Serotonin-dopamine interaction: electrophysiological evidence.

In this review, the most relevant data regarding serotonin (5-hydroxytryptamine, 5-HT)/dopamine (DA) interaction in the brain, as studied by both in vivo and in vitro electrophysiological methods, are reported and discussed. The bulk of neuroanatomical data available clearly indicate that DA-containing neurons in the brain receive a prominent innervation from 5-HT originating in the raphe nuclei of the brainstem. Furthermore, this modulation seems to be reciprocal; DA neurons innervate the raphe nuclei and exert a tonic excitatory effect on them. Compelling electrophysiological data show that 5-HT can exert complex effects on the electrical activity of midbrain DA neurons mediated by the various receptor subtypes. The main control seems to be inhibitory, this effect being more marked in the ventral tegmental area (VTA) as compared to the substantia nigra pars compacta (SNc). In spite of a direct effect of 5-HT by its receptors located on DA cells, 5-HT can modulate their activity indirectly, modifying gamma-amino-n-butyric acid (GABA)-ergic and glutamatergic input to the VTA and SNc. Although 5-HT/DA interaction in the brain has been extensively studied, much work remains to be done to clarify this issue. The recent development of subtype-selective ligands for 5-HT receptors will not only allow a detailed understanding of this interaction but also lead to development of new treatment strategies, appropriate for those neuropsychiatric disorders in which an alteration of the 5-HT/DA balance is supposed.

[1]  J. Palacios,et al.  Serotonin-1 receptor binding sites in the human basal ganglia are decreased in huntington's chorea but not in parkinson's disease: A quantitative in vitro autoradiography study , 1989, Neuroscience.

[2]  J. Kauer,et al.  Amphetamine Depresses Excitatory Synaptic Transmission via Serotonin Receptors in the Ventral Tegmental Area , 1999, The Journal of Neuroscience.

[3]  B. Bunney,et al.  Ritanserin, a 5-HT2A/2C antagonist, reverses direct dopamine agonist-induced inhibition of midbrain dopamine neurons. , 1995, The Journal of pharmacology and experimental therapeutics.

[4]  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.

[5]  L. Tecott,et al.  Inactivation of 5-HT2C Receptors Potentiates Consequences of Serotonin Reuptake Blockade , 2004, Neuropsychopharmacology.

[6]  T. Blackburn,et al.  Immunohistochemical localisation of the 5-HT2C receptor protein in the rat CNS , 2000, Neuropharmacology.

[7]  M. Geffard,et al.  Quantitative and morphometric data indicate precise cellular interactions between serotonin terminals and postsynaptic targets in rat substantia nigra , 1997, Neuroscience.

[8]  Y. Minabe,et al.  Acute and repeated administration of the selective 5‐HT2A receptor antagonist M100907 significantly alters the activity of midbrain dopamine neurons: An in vivo electrophysiological study , 2001, Synapse.

[9]  J. Palacios,et al.  Serotonin receptors in the human brain. II. Characterization and autoradiographic localization of 5-HT1C and 5-HT2 recognition sites , 1986, Brain Research.

[10]  Q. Wan,et al.  Disruption of PTEN coupling with 5-HT2C receptors suppresses behavioral responses induced by drugs of abuse , 2006, Nature Medicine.

[11]  K. Fuxe,et al.  EVIDENCE FOR THE EXISTENCE OF MONOAMINE NEURONS IN THE CENTRAL NERVOUS SYSTEM. IV. DISTRIBUTION OF MONOAMINE NERVE TERMINALS IN THE CENTRAL NERVOUS SYSTEM. , 1965, Acta physiologica Scandinavica. Supplementum.

[12]  W. Faustman,et al.  Zacopride in schizophrenia: a single-blind serotonin type 3 antagonist trial. , 1992, Archives of general psychiatry.

[13]  Saavedra Jm Distribution of serotonin and synthesizing enzymes in discrete areas of the brain. , 1977 .

[14]  L. Descarries,et al.  Cellular and subcellular distribution of the serotonin 5‐HT2A receptor in the central nervous system of adult rat , 1999, The Journal of comparative neurology.

[15]  A. Grace,et al.  Nigral dopamine neurons: intracellular recording and identification with L-dopa injection and histofluorescence. , 1980, Science.

[16]  T. Svensson,et al.  Ritanserin potentiates the stimulatory effects of raclopride on neuronal activity and dopamine release selectively in the mesolimbic dopaminergic system , 1995, Naunyn-Schmiedeberg's Archives of Pharmacology.

[17]  D. Dorsa,et al.  Colocalization of serotonin receptor subtypes 5‐HT2A, 5‐HT2C, and 5‐HT6 with neuropeptides in rat striatum , 1996, The Journal of comparative neurology.

[18]  H. Fibiger,et al.  An anatomical and electrophysiological investigation of the serotonergic projection from the dorsal raphe nucleus to the substantia nigra in the rat , 1977, Neuroscience.

[19]  C. Kruse,et al.  5-HT2 receptors differentially modulate dopamine-mediated auto-inhibition in A9 and A10 midbrain areas of the rat , 2004, Neuropharmacology.

[20]  C. Rouillard,et al.  Dorsal raphe stimulation differentially modulates dopaminergic neurons in the ventral tegmental area and substantia nigra , 2000, Synapse.

[21]  J. Williams,et al.  Australasian Society of Clinical and Experimental Pharmacologists and Toxicologists, 1994: OPPOSING ROLES FOR DOPAMINE AND SEROTONIN AT PRESYNAPTIC RECEPTORS IN THE VENTRAL TEGMENTAL AREA , 1995, Clinical and experimental pharmacology & physiology.

[22]  Jian Liu,et al.  Changes in the firing activity of serotonergic neurons in the dorsal raphe nucleus in a rat model of Parkinson's disease. , 2007, Sheng li xue bao : [Acta physiologica Sinica].

[23]  P. De Deurwaerdère,et al.  Neurochemical and electrophysiological evidence that 5‐HT4 receptors exert a state‐dependent facilitatory control in vivo on nigrostriatal, but not mesoaccumbal, dopaminergic function , 2001, The European journal of neuroscience.

[24]  T. Blackburn,et al.  Acute and repeated administration of fluoxetine, citalopram, and paroxetine significantly alters the activity of midbrain dopamine neurons in rats: An in vivo electrophysiological study , 2007, Synapse.

[25]  A. Beaudet,et al.  Serotonin axon terminals in the ventral tegmental area of the rat: fine structure and synaptic input to dopaminergic neurons , 1987, Brain Research.

[26]  J. Kehne,et al.  Characterization of the 5-HT2 receptor antagonist MDL 100907 as a putative atypical antipsychotic: behavioral, electrophysiological and neurochemical studies. , 1993, The Journal of pharmacology and experimental therapeutics.

[27]  M. Hamon,et al.  Cellular and subcellular localization of 5-hydroxytryptamine1B receptors in the rat central nervous system: immunocytochemical, autoradiographic and lesion studies , 1999, Neuroscience.

[28]  M. Millan,et al.  Serotonin2C receptors tonically suppress the activity of mesocortical dopaminergic and adrenergic, but not serotonergic, pathways: A combined dialysis and electrophysiological analysis in the rat , 2000, Synapse.

[29]  M. Jouvet,et al.  Afferent connections of the nucleus raphe dorsalis in the cat as visualized by the horseradish peroxidase technique , 1977, Brain Research.

[30]  B. Bunney,et al.  Possible mechanisms by which repeated clozapine administration differentially affects the activity of two subpopulations of midbrain dopamine neurons , 1985, Journal of Neuroscience.

[31]  T. Maeda,et al.  Distribution of dopamine-immunoreactive fibers in the rat brainstem , 2000, Journal of Chemical Neuroanatomy.

[32]  Elyssa B. Margolis,et al.  The ventral tegmental area revisited: is there an electrophysiological marker for dopaminergic neurons? , 2006, The Journal of physiology.

[33]  Wei-Xing Shi Slow oscillatory firing: a major firing pattern of dopamine neurons in the ventral tegmental area. , 2005, Journal of neurophysiology.

[34]  B. Roth,et al.  Localization of 5-HT2A receptors on dopamine cells in subnuclei of the midbrain A10 cell group , 2002, Neuroscience.

[35]  D. Wright,et al.  Comparative localization of serotonin1A, 1C, and 2 receptor subtype mRNAs in rat brain , 1995, The Journal of comparative neurology.

[36]  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.

[37]  M. Millan,et al.  Induction of burst firing in ventral tegmental area dopaminergic neurons by activation of serotonin (5‐HT)1A receptors: WAY 100,635‐reversible actions of the highly selective ligands, flesinoxan and S 15535 , 1998, Synapse.

[38]  J. Bolam,et al.  Uniform Inhibition of Dopamine Neurons in the Ventral Tegmental Area by Aversive Stimuli , 2004, Science.

[39]  T. Svensson,et al.  Ritanserin, a 5-HT2 receptor antagonist, activates midbrain dopamine neurons by blocking serotonergic inhibition , 2004, Psychopharmacology.

[40]  Q. Yan,et al.  Serotonin‐1B receptor‐mediated inhibition of [3H]GABA release from rat ventral tegmental area slices , 2001, Journal of neurochemistry.

[41]  M. Brodie,et al.  The effects of clomipramine on the excitatory action of ethanol on dopaminergic neurons of the ventral tegmental area in vitro. , 1996, The Journal of pharmacology and experimental therapeutics.

[42]  B. Bunney,et al.  Inhibition of both noradrenergic and serotonergic neurons in brain by the α-adrenergic agonist clonidine , 1975, Brain Research.

[43]  M. Staufenbiel,et al.  Localization of the 5-hydroxytryptamine2C receptor protein in human and rat brain using specific antisera , 1995, Neuropharmacology.

[44]  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.

[45]  J. Palacios,et al.  Quantitative autoradiographic mapping of serotonin receptors in the rat brain. I. Serotonin-1 receptors , 1985, Brain Research.

[46]  J. Barrett,et al.  WAY-163909 [(7bR,10aR)-1,2,3,4,8,9,10,10a-Octahydro-7bH-cyclopenta-[b][1,4]diazepino[6,7,1hi]indole]: A Novel 5-Hydroxytryptamine 2C Receptor-Selective Agonist with Preclinical Antipsychotic-Like Activity , 2007, Journal of Pharmacology and Experimental Therapeutics.

[47]  M. Brodie,et al.  Serotonin potentiates dopamine inhibition of ventral tegmental area neurons in vitro. , 1996, Journal of neurophysiology.

[48]  Kieran Rea,et al.  Augmentation of SSRI Effects on Serotonin by 5-HT2C Antagonists: Mechanistic Studies , 2007, Neuropsychopharmacology.

[49]  C. Sinton,et al.  Electrophysiological evidence for a functional differentiation between subtypes of the 5-HT1 receptor. , 1988, European journal of pharmacology.

[50]  B. Bunney,et al.  Dopamine “Autoreceptors”: Pharmacological characterization by microiontophoretic single cell recording studies , 1977, Naunyn-Schmiedeberg's Archives of Pharmacology.

[51]  M. Brodie,et al.  Cocaine potentiates ethanol-induced excitation of dopaminergic reward neurons in the ventral tegmental area. , 2000, The Journal of pharmacology and experimental therapeutics.

[52]  K. Rasmussen,et al.  The 5-HT3 receptor antagonist zatosetron decreases the number of spontaneously active A10 dopamine neurons. , 1991, European journal of pharmacology.

[53]  F. Artigas,et al.  Dopamine D2 receptor-mediated regulation of serotonin extracellular concentration in the dorsal raphe nucleus of freely moving rats. , 2006, Journal of neurochemistry.

[54]  U. Spampinato,et al.  Selective blockade of serotonin-2C/2B receptors enhances mesolimbic and mesostriatal dopaminergic function: a combined in vivo electrophysiological and microdialysis study , 1999, Neuroscience.

[55]  E. Esposito,et al.  Serotonin-dopamine interaction in the rat ventral tegmental area: an electrophysiological study in vivo. , 1994, The Journal of pharmacology and experimental therapeutics.

[56]  Y. Minabe,et al.  The 5-HT3 receptor antagonists LY 277359 and granisetron potentiate the suppressant action of apomorphine on the basal firing rate of ventral tegmental dopamine cells. , 1991, European journal of pharmacology.

[57]  J. Axelrod,et al.  Serotonin stimulates phospholipase A2 and the release of arachidonic acid in hippocampal neurons by a type 2 serotonin receptor that is independent of inositolphospholipid hydrolysis. , 1990, Proceedings of the National Academy of Sciences of the United States of America.

[58]  K. Shannak,et al.  Brain monoamines in the rhesus monkey during long-term neuroleptic administration. , 1980, Advances in biochemical psychopharmacology.

[59]  A. Grace,et al.  The control of firing pattern in nigral dopamine neurons: burst firing , 1984, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[60]  E. Esposito,et al.  Stimulation of Serotonin2C Receptors Blocks the Hyperactivation of Midbrain Dopamine Neurons Induced by Nicotine Administration , 2004, Journal of Pharmacology and Experimental Therapeutics.

[61]  R. Vertes,et al.  Comparison of projections of the dorsal and median raphe nuclei, with some functional considerations , 2007 .

[62]  K. Hashimoto,et al.  Effect of the acute and chronic administration of the selective 5‐HT6 receptor antagonist SB‐271046 on the activity of midbrain dopamine neurons in rats: An in vivo electrophysiological study , 2004, Synapse.

[63]  S. Haj-Dahmane,et al.  D2-Like Dopamine Receptors Depolarize Dorsal Raphe Serotonin Neurons through the Activation of Nonselective Cationic Conductance , 2007, Journal of Pharmacology and Experimental Therapeutics.

[64]  J. Williams,et al.  A subset of ventral tegmental area neurons is inhibited by dopamine, 5-hydroxytryptamine and opioids , 1997, Neuroscience.

[65]  R. Roth,et al.  Dopaminergic neurons: effect of antipsychotic drugs and amphetamine on single cell activity. , 1973, The Journal of pharmacology and experimental therapeutics.

[66]  Role of central 5-HT2C receptor in the control of basal ganglia functions , 2007 .

[67]  O. Lindvall,et al.  Projections from the ventral tegmental area and mesencephalic raphe to the dorsal raphe nucleus in the rat , 1988, Experimental Brain Research.

[68]  V. Grutta,et al.  m-Chlorophenylpiperazine excites non-dopaminergic neurons in the rat substantia nigra and ventral tegmental area by activating serotonin-2C receptors , 2001, Neuroscience.

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

[70]  Trevor Sharp,et al.  A review of central 5-HT receptors and their function , 1999, Neuropharmacology.

[71]  J. Hagan,et al.  5‐HT6 receptor antagonist SB‐271046 enhances extracellular levels of monoamines in the rat medial prefrontal cortex , 2004, Synapse.

[72]  P. Celada,et al.  Involvement of 5-HT1A Receptors in Prefrontal Cortex in the Modulation of Dopaminergic Activity: Role in Atypical Antipsychotic Action , 2005, The Journal of Neuroscience.

[73]  J. Williams,et al.  Cocaine inhibits GABA release in the VTA through endogenous 5-HT , 1994, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[74]  G. Mengod,et al.  Control of serotonergic neurons in rat brain by dopaminergic receptors outside the dorsal raphe nucleus , 2001, Journal of neurochemistry.

[75]  K. Uryu,et al.  Pattern of expression of the serotonin2C receptor messenger RNA in the basal ganglia of adult rats , 1997, The Journal of comparative neurology.

[76]  D. Morilak,et al.  Immunocytochemical localization and description of neurons expressing serotonin2 receptors in the rat brain , 1993, Neuroscience.

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

[78]  E. Esposito,et al.  Serotonin involvement in the basal ganglia pathophysiology: could the 5-HT2C receptor be a new target for therapeutic strategies? , 2006, Current medicinal chemistry.

[79]  A. Dray,et al.  Evidence for the existence of a raphe projection to the substantia nigra in rat , 1976, Brain Research.

[80]  C. Kruse,et al.  Modulation of midbrain dopamine neurotransmission by serotonin, a versatile interaction between neurotransmitters and significance for antipsychotic drug action. , 2006, Current neuropharmacology.

[81]  K. Fuxe,et al.  Evidence for the existence of monoamine neurons in the central nervous system , 1965, Zeitschrift für Zellforschung und Mikroskopische Anatomie.

[82]  A. Grace,et al.  Intracellular and extracellular electrophysiology of nigral dopaminergic neurons—2. Action potential generating mechanisms and morphological correlates , 1983, Neuroscience.

[83]  U. Spampinato,et al.  5-HT2A and 5-HT2C/2B Receptor Subtypes Modulate Dopamine Release Induced in Vivo by Amphetamine and Morphine in Both the Rat Nucleus Accumbens and Striatum , 2002, Neuropsychopharmacology.

[84]  E. Esposito,et al.  Role of 5-HT(2C) receptors in the control of central dopamine function. , 2001, Trends in pharmacological sciences.

[85]  M. Pompeiano,et al.  Distribution of the serotonin 5-HT2 receptor family mRNAs: comparison between 5-HT2A and 5-HT2C receptors. , 1994, Brain research. Molecular brain research.

[86]  A. Parent,et al.  Immunohistochemical study of the serotoninergic innervation of the basal ganglia in the squirrel monkey , 1990, The Journal of comparative neurology.

[87]  H. Akil,et al.  Localization of dopamine D2 receptor mRNA and D1 and D2 receptor binding in the rat brain and pituitary: an in situ hybridization- receptor autoradiographic analysis , 1990, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[88]  E. Esposito,et al.  Preferential modulation of mesolimbic vs. nigrostriatal dopaminergic function by serotonin2C/2B receptor agonists: a combined in vivo electrophysiological and microdialysis study , 2000, Synapse.

[89]  J. Maj,et al.  Effects of sertraline and citalopram given repeatedly on the responsiveness of 5-HT receptor subpopulations , 2005, Journal of Neural Transmission / General Section JNT.

[90]  Peter S. Freestone,et al.  Acute effects of 6-hydroxydopamine on dopaminergic neurons of the rat substantia nigra pars compacta in vitro. , 2005, Neurotoxicology.

[91]  R. Roth,et al.  Comparison of effects of L-dopa, amphetamine and apomorphine on firing rate of rat dopaminergic neurones. , 1973, Nature: New biology.

[92]  P. Davies,et al.  REGIONAL DISTRIBUTION OF MONOAMINES AND THEIR METABOLITES IN THE HUMAN BRAIN , 1978, Journal of neurochemistry.

[93]  S. A. Shefner,et al.  Serotonin potentiates ethanol-induced excitation of ventral tegmental area neurons in brain slices from three different rat strains. , 1995, The Journal of pharmacology and experimental therapeutics.

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

[95]  K. Cunningham,et al.  Serotonin2C receptor localization in GABA neurons of the rat medial prefrontal cortex: Implications for understanding the neurobiology of addiction , 2007, Neuroscience.

[96]  J. Bolam,et al.  Facilitation of a dendritic calcium conductance by 5-hydroxytryptamine in the substantia nigra , 1988, Nature.

[97]  G. Doucet,et al.  Ultrastructure and synaptic targets of the raphe-nigral projection in the rat , 1993, Neuroscience.

[98]  P. Sokoloff,et al.  D3 dopamine receptor mRNA is widely expressed in the human brain , 1998, Brain Research.

[99]  J. Palacios,et al.  Localization of 5-HT1B, 5-HT1Dα, 5-HT1E and 5-HT1F receptor messenger RNA in rodent and primate brain , 1994, Neuropharmacology.

[100]  M. Mikuni,et al.  Human midbrain dopamine neurons express serotonin 2A receptor: an immunohistochemical demonstration , 2000, Brain Research.

[101]  H. Steinbusch,et al.  Distribution of serotonin-immunoreactivity in the central nervous system of the rat—Cell bodies and terminals , 1981, Neuroscience.

[102]  T. Sharp,et al.  Investigation of the SSRI augmentation properties of 5-HT2 receptor antagonists using in vivo microdialysis , 2006, Neuropharmacology.

[103]  Elyssa B. Margolis,et al.  Kappa opioids selectively control dopaminergic neurons projecting to the prefrontal cortex. , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[104]  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.

[105]  W. Nauta,et al.  Efferent connections of the substantia nigra and ventral tegmental area in the rat , 1979, Brain Research.

[106]  E. Esposito,et al.  Central serotonin2C receptor: from physiology to pathology. , 2006, Current topics in medicinal chemistry.

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

[108]  K. Cunningham,et al.  Distribution of serotonin 5-HT2C receptors in the ventral tegmental area , 2007, Neuroscience.

[109]  T. Blackburn,et al.  Evidence for expression of the 5-hydroxytryptamine-2B receptor protein in the rat central nervous system , 1997, Neuroscience.

[110]  C. Müller,et al.  Intracellular 5-HT 2C-receptor dephosphorylation: a new target for treating drug addiction. , 2006, Trends in pharmacological sciences.

[111]  M. Pompeiano,et al.  Localization of the mRNA for the 5-HT2 receptor by in situ hybridization histochemistry. Correlation with the distribution of receptor sites , 1990, Brain Research.

[112]  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.

[113]  C. Ashby,et al.  Chronic BRL 43694, a selective 5-HT3 receptor antagonist, fails to alter the number of spontaneously active midbrain dopamine neurons. , 1990, European journal of pharmacology.

[114]  C. Montigny,et al.  Effect of repeated amiflamine administration on serotonergic and noradrenergic neurotransmission: Electrophysiological studies in the rat CNS , 1986, Naunyn-Schmiedeberg's Archives of Pharmacology.

[115]  E. Esposito,et al.  Chronic treatment with DAU 6215, a new 5-HT3 receptor antagonist, causes a selective decrease in the number of spontaneously active dopaminergic neurons in the rat ventral tegmental area. , 1992, European journal of pharmacology.

[116]  A. Grace,et al.  Induction of depolarization block in midbrain dopamine neurons by repeated administration of haloperidol: analysis using in vivo intracellular recording. , 1986, The Journal of pharmacology and experimental therapeutics.

[117]  V. Pickel,et al.  Ultrastructure of serotonin‐immunoreactive terminals in the core and shell of the rat nucleus accumbens: Cellular substrates for interactions with catecholamine afferents , 1993, The Journal of comparative neurology.

[118]  A. Tozzi,et al.  Depression of mGluR‐mediated IPSCs by 5‐HT in dopamine neurons of the rat substantia nigra pars compacta , 2003, The European journal of neuroscience.

[119]  Daniel Hoyer,et al.  Molecular, pharmacological and functional diversity of 5-HT receptors , 2002, Pharmacology Biochemistry and Behavior.

[120]  M. Brodie,et al.  Serotonin reduces the hyperpolarization-activated current (Ih) in ventral tegmental area dopamine neurons: involvement of 5-HT2 receptors and protein kinase C. , 2003, Journal of neurophysiology.

[121]  A. Grace,et al.  Intracellular and extracellular electrophysiology of nigral dopaminergic neurons—1. Identification and characterization , 1983, Neuroscience.

[122]  J. Palacios,et al.  The distribution and cellular localization of the serotonin 1C receptor mRNA in the rodent brain examined by in situ hybridization histochemistry. Comparison with receptor binding distribution , 1990, Neuroscience.

[123]  N. Mons,et al.  First visualization of dopaminergic neurons with a monoclonal antibody to dopamine: a light and electron microscopic study. , 1987, The journal of histochemistry and cytochemistry : official journal of the Histochemistry Society.

[124]  V. Pickel,et al.  Targeting of serotonin 1a receptors to dopaminergic neurons within the parabrachial subdivision of the ventral tegmental area in rat brain , 2001, The Journal of comparative neurology.

[125]  T. Matsuura,et al.  Light and electron microscopic immunohistochemical studies of serotonin nerve fibers in the substantia nigra of the rat, cat and monkey , 2004, Anatomy and Embryology.

[126]  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.

[127]  M. Palkovits,et al.  Serotonin content of the brain stem nuclei in the rat. , 1974, Brain research.

[128]  J. Harvey,et al.  Physiological relevance of constitutive activity of 5-HT2A and 5-HT2C receptors. , 2005, Trends in pharmacological sciences.

[129]  I. Martin,et al.  Molecular biology of 5-HT receptors , 1994, Neuropharmacology.

[130]  M. Castagna,et al.  Distribution and cellular localization of the serotonin type 2C receptor messenger RNA in human brain , 1999, Neuroscience.

[131]  J. Palacios,et al.  Serotonin receptors in the human brain—IV. Autoradiographic mapping of serotonin-2 receptors , 1987, Neuroscience.

[132]  Zul Merali,et al.  Functional interactions between dopamine, serotonin and norepinephrine neurons: an in-vivo electrophysiological study in rats with monoaminergic lesions. , 2008, The international journal of neuropsychopharmacology.

[133]  S. Haj-Dahmane D2‐like dopamine receptor activation excites rat dorsal raphe 5‐HT neurons in vitro , 2001, The European journal of neuroscience.

[134]  K. Hashimoto,et al.  Effect of acute and chronic administration of the selective 5‐HT2C receptor antagonist SB‐243213 on midbrain dopamine neurons in the rat: An in vivo extracellular single cell study , 2002, Synapse.

[135]  U. Spampinato,et al.  Central serotonin4 receptors selectively regulate the impulse-dependent exocytosis of dopamine in the rat striatum: in vivo studies with morphine, amphetamine and cocaine , 2002, Neuropharmacology.

[136]  Effects of the serotonin 5-HT(7) receptor antagonist SB-269970 on the inhibition of dopamine neuronal firing induced by amphetamine. , 2007, European journal of pharmacology.

[137]  Donatella Marazziti,et al.  Distribution and characterization of [3H]mesulergine binding in human brain postmortem , 1999, European Neuropsychopharmacology.

[138]  E. Esposito,et al.  The degree of inhibition of dopaminergic neurons in the ventral tegmental area induced by selective serotonin reuptake inhibitors is a function of the density-power-spectrum of the interspike interval. , 1997, Neuroscience.

[139]  N. Mercuri,et al.  5-hydroxytryptamine1B receptors block the GABAB synaptic potential in rat dopamine neurons , 1992, The Journal of neuroscience : the official journal of the Society for Neuroscience.

[140]  G. Martin,et al.  Receptors for 5-Hydroxytryptamine: Current perspectives on classification and nomenclature , 1994, Neuropharmacology.

[141]  E. Esposito,et al.  Selective activation of 5-HT2C receptors stimulates GABA-ergic function in the rat substantia nigra pars reticulata: A combined in vivo electrophysiological and neurochemical study , 2007, Neuroscience.

[142]  M. Palfreyman,et al.  Effect of acute and chronic MDL 73,147EF, a 5-HT3 receptor antagonist, on A9 and A10 dopamine neurons. , 1989, European journal of pharmacology.

[143]  E. Esposito,et al.  Biochemical and electrophysiological evidence that RO 60-0175 inhibits mesolimbic dopaminergic function through serotonin2C receptors , 2000, Brain Research.

[144]  P. Tongroach,et al.  The dorsal and medial raphe projections to the substantia nigra in the rat: Electrophysiological, biochemical and behavioural observations , 1978, Brain Research.

[145]  [Changes of discharge rate and pattern of 5-hydroxytrypamine neurons of dorsal raphe nucleus in a rat model of Parkinson's disease]. , 2004, Sheng li xue bao : [Acta physiologica Sinica].

[146]  V. Pickel,et al.  Ultrastructural localization of the serotonin 2A receptor in dopaminergic neurons in the ventral tegmental area , 2000, Brain Research.

[147]  L. Chiodo Dopamine-containing neurons in the mammalian central nervous system: Electrophysiology and pharmacology , 1988, Neuroscience & Biobehavioral Reviews.

[148]  S Fahn,et al.  Monoamines in the human neostriatum: topographic distribution in normals and in Parkinson's disease and their role in akinesia, rigidity, chorea, and tremor. , 1971, Journal of the neurological sciences.

[149]  J. Tepper,et al.  Dorsal raphé stimulation modifies striatal-evoked antidromic invasion of nigral dopaminergic neurons in vivo , 1991, Experimental Brain Research.

[150]  E. Esposito,et al.  Differential effects of acute and chronic fluoxetine administration on the spontaneous activity of dopaminergic neurones in the ventral tegmental area , 1995, British journal of pharmacology.

[151]  E. Esposito,et al.  SB 242 084, a selective serotonin2C receptor antagonist, increases dopaminergic transmission in the mesolimbic system , 1999, Neuropharmacology.

[152]  K. Chergui,et al.  The 5-HT1A receptor selective ligands, (R)-8-OH-DPAT and (S)-UH-301, differentially affect the activity of midbrain dopamine neurons , 1993, Naunyn-Schmiedeberg's Archives of Pharmacology.