Modulation of the activity of pyramidal neurons in rat prefrontal cortex by raphe stimulation in vivo: Involvement of serotonin and GABA

Cerebral Cortex

Volumn 15, Issue 1, 2005, Pages 1-14

  Puig, M Victoria ^a   Artigas, Francesc ^a,b   Celada, Pau ^a  

^a INSTITUT D INVESTIGACIONS BIOMÈDIQUES AUGUST PI I SUNYER IDIBAPS   (Spain)

^b INST D INVESTIGACIONS B   (Spain)

Author keywords

5 HT1A receptors; 5 HT2A receptors; Dorsal raphe; Medial prefrontal cortex; Median raphe

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID RECEPTOR BLOCKING AGENT; N [2 [4 (2 METHOXYPHENYL) 1 PIPERAZINYL]ETHYL] N (2 PYRIDYL)CYCLOHEXANECARBOXAMIDE; PICROTOXIN; SEROTONIN; SEROTONIN ANTAGONIST;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN FUNCTION; CELL ACTIVITY; CONTROLLED STUDY; DORSAL RAPHE NUCLEUS; ELECTROSTIMULATION; EXCITATION; GABAERGIC TRANSMISSION; IN VIVO STUDY; LATENT PERIOD; MAJOR DEPRESSION; MALE; MEDIAN RAPHE NUCLEUS; MOTOR CORTEX; NONHUMAN; PREFRONTAL CORTEX; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SCHIZOPHRENIA; SEROTONINERGIC TRANSMISSION;

ANIMALS; ELECTRIC STIMULATION; EVOKED POTENTIALS; GAMMA-AMINOBUTYRIC ACID; MALE; MOTOR CORTEX; NEURAL INHIBITION; NEURAL PATHWAYS; PIPERAZINES; PREFRONTAL CORTEX; PYRAMIDAL CELLS; PYRIDINES; RAPHE NUCLEI; RATS; RATS, WISTAR; SEROTONIN; SEROTONIN ANTAGONISTS;

EID: 10944240456     PISSN: 10473211     EISSN: None     Source Type: Journal    
DOI: 10.1093/cercor/bhh104     Document Type: Article

References (93)

1. Aghajanian GK, Marek GJ (1997) Serotonin induces excitatory post-synaptic potentials in apical dendrites of neocortical pyramidal cells. Neuropharmacology 36:589-599.
2. Aghajanian GK, Marek GJ (1999) Serotonin-glutamate interactions: a new target for antipsychotic drugs. Neuropsychopharmacology 21:S122-S133.
3. Aghajanian GK, Wang RY (1977) Habenular and other midbrain raphe afferents demonstrated by a modified retrograde tracing technique. Brain Res 122:229-242.
4. 2a receptors in pyramidal neurons of prefrontal cortex. Cereb Cortex 14:281-299.
5. Araneda R, Andrade R (1991) 5-Hydroxytryptamine-2 and 5-hydroxy-tryptamine-1A receptors mediate opposing responses on membrane excitability in rat association cortex. Neuroscience 40:399-412.
6. Arango V, Underwood MD, Mann JJ (2002) Serotonin brain circuits involved in major depression and suicide. Prog Brain Res 136:443-453.
7. 2A/2C receptor agonist DOB on NMDA-evoked responses in the rat medial prefrontal cortex. Eur J Neurosci 11:2917-2934.
8. 3 receptors in the medial prefrontal cortex: a microiontophoretic study. Eur J Pharmacol 173:193-196.
9. Ashby CR, Jiang LH, Kasser RJ, Wang RY (1990) Electrophysiological characterization of 5-hydroxytryptamine-2 receptors in the rat medial prefrontal cortex. J Pharmacol Exp Ther 252:171-178.
10. Ashby CR, Edwards E, Wang RY (1994) Electrophysiological evidence for a functional interaction between 5-HT(1A) and 5-HT(2A) receptors in the rat medial prefrontal cortex: an iontophoretic study. Synapse 17:173-181.
11. Azmitia EC, Segal M (1978) An autoradiographic analysis of the differential ascending projections of the dorsal and median raphe nuclei in the rat. J Comp Neurol 179:641-668.
12. 1A receptor in primate brain neurons and glial cells. Neuropsychopharmacology 14:35-46.
13. 2 receptors and serotonergic axons in rat neocortex. Brain Res 453:315-328.
14. Carr DB, Sesack SR (2000) GABA-containing neurons in the rat ventral tegmental area project to the prefrontal cortex. Synapse 38:114-123
15. Ceci A, Baschirotto A, Borsini F (1993) Effect of fluoxetine on the spontaneous electrical activity of fronto-cortical neurons. Eur J Pharmacol 250:461-464.
16. Celada P, Puig MV, Casanovas JM, Guillazo G, Artigas F (2001) Control of dorsal raphe serotonergic neurons by the medial prefrontal cortex: Involvement of serotonin-1A GABA(A) and glutamate receptors. J Neurosci 21:9917-9929.
17. 2A receptor in the central nervous system of adult rat. J Comp Neurol 409:187-209.
18. 1A receptors at the axon initial segment of prefrontal pyramidal neurons in schizophrenia. Am J Psychiatry 161:739-742.
19. 1A receptors might control the output of cortical glutamatergic neurons in rat cingulate cortex. Brain Res 989:42-51.
20. De Felipe J, Arellano JI, Gomez A, Azmitia EC, Muñoz A (2001) Pyramidal cell axons show a local specialization for GABA and 5-HT inputs in monkey and human cerebral cortex. J Comp Neurol 433:148-155.
21. Dégenètais E, Thierry AM, Glowinski J, Gioanni Y (2002) Electrophysiological properties of pyramidal neurons in the rat prefrontal cortex: an in vivo intracellular recording study. Cereb Cortex 12:1-16.
22. 2A receptor affects human memory. Nat Neurosci 6:1141-1142.
23. De Vry J (1995) 5-HT1A receptor agonists: recent developments and controversial issues. Psychopharmacology 121:1-26.
24. 3 receptors mediate serotonergic fast synaptic excitation of neocortical vasoactive intestinal peptide/cholecystokinin interneurons. J Neurosci 22:7389-7397.
25. Fuller JH, Schlag JD (1976) Determination of antidromic excitation by the collision test: problems of interpretation. Brain Res 112:283-298.
26. Fuster JM (2001) The prefrontal cortex-an update: time is of the essence. Neuron 30:319-333.
27. Gartside SE, Hajos-Korcsok E, Bagdy E, Harsing LG Jr, Sharp T, Hajós M (2000) Neurochemical and electrophysiological studies on the functional significance of burst firing in serotonergic neurons. Neuroscience 98:295-300.
28. Goldman-Rakic PS (1996) Regional and cellular fractionation of working memory. Proc Natl Acad Sci USA 93:13473-13480.
29. Glowinski J, Tassin JP, Thierry AM (1984) The mesocortico-prefrontal dopaminergic neurons. Trends Neurosci 7:415-418.
30. Gras C, Herzog E, Bellenchi GC, Bernard V, Ravassard P, Pohl M, Gasnier B, Giros B, El Mestikawy S (2002) A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J Neurosci 22:5442-5451.
31. Groenewegen HJ, Uylings HB (2000) The prefrontal cortex and the integration of sensory limbic and autonomic information. Prog Brain Res 126:3-28.
32. Hajós M, Richards CD, Szekely AD, Sharp T (1998) An electrophysiological and neuroanatomical study of the medial prefrontal cortical projection to the midbrain raphe nuclei in the rat. Neuroscience 87:95-108.
33. Hajós M, Hoffmann WE, Tetko IV, Hyland B, Sharp T, Villa AE (2001) Different tonic regulation of neuronal activity in the rat dorsal raphe and medial prefrontal cortex via 5-HT(1A) receptors. Neurosci Lett 304:29-32.
34. 1A receptors. Neuropharmacology 45:72-81.
35. Hall H, Farde L, Halldin C, Lundkvist C, Sedvall G (2000) Autoradiographic localization of 5-HT(2A) receptors in the human brain using [3H]M100907 and [11C]M100907. Synapse 38:421-431.
36. 1A antagonist WAY 100 635 alleviates cognitive impairments induced by dizocilpine (MK-801) in monkeys. Neuropharmacology 39:547-552.
37. Herzog E, Gilchrist J, Gras C, Muzerelle A, Ravassard P, Giros B, Gaspar P, El Mestikawy S (2004) Localization of VGLUT3, the vesicular glutamate transporter type 3, in the rat brain. Neuroscience 123:983-1002.
38. 3H]8-OH-DPAT (-)[1251]iodocyanopindolol, [3H]mesulergine and [3H]ketanserin. Eur J Pharmacol 118:13-23.
39. Jacobs BL, Azmitia EC (1992) Structure and function of the brain serotonin system. Physiol Rev 72:165-229.
40. Jakab RL, Goldman-Rakic PS (1998) 5-Hydroxytryptamine(2A) serotonin receptors in the primate cerebral cortex: Possible site of action of hallucinogenic and antipsychotic drugs in pyramidal cell apical dendrites. Proc Natl Acad Sci USA 95:735-740.
41. 3 receptors in inhibitory circuits of the primate cerebral cortex. J Comp Neurol 417:337-348.
42. Jankowski MP, Sesack SR (2002) Electron microscopic analysis of the GABA projection from the dorsal raphe nucleus to the prefrontal cortex in the rat. Soc Neurosci Abstr 587.8.
43. Jansson A, Tinner B, Bancila M, Vergé D, Steinbusch HW, Agnati LF, Fuxe K (2001) Relationships of 5-hydroxytryptamine immunoreactive terminal-like varicosities to 5-hydroxytryptamine-2A receptor-immunoreactive neuronal processes in the rat forebrain. J Chem Neuroanat 22:185-203.
44. Johnson MD (1994) Synaptic glutamate release by postnatal rat serotonergic neurons in microculture. Neuron 12:433-442.
45. Kia HK, Miquel MC, Brisorgueil MJ, Daval G, Riad M, Elmestikawy S, Hamon M, Vergé D (1996) Immunocytochemical localization of serotonin(1A) receptors in the rat central nervous system. J Comp Neurol 365:289-305.
46. Kosofsky BE, Molliver ME (1987) The serotoninergic innervation of cerebral cortex: different classes of axon terminals arise from dorsal and median raphe nuclei. Synapse 1:153-168.
47. Kroeze WK, Roth BL (1998) The molecular biology of serotonin receptors: therapeutic implications for the interface of mood and psychosis. Biol Psychiatry 44:1128-1142.
48. Lewis BL, O'Donnell P (2000) Ventral tegmental area afferents to the prefrontal cortex maintain membrane potential 'up' states in pyramidal neurons via D(1) dopamine receptors. Cereb Cortex 10:1168-1175.
49. Li YQ, Li H, Kaneko T, Mizuno N (2001) Morphological features and electrophysiological properties of serotonergic and non-serotonergic projection neurons in the dorsal raphe nucleus. An intracellular recording and labeling study in rat brain slices. Brain Res 900:110-118.
50. 2A receptors by autoradiography with [3H]MDL 100 907. Naunyn Schmied Arch Pharmacol 356:446-454.
51. Mamounas LA, Molliver ME (1988) Evidence for dual serotonergic projections to neocortex: axons from the dorsal and median raphe nuclei are differentially vulnerable to the neurotoxin P-chloroamphetamine (PCA). Exp Neurol 102:23-36.
52. Mantz J, Godbout R, Tassin JP, Glowinski J, Thierry AM (1990) Inhibition of spontaneous and evoked unit activity in the rat medial prefrontal cortex by mesencephalic raphe nuclei. Brain Res 524:22-30.
53. Martin LP, Jackson DM, Wallsten C, Waszczak BL (1999) Electrophysiological comparison of 5-hydroxytryptamine(1A) receptor antagonists on dorsal raphe cell firing. J Pharmacol Exp Ther 288:820-826.
54. Martín-Ruiz R, Puig MV, Celada P, Shapiro DA, Roth BL, Mengod G, Artigas F (2001) Control of serotonergic function in medial prefrontal cortex by serotonin-2A receptors through a glutamate-dependent mechanism. J Neurosci 21:9856-9866.
55. Martinez D, Hwang DR, Mawlawi O, Slifstein M, Kent J, Simpson N, Parsey RV, Hashimoto T, Huang YY, Shinn A, VanHeertum R, Abidargham A, Caltabiano S, Malizia A, Cowley H, Mann JJ, Laruelle M (2001) Differential occupancy of somatodendritic and postsynaptic 5HT(1A) receptors by pindolol: a dose-occupancy study with [C-11]WAY 100635 and position emission tomography in humans. Neuropsychopharmacology 24:209-229.
56. Maurice N, Deniau JM, Glowinski J, Thierry AM (1998) Relationships between the prefrontal cortex and the basal ganglia in the rat: physiology of the corticosubthalamic circuits. J Neurosci 18:9539-946.
57. McCormick DA, Wang Z, Huguenard J (1993) Neurotransmitter control of neocortical neuronal activity and excitability. Cereb Cortex 3:387-398.
58. 1A) receptor in the agranular insular cortex in the consolidation of memory for inhibitory avoidance in rats. Behav Pharmacol 12:349-353.
59. Meltzer HY (1999) The role of serotonin in antipsychotic drug action. Neuropsychopharmacology 21:S106-S115.
60. Miner LA, Backstrom JR, Sanders-Bush E, Sesack SR (2003) Ultrastructural localization of serotonin(2A) receptors in the middle layers of the rat prelimbic prefrontal cortex. Neuroscience 116:107-117.
61. 1A antagonists WAY 100635 and NAD-299 attenuate the impairment of passive avoidance caused by scopolamine in the rat. Neuropsychopharmacology 28:253-264.
62. 3 receptor is present in different subpopulations of GABAergic neurons in the rat telencephalon. J Neurosci 17:3157-3167.
63. Newberry NR, Footitt DR, Papanastassiou V, Reynolds DJ (1999) Actions of 5-HT on human neocortical neurones in vitro. Brain Res 833:93-100.
64. O'Donnell P (2003) Dopamine gating of forebrain neural ensembles. Eur J Neurosci 17:429-435.
65. O'Hearn E, Molliver ME (1984) Organization of raphe-cortical projections in rat: a quantitative retrograde study. Brain Res Bull 13:709-726.
66. O'Hearn E, Battaglia G, De Souza EB, Kuhar MJ, Molliver ME (1988) Methylenedioxyamphetamine (MDA) and methylenedioxymethamphetamine (MDMA) cause selective ablation of serotonergic axon terminals in forebrain: immunocytochemical evidence for neurotoxicity. J Neurosci 8:2788-2803.
67. Paladini CA, Celada P, Tepper JM (1999) Striatal, pallidal, and pars reticulata evoked inhibition of nigrostriatal dopaminergic neurons is mediated by GABA(A) receptors in vivo. Neuroscience 89:799-812.
68. Paxinos G, Watson C (1998) The rat brain in stereotaxic coordinates, 4th edn. Sydney: Academic Press.
69. 3H]spiroperidol. Mol Pharmacol 16:687-699.
70. Peyron C, Petit JM, Rampon C, Jouvet M, Luppi PH (1998) Forebrain afferents to the rat dorsal raphe nucleus demonstrated by retrograde and anterograde tracing methods. Neuroscience 82:443-468.
71. Pirot S, Jay TM, Glowinski J, Thierry AM (1994) Anatomical and electrophysiological evidence for an excitatory amino acid pathway from the thalamic mediodorsal nucleus to the prefrontal cortex in the rat. Eur J Neurosci 6:1225-1234.
72. 1A receptor in the rat brain: correlation with receptor binding. J Neurosci 12:440-453.
73. 2C receptors. Mol Brain Res 23:163-178.
74. 2A receptors. Relationship to thalamocortical afferents. Cereb Cortex 13:1870-1882.
75. 3 receptors. Cereb Cortex (in press).
76. 1B serotonin receptors in adult rat brain. J Comp Neurol 417:181-194.
77. Robbins TW (2000) From arousal to cognition: the integrative position of the prefrontal cortex. Prog Brain Res 126:469-483.
78. 2A receptors in pyramidal and GABAergic neurons of the rat prefrontal cortex. Cereb Cortex (in press).
79. Sesack SR, Deutch AY, Roth RH, Bunney BS (1989) Topographical organization of the efferent projections of the medial prefrontal cortex in the rat: an anterograde tract-tracing study with Phaseolus vulgaris leucoagglutinin. J Comp Neurol 290:213-242.
80. Somogyi P, Tanás G, Lujan R, Buhl EH (1998) Salient features of the synaptic organization in the cerebral cortex. Brain Res Rev 26:113-135.
81. Swanson LW (1998) Brain maps: structure of the rat brain. Amsterdam: Elsevier.
82. Takagishi M, Chiba T (1991) Efferent projections of the infralimbic (area 25) region of the medial prefrontal cortex in the rat: an anterograde tracer PHA-L study. Brain Res 566:26-39.
83. 2A receptor occupancy in M100907-treated schizophrenic patients. Psychopharmacology 148:400-443.
84. Tanaka E, North RA (1993) Actions of 5 hydroxytryptamine on neurons of the rat cingulate cortex. J Neurophysiol 69:1749-1757.
85. Trantham H, Szumlinski KK, McFarland K, Kalivas PW, Lavin A (2002) Repeated cocaine administration alters the electrophysiological properties of prefrontal cortical neurons. Neuroscience 113:749-753.
86. Tzschentke TM (2001) Pharmacology and behavioral pharmacology of the mesocortical dopamine system. Prog Neurobiol 63:241-320.
87. Vertes RP (2004) Differential projections of the infralimbic and prelimbic cortex in the rat. Synapse 51:32-58.
88. Wang M, Vijayraghavan S, Goldman-Rakic PS (2003) Selective D2 receptor actions on working memory circuitry. Program no. 835.9. 2002 abstract viewer/intinerary planner. Washington, DC: Society for Neuroscience.
89. 1 receptors in prefrontal cortex. Nature 376:572-575.
90. 2A receptors in working memory. J Neurosci 22:2843-2854.
91. Yang CR, Seamans JK (1996) Dopamine D1 receptor actions in layers V-VI rat prefrontal cortex neurons in vitro: modulation of dendiritcsomatic signal integration. J Neurosci 16:1922-1935.
92. Yang CR, Seamans JK, Gorelova N (1996) Electrophysiological and morphological properties of layers V-VI principal pyramidal cells in rat prefrontal cortex in vitro. J Neurosci 16:1904-1921.
93. Zhou FM and Hablitz JJ (1999) Activation of serotonin receptors modulates synaptic transmission in rat cerebral cortex. J Neurophysiol 82:2989-2999.