Endogenous serotonin excites striatal cholinergic interneurons via the activation of 5-HT 2C, 5-HT6, and 5-HT7 serotonin receptors: Implications for extrapyramidal side effects of serotonin reuptake inhibitors

Neuropsychopharmacology

Volumn 32, Issue 8, 2007, Pages 1840-1854

  Bonsi, Paola ^a   Cuomo, Dario ^a,b   Ding, Jun ^c   Sciamanna, Giuseppe ^a   Ulrich, Sasha ^c   Tscherter, Anne ^b   Bernardi, Giorgio ^a,b   Surmeier, D James ^c   Pisani, Antonio ^a,b  

^a EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^b UNIVERSITY OF ROME TOR VERGATA   (Italy)

^c NORTHWESTERN UNIVERSITY   (United States)

Author keywords

5 HT; Cholinergic interneuron; Electrophysiology; Slices; Striatum; TANs

Indexed keywords

1 [[6 (3 METHOXYESTRA 1,3,5(10) TRIEN 17BETA YL)AMINO]HEXYL] 1H PYRROLE 2,5 DIONE; 3 [2 [2 (4 METHYL 1 PIPERIDINYL)ETHYL] 1 PYRROLIDINESULFONYL]PHENOL; 4 AMINO 5 CHLORO 2 METHOXYBENZOIC ACID 3 PIPERIDINOPROPYL ESTER; 4 IODO 2,5 DIMETHOXYAMPHETAMINE; 8 [4 (5 AMINO 2,4 DIMETHOXYBENZOYL)BUTYL] 1,3,8 TRIAZASPIRO[4.5]DECANE 2,4 DIONE; 9 (TETRAHYDRO 2 FURYL)ADENINE; BARIUM; CITALOPRAM; FLUVOXAMINE; KETANSERIN; MESSENGER RNA; PHOSPHOLIPASE C; POTASSIUM CHANNEL; POTASSIUM ION; SB 258585; SEROTONIN; SEROTONIN 1 AGONIST; SEROTONIN 2 AGONIST; SEROTONIN 2C ANTAGONIST; SEROTONIN 2C RECEPTOR; SEROTONIN 3 ANTAGONIST; SEROTONIN 4 ANTAGONIST; SEROTONIN 6 ANTAGONIST; SEROTONIN 6 RECEPTOR; SEROTONIN 7 RECEPTOR; SEROTONIN AGONIST; SEROTONIN ANTAGONIST; SEROTONIN UPTAKE INHIBITOR; TROPISETRON; UNCLASSIFIED DRUG; UNINDEXED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CHOLINERGIC NERVE; CONTROLLED STUDY; DEPOLARIZATION; EXTRAPYRAMIDAL SYMPTOM; INTERNEURON; INTRACELLULAR RECORDING; MALE; MEMBRANE CURRENT; MEMBRANE DEPOLARIZATION; NERVE EXCITABILITY; NERVE POTENTIAL; NONHUMAN; NUCLEOTIDE SEQUENCE; PATCH CLAMP; PRIORITY JOURNAL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; WHOLE CELL;

ACETYLCHOLINE; ANIMALS; CORPUS STRIATUM; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ELECTRIC STIMULATION; ENZYME INHIBITORS; INTERNEURONS; MALE; MEMBRANE POTENTIALS; PATCH-CLAMP TECHNIQUES; RATS; RATS, WISTAR; RECEPTORS, SEROTONIN; SEROTONIN; SEROTONIN AGENTS;

EID: 34250191571     PISSN: 0893133X     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.npp.1301294     Document Type: Article

References (68)

1. 123I]iodobenzovesamicol binding in idiopathic cervical dystonia. Ann Neurol 53: 528-532.
2. Aosaki T, Kiuchi K, Kawaguchi Y (1998). Dopamine D1-like receptor activation excites rat striatal large aspiny neurons in vitro. J Neurosci 18: 5180-5190.
3. Bayliss DA, Li YW, Talley EM (1997). Effects of serotonin on caudal raphe neurons: inhibition of N- and P/Q-type calcium channels and the afterhyperpolarization. J Neurophysiol 77: 1362-1374.
4. Bennett BD, Callaway JC, Wilson CJ (2000). Intrinsic membrane properties underlying spontaneous tonic firing in neostriatal cholinergic interneurons. J Neurosci 20: 8493-8503.
5. Bennett BD, Wilson CJ (1999). Spontaneous activity of neostriatal cholinergic interneurons in vitro. J Neurosci 19: 5586-5596.
6. Bianchi C, Siniscalchi A, Beani L (1989). Effect of 5-hydroxytryptamine on [3H]-acetylcholine release from guinea-pig striatal slices. Br J Pharmacol 97: 213-221.
7. Blandina P, Goldfarb J, Craddock-Royal B, Green JP (1989). Release of endogenous dopamine by stimulation of 5-hydroxytryptamine3 receptors in rat striatum. J Pharmacol Exp Ther 251: 803-809.
8. Bonsi P, Cuomo D, De Persis C, Centonze D, Bernardi G, Calabresi P et al (2005). Modulatory action of metabotropic glutamate receptor (mGluR) 5 on mGluR1 function in striatal cholinergic interneurons. Neuropharmacology 49: 104-113.
9. Bonsi P, De Persis C, Calabresi P, Bernardi G, Pisani A (2004). Coordinate high-frequency pattern of stimulation and calcium levels control the induction of LTP in striatal cholinergic interneurons. Learn Mem 11: 755-760.
10. Bourson A, Boess FG, Bos M, Sleight AJ (1998). Involvement of 5-HT6 receptors in nigro-striatal function in rodents. Br J Pharmacol 125: 1562-1566.
11. Branchek TA, Blackburn TP (2000). 5-HT6 receptors as emerging targets for drug discovery. Annu Rev Toxicol 40: 319-334.
12. Bruinvels AT, Landwehrmeyer B, Gustafson EL, Durkin MM, Mengod G, Branchek TA et al (1994). Localization of 5-HT1B, 5-HT1Dalpha, 5-HT1E and 5-HT1F receptor messenger RNA in rodent and primate brain. Neuropharm 33: 367-386.
13. Caley CF (1997). Extrapyramidal reactions and the selective serotonin-reuptake inhibitors. Ann Pharmacother 31: 1481-1489.
14. Cassel J-C, Jeltsch H (1995). Serotonergic modulation of cholinergic function in the central nervous system: cognitive implications. Neurosci 69: 1-41.
15. Chapin EM, Andrade R (2001). A 5-HT(7) receptor-mediated depolarization in the anterodorsal thalamus. II. Involvement of the hyperpolarization-activated current I(h). J Pharmacol Exp Ther 297: 403-409.
16. Chapin EM, Haj-Dahmane S, Torres G, Andrade R (2002). The 5-HT(4) receptor-induced depolarization in rat hippocampal neurons is mediated by cAMP but is independent of I(h). Neurosci Lett 324: 1-4.
17. De Deurwaerdere P, Navailles S, Berg KA, Clarke WP, Spampinato U (2004). Constitutive activity of the serotonin2C receptor inhibits in vivo dopamine release in the rat striatum and nucleus accumbens. J Neurosci 24: 3235-3241.
18. Gerald C, Adham N, Kao HT, Olsen MA, Laz TM, Schechter LE et al (1995). The 5-HT4 receptor: molecular cloning and pharmacological characterization of two splice variants. EMBO J 14: 2806-2815.
19. Gerard C, Martres MP, Lefevre K, Miquel MC, Verge D, Lanfumey L et al (1997). Immuno-localization of serotonin 5-HT6 receptor-like material in the rat central nervous system. Brain Res 746: 207-219.
20. Halliday GM, Blumbergs PC, Cotton RG, Blessing WW, Geffen LB (1990). Loss of brainstem serotonin- and substance P-containing neurons in Parkinson's disease. Brain Res 510: 104-107.
21. Hopwood SE, Trapp S (2005). TASK-like K+ channels mediate effects of 5-HT and extracellular pH in rat dorsal vagal neurones in vitro. J Physiol 568: 145-154.
22. Hoyer D, Hannon JP, Martin GR (2002). Molecular, pharmacological and functional diversity of 5-HT receptors. Pharmacol Biochem Behav 71: 533-554.
23. Hsiao CF, Trueblood PR, Levine MS, Chandler SH (1997). Multiple effects of serotonin on membrane properties of trigeminal motoneurons in vitro. J Neurophysiol 77: 2910-2924.
24. Izzo PN, Bolam JP (1988). Cholinergic synaptic input to different parts of spiny striatonigral neurons in the rat. J Comp Neurol 269: 219-234.
25. Jakeman LB, To ZP, Eglen RM, Wong EH, Bonhaus DW (1994). Quantitative autoradiography of 5-HT4 receptors in brains of three species using two structurally distinct radioligands, [3H]GR113808 and [3H]BIMU-1. Neuropharm 33: 1027-1038.
26. Jiang ZG, North RA (1991). Membrane properties and synaptic responses of rat striatal neurones in vitro. J Physiol 443: 533-553.
27. Kaneko S, Hikida T, Watanabe D, Ichinose H, Nagatsu T, Kreitman RJ et al (2000). Synaptic integration mediated by striatal cholinergic interneurons in basal ganglia function. Science 289: 633-637.
28. Kawaguchi Y (1993). Physiological, morphological and histochemical characterization of three classes of interneurons in rat neostriatum. J Neurosci 13: 4908-4923.
29. Kjaerulff O, Kiehn O (2001). 5-HT modulation of multiple inward rectifiers in motoneurons in intact preparations of the neonatal rat spinal cord. J Neurophysiol 85: 580-593.
30. Larkman PM, Kelly JS (1997). Modulation of IH by 5-HT in neonatal rat motoneurones in vitro: mediation through a phosphorylation independent action of cAMP. Neuropharmacology 36: 721-733.
31. Lavoie B, Parent A (1990). Immunohistochemical study of the serotoninergic innervation of the basal ganglia in the squirrel monkey. J Comp Neurol 299: 1-16.
32. Lehmann J, Langer SZ (1983). The striatal cholinergic interneuron: synaptic target of dopaminergic terminals? Neuroscience 10: 1105-1120.
33. Leo RJ (1996). Movement disorders associated with the serotonin selective reuptake inhibitors. J Clin Psychiatry 57: 449-454.
34. Li SJ, Wang Y, Strahlendorf HK, Strahlendorf JC (1993). Serotonin alters an inwardly rectifying current (Ih) in rat cerebellar Purkinje cells under voltage clamp. Brain Res 617: 87-95.
35. Liu Z, Bunney EB, Appel SB, Brodie MS (2003). Serotonin reduces the hyperpolarization-activated current (Ih) in ventral tegmental area dopamine neurons: involvement of 5-HT2 receptors and protein kinase C. J Neurophysiol 90: 3201-3212.
36. Martin-Cora FJ, Pazos A (2004). Autoradiographic distribution of 5-HT7 receptors in the human brain using [3H]mesulergine: comparison to other mammalian species. Br J Pharmacol 141: 92-104.
37. Maurice N, Mercer J, Chan CS, Hernandez-Lopez S, Held J, Tkatch T et al (2004). D2 dopamine receptor-mediated modulation of voltage-dependent Na+ channels reduces autonomous activity in striatal cholinergic interneurons. J Neurosci 24: 10289-10301.
38. McCormick DA, Pape HC (1990). Noradrenergic and serotonergic modulation of a hyperpolarization-activated cation current in thalamic relay neurones. J Physiol 431: 319-342.
39. North RA, Uchimura N (1989). 5-Hydroxytryptamine acts at 5-HT2 receptors to decrease potassium conductance in rat nucleus accumbens neurones. J Physiol 417: 1-12.
40. Pape HC (1996). Queer current and pacemaker: hyperpolarization-activated cation current in neurons. Annu Rev Physiol 58: 299-327.
41. Park MR, Gonzales-Vegas JA, Kitai ST (1982). Serotonergic excitation from dorsal raphe stimulation recorded intracellularly from rat caudate-putamen. Brain Res 243: 49-58.
42. Patel S, Roberts J, Moorman J, Reavill C (1995). Localization of serotonin-4 receptors in the striatonigral pathway in rat brain. Neurosci 69: 1159-1167.
43. Pina Latorre MA, Modrego PJ, Rodilla F, Catalan C, Calvo M (2001). Parkinsonism and Parkinson's disease associated with long-term administration of sertraline. J Clin Pharm Ther 26: 111-112.
44. Pisani A, Bonsi P, Centonze D, Calabresi P, Bernardi G (2000). Activation of D2-like dopamine receptors reduces synaptic inputs to striatal cholinergic interneurons. J Neurosci 20: RC69.
45. Pisani A, Bonsi P, Centonze D, Martorana A, Fusco F, Sancesario G et al (2003). Activation of β1-adrenoceptors excites striatal cholinergic interneurons through a cAMP-dependent, protein kinase-independent pathway. J Neurosci 23: 5272-5282.
46. Raz A, Frechter-Mazar V, Feingold A, Abeles M, Vaadia E, Bergman H (2001). Activity of pallidal and striatal tonically active neurons is correlated in mptp-treated monkeys but not in normal monkeys. J Neurosci 21: RC128.
47. Rick CE, Stanford IM, Lacey MG (1995). Excitation of rat substantia nigra pars reticulata neurons by 5-hydroxytryptamine in vitro: evidence for a direct action mediated by 5-hydroxytryptamine2C receptors. Neurosci 69: 903-913.
48. Rondé P, Nichols RA (1998). High calcium permeability of serotonin 5-HT3 receptors on presynaptic nerve terminals from rat striatum. J Neurochem 70: 1094-1103.
49. Ruat M, Traiffort E, Arrang JM, Tardivel-Lacombe J, Diaz J, Leurs R et al (1993). A novel rat serotonin (5-HT6) receptor: molecular cloning, localization and stimulation of cAMP accumulation. Biochem Biophys Res Commun 193: 268-276.
50. Sandyk R, Fisher H (1988). Serotonin in involuntary movement disorders. Int J Neurosci 42: 185-208.
51. Saulle E, Gubellini P, Picconi B, Centonze D, Tropepi D, Pisani A et al (2004). Neuronal vulnerability following inhibition of mitochondrial complex II: a possible ionic mechanism for Huntington's disease. Mol Cell Neurosci 25: 9-20.
52. Sebben M, Ansanay H, Bockaert J, Dumuis A (1994). 5-HT6 receptors positively coupled to adenylyl cyclase in striatal neurones in culture. Neuroreport 18: 2553-2557.
53. + channels in Aplysia sensory neurons. Nature 299: 413-417.
54. Stefani A, Surmeier DJ, Kitai ST (1990). Serotonin enhances excitability in neostriatal neurons by reducing voltage-dependent potassium currents. Brain Res 529: 354-357.
55. Suzuki T, Miura M, Nishimura K, Aosaki T (2001). Dopamine-dependent synaptic plasticity in the striatal cholinergic interneurons. J Neurosci 21: 6492-6501.
56. Takano K, Yasufuku-Takano J, Kozasa T, Singer WD, Nakajima S, Nakajima Y (1996). Gq/11 and PLC-beta 1 mediate the substance P-induced inhibition of an inward rectifier K+ channel in brain neurons. J Neurophysiol 76: 2131-2136.
57. Takeshita Y, Harata N, Akaike N (1996). Suppression of K+ conductance by metabotropic glutamate receptor in acutely dissociated large cholinergic neurons of rat caudate putamen. J Neurophysiol 76: 1545-1558.
58. Tkatch T, Baranauskas G, Surmeier DJ (1998). Basal forebrain neurons adjacent to the globus pallidus co-express GABAergic and cholinergic marker mRNAs. Neuroreport 9: 1935-1939.
59. Vizuete ML, Venero JL, Traiffort E, Vargas C, Machado A, Cano J (1997). Expression of 5-HT7 receptor mRNA in rat brain during postnatal development. Neurocsi Lett 227: 53-56.
60. Waeber C, Sebben M, Nieoullon A, Bockaert J, Dumuis A (1994). Regional distribution and ontogeny of 5-HT4 binding sites in rodent brain. Neuropharm 33: 527-541.
61. Ward RP, Dorsa DM (1996). Colocalization of serotonin receptor subtypes 5-HT2A, 5-HT2C, and 5-HT6 with neuropeptides in rat striatum. J Comp Neurol 370: 405-414.
62. Warren NM, Piggott MA, Perry EK, Burn DJ (2005). Cholinergic systems in progressive supranuclear palsy. Brain 128: 239-249.
63. Wilson CJ (2005). The mechanisms of intrinsic amplification of hyperpolarizations and spontaneous bursting in striatal cholinergic interneurons. Neuron 45: 575-585.
64. Xiang Z, Wang L, Kitai ST (2005). Modulation of spontaneous firing in rat subthalamic neurons by 5-HT reeptor subtypes. J Neurophysiol 93: 1145-1157.
65. Yakel JL, Trussell LO, Jackson MB (1988). Three serotonin responses in cultured mouse hippocampal and striatal neurons. Neuroscience 8: 1273-1285.
66. Yan Z, Surmeier DJ (1997). D5 dopamine receptors enhance Zn2+-sensitive GABA(A) currents in striatal cholinergic interneurons through a PKA/PP1 cascade. Neuron 19: 1115-1126.
67. Yan Z, Song WJ, Surmeier J (1997). D2 dopamine receptors reduce N-type Ca2+ currents in rat neostriatal cholinergic interneurons through a membrane-delimited, protein-kinase-C-insensitive pathway. J Neurophysiol 77: 1003-1015.
68. Zhang ZW (2003). Serotonin induces tonic firing in layer V pyramidal neurons of rat prefrontal cortex during postnatal development. J Neurosci 23: 3373-3384.