Opposite Change of In Vivo Dopamine Release in the Rat Nucleus Accumbens and Striatum That Follows Electrical Stimulation of Dorsal Raphe Nucleus: Role of 5-HT3 Receptors

In the present study we investigate, using in vivomicrodialysis, the involvement of central 5-HT3 receptors in the effect of dorsal raphe nucleus (DRN) electrical stimulation on dopamine (DA), 3,4-dihydroxyphenylacetic acid (DOPAC), and 5-hydroxyindole-3-acetic acid (5-HIAA) extracellular levels monitored in the nucleus accumbens and the striatum of halothane-anesthetized rats. DRN stimulation (300 μA, 1 msec at 3, 5, 10, and 20 Hz for 15 min) induced a frequency-dependent increase of accumbal DA release and a concomitant reduction of DA release in the ipsilateral striatum at 20 Hz. In both structures DOPAC and 5-HIAA dialysate contents were enhanced in a frequency-dependent manner. Central serotonin (5-HT) depletion, induced by intra-raphe injections of 5,7-dihydroxytryptamine neurotoxin, abolished the effect of 20 Hz DRN stimulation on DA, DOPAC, and 5-HIAA extracellular levels in both regions. The 5-HT synthesis inhibitor para-chlorophenylalanine (3 × 400 mg/kg, i.p., for 3 d), although preventing the effect on DA release, failed to modify significantly the effect of 20 Hz DRN stimulation on DOPAC and 5-HIAA outflow in both structures. Ondansetron (0.1 and 1 mg/kg) and (S)-zacopride (0.1 mg/kg), two 5-HT3 antagonists, significantly impaired the increase of accumbal DA release induced by 20 Hz DRN stimulation but did not affect either the decrease of striatal DA release or the increase in DOPAC outflow in both structures. These results indicate that an enhancement of central 5-HT transmission induced by DRN stimulation differentially affects striatal and accumbal DA release and that endogenous 5-HT, via its action on 5-HT3 receptors, exerts a facilitatory control restricted to the mesoaccumbal DA pathway.

[1]  O. H. Lowry,et al.  Protein measurement with the Folin phenol reagent. , 1951, The Journal of biological chemistry.

[2]  A. Weissman,et al.  p-Chlorophenylalanine: a specific depletor of brain serotonin. , 1966, The Journal of pharmacology and experimental therapeutics.

[3]  A. Björklund,et al.  Evaluation of the effects of 5,7-dihydroxytryptamine on serotonin and catecholamine neurons in the rat CNS. , 1973, Acta physiologica Scandinavica. Supplementum.

[4]  E. Azmitia,et al.  An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat , 1978, The Journal of comparative neurology.

[5]  Rotational behaviour elicited by 5‐HT in the rat: evidence for an inhibitory role of 5‐HT in the substantia nigra and corpus striatum , 1980, The Journal of pharmacy and pharmacology.

[6]  Per Brodal,et al.  A stereotaxic atlas of the rat brain L. J. Pellegrino, A. S. Pellegrino & A. J. Cushman. Plenum Press, New York (1979). 122 Figures. £22.50 , 1980, Neuroscience.

[7]  N. Dafny,et al.  Electrophysiological evidence of concurrent dorsal raphe input to caudate, septum, habenula, thalamus hippocampus, cerebellum and olfactory bulb. , 1983, The International journal of neuroscience.

[8]  G. Paxinos,et al.  The Rat Brain in Stereotaxic Coordinates , 1983 .

[9]  P. Soubrié,et al.  Functional aspects of serotonin transmission in the basal ganglia: A review and in vivo approach using the push-pull cannula technique , 1984, Neuroscience.

[10]  W Kostowski,et al.  Interaction between serotonergic and dopaminergic systems detected in striatum by differential pulse voltammetry. , 1985, European journal of pharmacology.

[11]  K. Moore,et al.  A Comparison of Biochemical Indices of 5‐Hydroxytryptaminergic Neuronal Activity Following Electrical Stimulation of the Dorsal Raphe Nucleus , 1986, Journal of neurochemistry.

[12]  S. Algeri,et al.  Modulation of striatal dopamine metabolism by the activity of dorsal raphe serotonergic afferences , 1987, Brain Research.

[13]  Gavin Kilpatrick,et al.  Identification and distribution of 5-HT3 receptors in rat brain using radioligand binding , 1987, Nature.

[14]  T. R. Stratford,et al.  Evidence that serotonergic projections to the substantia nigra in the rat arise in the dorsal, but not the median, raphe nucleus , 1987, Neuroscience Letters.

[15]  B. Costall,et al.  Effects of the 5‐HT3 receptor antagonist, GR38032F, on raised dopaminergic activity in the mesolimbic system of the rat and marmoset brain , 1987, British journal of pharmacology.

[16]  Julia M. Hill,et al.  Effect of the 5-HT3 receptor antagonist, GR38032F, on responses to injection of a neurokinin agonist into the ventral tegmental area of the rat brain. , 1987, European journal of pharmacology.

[17]  D. Duverger,et al.  Influence of ascending serotonergic pathways on glucose use in the conscious rat brain. II. Effects of electrical stimulation of the rostral raphé nuclei , 1988, Brain Research.

[18]  G. Di Chiara,et al.  Differential inhibitory effects of a 5-HT3 antagonist on drug-induced stimulation of dopamine release. , 1989, European journal of pharmacology.

[19]  J. Green,et al.  Release of endogenous dopamine by stimulation of 5-hydroxytryptamine3 receptors in rat striatum. , 1989, The Journal of pharmacology and experimental therapeutics.

[20]  W. Mcbride,et al.  Serotonin microinfusion into the ventral tegmental area increases accumbens dopamine release , 1989, Brain Research Bulletin.

[21]  A. Imperato,et al.  5-HT3 receptors control dopamine release in the nucleus accumbens of freely moving rats , 1989, Neuroscience Letters.

[22]  D G Grahame-Smith,et al.  In Vivo Measurement of Extracellular 5‐Hydroxytryptamine in Hippocampus of the Anaesthetized Rat Using Microdialysis: Changes in Relation to 5‐Hydroxytryptaminergic Neuronal Activity , 1989, Journal of neurochemistry.

[23]  D. Perry.  Autoradiography of [3H]quipazine in rodent brain. , 1990, European journal of pharmacology.

[24]  W. Soudijn,et al.  The concept of selectivity in 5-HT receptor research. , 1990, European journal of pharmacology.

[25]  M. Reith,et al.  5-HT3 receptor antagonists attenuate cocaine-induced locomotion in mice. , 1990, European journal of pharmacology.

[26]  R. Kasser,et al.  The effect of intraventricular administration of the 5-HT3 receptor agonist 2-methylserotonin on the release of dopamine in the nucleus accumbens: an in vivo chronocoulometric study , 1990, Brain Research.

[27]  B. Costall,et al.  Characterisation and autoradiographic localisation of 5-HT3 receptor recognition sites identified with [3H]-(S)-zacopride in the forebrain of the rat , 1990, Neuropharmacology.

[28]  P. Hicks.  The effect of serotonergic agents on haloperidol-induced catalepsy , 1989, Schizophrenia Research.

[29]  L. Chiodo,et al.  Serotonergic afferent regulation of the basic physiology and pharmacological responsiveness of nigrostriatal dopamine neurons. , 1990, The Journal of pharmacology and experimental therapeutics.

[30]  R. Peltier,et al.  GR38032F, a serotonin 5-HT3 antagonist, fails to alter cocaine self-administration in rats , 1991, Pharmacology Biochemistry and Behavior.

[31]  B. Bunney,et al.  Mechanisms of action of atypical antipsychotic drugs Implications for novel therapeutic strategies for schizophrenia , 1991, Schizophrenia Research.

[32]  M. Galloway,et al.  Facilitation of dopamine release in vivo by serotonin agonists: studies with microdialysis. , 1991, European journal of pharmacology.

[33]  H. Meltzer,et al.  Effects of antipsychotic drugs on serotonin receptors. , 1991, Pharmacological reviews.

[34]  E. Gardner,et al.  Activation of 5-HT3 receptor by 1-phenylbiguanide increases dopamine release in the rat nucleus accumbens , 1991, Brain Research.

[35]  R. Hitzemann,et al.  5-HT3 receptor antagonists block cocaine-induced locomotion via a PCPA-sensitive mechanism , 1992, Pharmacology Biochemistry and Behavior.

[36]  A. Greenshaw.  Behavioural pharmacology of 5-HT3 receptor antagonists: a critical update on therapeutic potential. , 1993, Trends in pharmacological sciences.

[37]  L. Chiodo,et al.  Ascending afferent regulation of rat midbrain dopamine neurons , 1993, Brain Research Bulletin.

[38]  X. Langlois,et al.  5-HT3 receptors in the rat central nervous system are mainly located on nerve fibres and terminals , 1993, Brain Research.

[39]  R. Leslie,et al.  5-HT3 receptor antagonists inhibit morphine-induced stimulation of mesolimbic dopamine release and function in the rat. , 1993, European journal of pharmacology.

[40]  R. Strecker,et al.  The 5-HT3 antagonist zacopride attenuates cocaine-induced increases in extracellular dopamine in rat nucleus accumbens , 1993, Pharmacology Biochemistry and Behavior.

[41]  C. W. Ogle,et al.  5‐HT3 antagonists reduce morphine self‐administration in rats , 1993, British journal of pharmacology.

[42]  L. Parsons,et al.  Perfusate serotonin increases extracellular dopamine in the nucleus accumbens as measured by in vivo microdialysis , 1993, Brain Research.

[43]  E. V. Bockstaele,et al.  Synaptic structure and connectivity of serotonin terminals in the ventral tegmental area: potential sites for modulation of mesolimbic dopamine neurons , 1994, Brain Research.

[44]  A. Gifford,et al.  The effect of 5-HT3 receptor antagonists on the morphine-induced excitation of A10 dopamine cells: electrophysiological studies , 1994, Brain Research.

[45]  P P Humphrey,et al.  International Union of Pharmacology classification of receptors for 5-hydroxytryptamine (Serotonin). , 1994, Pharmacological reviews.

[46]  J. Rı́o,et al.  Role of 5‐HT3 receptors in basal and K+‐evoked dopamine release from rat olfactory tubercle and striatal slices , 1994, British journal of pharmacology.

[47]  Steven W. Johnson,et al.  Actions of 5-hydroxytryptamine on ventral tegmental area neurons of the rat in vitro , 1994, Brain Research.

[48]  U. Spampinato,et al.  Evidence for 5-HT4 receptor subtype involvement in the enhancement of striatal dopamine release induced by serotonin: a microdialysis study in the halothane-anesthetized rat , 1995, Neuropharmacology.

[49]  T. Sharp,et al.  Release of cerebral 5-hydroxytryptamine evoked by electrical stimulation of the dorsal and median raphe nuclei: effect of a neurotoxic amphetamine , 1995, Neuroscience.

[50]  J. Cano,et al.  5‐HT3 receptor agonist induced carrier‐mediated release of dopamine in rat striatum in vivo , 1995, British journal of pharmacology.

[51]  M. Le Moal,et al.  d‐Fenfluramine Increases Striatal Extracellular Dopamine In Vivo Independently of Serotonergic Terminals or Dopamine Uptake Sites , 1995, Journal of neurochemistry.

[52]  L. Kirby,et al.  Effect of destruction of serotonin neurons on basal and fenfluramine‐induced serotonin release in striatum , 1995, Synapse.

[53]  Gavin Kilpatrick,et al.  5-HT3 and 5-HT4 receptors in terminal regions of the mesolimbic system , 1995, Behavioural Brain Research.

[54]  Effect of the 5-hydroxytryptamine3 receptor antagonist itasetron (DAU 6215) on (+)-N-allylnormetazocine-induced dopamine release in the nucleus accumbens and in the corpus striatum of the rat: an in vivo microdialysis study. , 1995, The Journal of pharmacology and experimental therapeutics.

[55]  E. Mylecharane.  Ventral tegmental area 5-HT receptors: mesolimbic dopamine release and behavioural studies , 1995, Behavioural Brain Research.

[56]  M. Tricklebank.  The antipsychotic potential of subtype-selective 5-HT receptor ligands based on interactions with mesolimbic dopamine systems , 1995, Behavioural Brain Research.

[57]  E. Melamed,et al.  Psychosis in advanced Parkinson's disease , 1995, Neurology.

[58]  E. Wong,et al.  Stereoselective effects of (R)- and (S)-zacopride on cognitive performance in a spatial navigation task in rats , 1996, Neuropharmacology.

[59]  L. Pozzi,et al.  5-HT3 receptor antagonists do not modify cocaine place conditioning or the rise in extracellular dopamine in the nucleus accumbens of rats , 1996, Pharmacology Biochemistry and Behavior.

[60]  Opposite changes in striatal neuropeptide Y immunoreactivity after partial and complete serotonergic depletion in the rat , 1996, Synapse.

[61]  Y. Minabe,et al.  The depletion of brain serotonin levels by para‐chlorophenylalanine administration significantly alters the activity of midbrain dopamine cells in rats: An extracellular single cell recording study , 1996, Synapse.

[62]  C R Ashby,et al.  Pharmacological actions of the atypical antipsychotic drug clozapine: A review , 1996, Synapse.

[63]  S. Kapur,et al.  Serotonin-dopamine interaction and its relevance to schizophrenia. , 1996, The American journal of psychiatry.

[64]  F. Bloom,et al.  The 5-HT3 Receptor Is Present in Different Subpopulations of GABAergic Neurons in the Rat Telencephalon , 1997, The Journal of Neuroscience.