuse viewed from the perspective of its role in motivation. Drug Alcohol Depend 38:95–137
Di Chiara G, Imperato A (1988) Drugs abused by humans preferentially increase synaptic dopamine concentrations in the mesolimbic system of freely moving rats. Proc Natl Acad Sci USA 85:5274–5278
Di Chiara G, Tanda G, Frau R, Carboni E (1993) On the preferential release of dopamine in the nucleus accumbens by amphetamine: further evidence obtained by vertically implanted concentric dialysis probes. Psychopharmacology 112:398–402
Goeders NE, Dworkin SI, Smith JE (1986) Neuropharmacological assessment of cocaine self-administration into the medial prefrontal cortex. Pharmacol Biochem Behav 24:1429–1440
Imperato A, Angelucci L (1989) 5-HT3 receptors control dopamine release in the nucleus accumbens of freely moving rats. Neurosci Lett 101:214–217
Imperato A, Puglisi-Allegra S, Casolini P, Zocchi A, Angelucci L (1989) Stress-induced enhancement of dopamine and acetylcholine release in limbic structure: role of corticosterone. Eur J Pharmacol 165:337–338
Imperato A, Puglisi-Allegra S, Zocchi A, Scrocco MG, Casolini P, Angelucci L (1990) Stress activation of limbic and cortical dopamine release is prevented by ICS 205–930 but not by diazepam. Eur J Pharmacol 175:211–214
Johnson SW, North RA (1992) Opioids excite dopamine neurons by hyperpolarization of local interneurons. J Neurosci 12:483–488
Kuczenski R, Segal DS (1992) Differential effects of amphetamine and dopamine uptake blockers (cocaine, nomifensine) on caudate and accumbens dialysate dopamine and 3-methoxytyramine. J Pharmacol Exp Ther 262:1085–1094
Le Moal M, Simon H (1991) Mesocorticolimbic dopaminergic network: functional and regulatory roles. Physiol Rev 71:155–234
Martin-Iverson MT, Szostak C, Fibiger HC (1986) 6-Hydroxydopamine lesions of the medial prefrontal cortex fail to influence intravenous self-administration of cocaine. Psychopharmacology 88:310–314
McCullough LD, Salamone JD (1992) Anxiogenic drugs β-CCE and FG 7142 increase extracellular dopamine levels in nucleus accumbens. Psychopharmacology 109:379–382
Mereu G, Yoon KWP, Boi V, Gessa GL, Naes L, Westfall TC (1987) Preferential stimulation of ventral tegmental area dopaminergic neurons by nicotine. Eur J Pharmacol 141:395–399
Moghaddam B, Bunney BS (1989) Differential effect of cocaine on extracellular dopamine levels in the rat medial prefrontal cortex and nucleus accumbens: a comparison with amphetamine. Synapse 4:156–161
Nisell M, Nomikos GG, Svensson TH (1994) Systemic nicotine-induced dopamine release in the rat nucleus accumbens is regulated by nicotinic receptors in the ventral tegmental area. Synapse 16:36–44
Paxinos G, Watson C (1987) The rat brain in stereotaxic coordinates, 2nd edn. Academic Press, New York
Richardson BP, Engel G, Donatsch P, Stadler PA (1985) Identification of serotonin M-receptor subtypes and their specific blockade by a new class of drugs. Nature 316:126–131
Salamone JD (1988) Dopaminergic involvement in activational aspects of motivation: effects of haloperidol on schedule-induced activity, feeding and foraging in rats. Psychobiology 16:196–206
Spyraki C, Kazandjian A, Varanos D (1985) Diazepam-induced place preference conditioning: appetitive and antiaversive properties. Psychopharmacology 87:225–232
Thiébot MH, Soubrié P, Sanger D (1988) Anxiogenic properties of beta-CCE and FG 7142: a review of promises and pitfalls. Psychopharmacology 94:452–463
Young AMJ, Joseph MH, Gray JA (1993) Latent inhibition of conditioned dopamine release in rat nucleus accumbens. Neuroscience 54:5–9
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An erratum to this article is available at http://dx.doi.org/10.1007/BF02806005.
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Bassareo, V., Tanda, G., Petromilli, P. et al. Non-psychostimulant drugs of abuse and anxiogenic drugs activate with differential selectivity dopamine transmission in the nucleus accumbens and in the medial prefrontal cortex of the rat. Psychopharmacology 124, 293–299 (1996). https://doi.org/10.1007/BF02247433
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DOI: https://doi.org/10.1007/BF02247433