Serotonin increases GABA release in rat entorhinal cortex by inhibiting interneuron TASK-3 K+ channels

Molecular and Cellular Neuroscience

Volumn 39, Issue 2, 2008, Pages 273-284

  Deng, Pan Yue ^a   Lei, Saobo ^a  

^a UNIVERSITY OF NORTH DAKOTA   (United States)

Author keywords

Channel; G Protein; Inhibition; Receptor; Synapse; Transmission

Indexed keywords

MAGNESIUM; PHOSPHOLIPASE C; POTASSIUM CHANNEL; SEROTONIN; SEROTONIN 2A RECEPTOR;

4 AMINOBUTYRIC ACID RELEASE; ACTION POTENTIAL; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENTORHINAL CORTEX; ENZYME ACTIVITY; EPILEPSY; GABAERGIC TRANSMISSION; INTERNEURON; MEMBRANE DEPOLARIZATION; NERVE CELL; NERVE CELL EXCITABILITY; NONHUMAN; PRIORITY JOURNAL; PYRAMIDAL NERVE CELL; RAT; SEIZURE; STIMULATION;

ACTION POTENTIALS; ANIMALS; ANIMALS, NEWBORN; ANTIBODIES; ARACHIDONIC ACIDS; DOSE-RESPONSE RELATIONSHIP, DRUG; ENTORHINAL CORTEX; ESTRENES; GAMMA-AMINOBUTYRIC ACID; GUANOSINE DIPHOSPHATE; INHIBITORY POSTSYNAPTIC POTENTIALS; INTERNEURONS; MAGNESIUM; NEURAL INHIBITION; PATCH-CLAMP TECHNIQUES; PHOSPHOLIPID ETHERS; PLATELET AGGREGATION INHIBITORS; POTASSIUM CHANNEL BLOCKERS; POTASSIUM CHANNELS, TANDEM PORE DOMAIN; PYRAMIDAL CELLS; PYRROLIDINES; PYRROLIDINONES; RATS; RATS, SPRAGUE-DAWLEY; RUTHENIUM RED; SEROTONIN; SEROTONIN AGENTS; SURAMIN; THIONUCLEOTIDES;

RATTUS;

EID: 52249106221     PISSN: 10447431     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.mcn.2008.07.005     Document Type: Article

References (74)

1. Abi-Saab W.M., Bubser M., Roth R.H., and Deutch A.Y. 5-HT2 receptor regulation of extracellular GABA levels in the prefrontal cortex. Neuropsychopharmacology 20 (1999) 92-96
2. Albert A.P., Spyer K.M., and Brooks P.A. The effect of 5-HT and selective 5-HT receptor agonists and antagonists on rat dorsal vagal preganglionic neurones in vitro. Br. J. Pharmacol. 119 (1996) 519-526
3. Babb T.L. Research on the anatomy and pathology of epileptic tissue. In: Luders H. (Ed). Epilepsy Surgery (1991), Raven, New York 719-727
4. Bayliss D.A., Sirois J.E., and Talley E.M. The TASK family: two-pore domain background K+ channels. Mol. Interv. 3 (2003) 205-219
5. Bennett B.D., Huguenard J.R., and Prince D.A. Adrenergic modulation of GABAA receptor-mediated inhibition in rat sensorimotor cortex. J. Neurophysiol. 79 (1998) 937-946
6. Berg A.P., and Bayliss D.A. Striatal cholinergic interneurons express a receptor-insensitive homomeric TASK-3-like background K+ current. J. Neurophysiol. 97 (2007) 1546-1552
7. Bobillier P., Pettijean F., Salvert D., Ligier M., and Seguin S. Differential projections of the nucleus raphe dorsalis and nucleus raphe centralis as revealed by autoradiography. Brain. Res. 85 (1975) 205-210
8. Braga M.F., Aroniadou-Anderjaska V., Manion S.T., Hough C.J., and Li H. Stress impairs alpha(1A) adrenoceptor-mediated noradrenergic facilitation of GABAergic transmission in the basolateral amygdala. Neuropsychopharmacology 29 (2004) 45-58
9. Browning K.N., and Travagli R.A. Characterization of the in vitro effects of 5-hydroxytryptamine (5-HT) on identified neurones of the rat dorsal motor nucleus of the vagus (DMV). Br. J. Pharmacol. 128 (1999) 1307-1315
10. Burwell R.D. The parahippocampal region: corticocortical connectivity. Ann. N. Y. Acad. Sci. 911 (2000) 25-42
11. Chen X., Talley E.M., Patel N., Gomis A., McIntire W.E., Dong B., Viana F., Garrison J.C., and Bayliss D.A. Inhibition of a background potassium channel by Gq protein alpha-subunits. Proc. Natl. Acad. Sci. USA 103 (2006) 3422-3427
12. Clements J.D., and Bekkers J.M. Detection of spontaneous synaptic events with an optimally scaled template. Biophys. J. 73 (1997) 220-229
13. de Curtis M., and Pare D. The rhinal cortices: a wall of inhibition between the neocortex and the hippocampus. Prog. Neurobiol. 74 (2004) 101-110
14. Deng P.Y., and Lei S. Bidirectional modulation of GABAergic transmission by cholecystokinin in hippocampal dentate gyrus granule cells of juvenile rats. J. Physiol. 572 (2006) 425-442
15. Deng P.Y., and Lei S. Long-term depression in identified stellate neurons of juvenile rat entorhinal cortex. J. Neurophysiol. 97 (2007) 727-737
16. Deng P.Y., Porter J.E., Shin H.S., and Lei S. Thyrotropin-releasing hormone increases GABA release in rat hippocampus. J. Physiol. 577 (2006) 497-511
17. + channels in the entorhinal cortex. Mol. Pharmacol. 72 (2007) 208-218
18. Dolcos F., LaBar K.S., and Cabeza R. Remembering one year later: role of the amygdala and the medial temporal lobe memory system in retrieving emotional memories. Proc. Natl. Acad. Sci. USA 102 (2005) 2626-2631
19. Dolorfo C.L., and Amaral D.G. Entorhinal cortex of the rat: organization of intrinsic connections. J. Comp. Neurol. 398 (1998) 49-82
20. Dolorfo C.L., and Amaral D.G. Entorhinal cortex of the rat: topographic organization of the cells of origin of the perforant path projection to the dentate gyrus. J. Comp. Neurol. 398 (1998) 25-48
21. Du F., Whetsell Jr. W.O., Abou-Khalil B., Blumenkopf B., Lothman E.W., and Schwarcz R. Preferential neuronal loss in layer III of the entorhinal cortex in patients with temporal lobe epilepsy. Epilepsy. Res. 16 (1993) 223-233
22. Feindel W., Leonard G., Caramanos Z., Li M., Harrison J., and Kuchela A. Role of the amygdala and entorhinal cortex in the surgery of temporal lobe seizures. Can. J. Neurol. Sci. 26 (1996) G07
23. Fink M., Duprat F., Lesage F., Reyes R., Romey G., Heurteaux C., and Lazdunski M. Cloning, functional expression and brain localization of a novel unconventional outward rectifier K+ channel. EMBO J. 15 (1996) 6854-6862
24. Fried I. Anatomic temporal lobe resections for temporal lobe epilepsy. Neurosurg. Clin. N. Am. 4 (1993) 233-242
25. Gloor P. Mesial temporal sclerosis: historical background and an overview from a modern perspective. In: Luders H. (Ed). Epilepsy Surgery (1991), Raven, New York 689-703
26. Goldring S., Edwards I., Harding G.W., and Bernardo K.L. Results of anterior temporal lobectomy that spares the amygdala in patients with complex partial seizures. J. Neurosurg. 77 (1992) 185-193
27. Goldring S., Edwards I., Harding G.W., and Bernardo K.L. Temporal lobectomy that spares the amygdala for temporal lobe epilepsy. Neurosurg. Clin. N. Am. 4 (1993) 263-272
28. Grünschlag C.R., Haas H.L., and Stevens D.R. 5-HT inhibits lateral entorhinal cortical neurons of the rat in vitro by activation of potassium channel-coupled 5-HT1A receptors. Brain. Res. 770 (1997) 10-17
29. Han J., Truell J., Gnatenco C., and Kim D. Characterization of four types of background potassium channels in rat cerebellar granule neurons. J. Physiol. 542 (2002) 431-444
30. Hirono M., and Obata K. Alpha-adrenoceptive dual modulation of inhibitory GABAergic inputs to Purkinje cells in the mouse cerebellum. J. Neurophysiol. 95 (2006) 700-708
31. Hopwood S.E., and Trapp S. TASK-like K+ channels mediate effects of 5-HT and extracellular pH in rat dorsal vagal neurones in vitro. J. Physiol. 568 (2005) 145-154
32. Hyman B.T., Van Hoesen G.W., Damasio A.R., and Barnes C.L. Alzheimer's disease: cell-specific pathology isolates the hippocampal formation. Science 225 (1984) 1168-1170
33. Jamali S., Bartolomei F., Robaglia-Schlupp A., Massacrier A., Peragut J.C., Regis J., Dufour H., Ravid R., Roll P., Pereira S., Royer B., Roeckel-Trevisiol N., Fontaine M., Guye M., Boucraut J., Chauvel P., Cau P., and Szepetowski P. Large-scale expression study of human mesial temporal lobe epilepsy: evidence for dysregulation of the neurotransmission and complement systems in the entorhinal cortex. Brain 129 (2006) 625-641
34. Joyal C.C., Laakso M.P., Tiihonen J., Syvalahti E., Vilkman H., Laakso A., Alakare B., Rakkolainen V., Salokangas R.K., Hia J., et al. A volumetric MRI study of the entorhinal cortex in first episode neuroleptic-naive schizophrenia. Biol. Psychiatry. 51 (2002) 1005-1007
35. Kang D., Mariash E., and Kim D. Functional expression of TRESK-2, a new member of the tandem-pore K+ channel family. J. Biol. Chem. 279 (2004) 28063-28070
36. Kilpatrick G.J., Jones B.J., and Tyers M.B. Identification and distribution of 5-HT3 receptors in rat brain using radioligand binding. Nature 330 (1987) 746-748
37. Kim Y., Bang H., and Kim D. TASK-3, a new member of the tandem pore K+ channel family. J. Biol. Chem. 275 (2000) 9340-9347
38. Kindler C.H., Yost C.S., and Gray A.T. Local anesthetic inhibition of baseline potassium channels with two pore domains in tandem. Anesthesiology 90 (1999) 1092-1102
39. Kohler C. Intrinsic connections of the retrohippocampal region in the rat brain. II. The medial entorhinal area. J. Comp. Neurol. 246 (1986) 149-169
40. Kotzbauer P.T., Trojanowsk J.Q., and Lee V.M. Lewy body pathology in Alzheimer's disease. J. Mol. Neurosci. 17 (2001) 225-232
41. Kumar S.S., and Buckmaster P.S. Hyperexcitability, interneurons, and loss of GABAergic synapses in entorhinal cortex in a model of temporal lobe epilepsy. J. Neurosci. 26 (2006) 4613-4623
42. Lei S., Deng P.Y., Porter J.E., and Shin H.S. Adrenergic facilitation of GABAergic transmission in rat entorhinal cortex. J. Neurophysiol. 98 (2007) 2868-2877
43. Lesage F. Pharmacology of neuronal background potassium channels. Neuropharmacology 44 (2003) 1-7
44. Lesage F., Guillemare E., Fink M., Duprat F., Lazdunski M., Romey G., and Barhanin J. TWIK-1, a ubiquitous human weakly inward rectifying K+ channel with a novel structure. EMBO J. 15 (1996) 1004-1011
45. Levesque M.F., Nakasato N., Vinters H.V., and Babb T.L. Surgical treatment of limbic epilepsy associated with extrahippocampal lesions: the problem of dual pathology. J. Neurosurg. 75 (1991) 364-370
46. Liu Z., Otsu Y., Vasuta C., Nawa H., and Murphy T.H. Action-potential-independent GABAergic tone mediated by nicotinic stimulation of immature striatal miniature synaptic transmission. J. Neurophysiol. 98 (2007) 581-593
47. Ma L., Shalinsky M.H., Alonso A., and Dickson C.T. Effects of serotonin on the intrinsic membrane properties of layer II medial entorhinal cortex neurons. Hippocampus 17 (2007) 114-129
48. Madison D.V., and Nicoll R.A. Norepinephrine decreases synaptic inhibition in the rat hippocampus. Brain. Res. 442 (1988) 131-138
49. Majak K., and Pitkanen A. Activation of the amygdalo-entorhinal pathway in fear-conditioning in rat. Eur. J. Neurosci. 18 (2003) 1652-1659
50. Mathie A. Neuronal two-pore-domain potassium channels and their regulation by G protein-coupled receptors. J. Physiol. 578 (2007) 377-385
51. Meenchke H.J., and Veith G. Hippocampal sclerosis in epilepsy. In: Luders H. (Ed). Epilepsy Surgery (1991), Raven, New York 705-715
52. Morales M., Wang S.D., Diaz-Ruiz O., and Jho D.H. Cannabinoid CB1 receptor and serotonin 3 receptor subunit A (5-HT3A) are co-expressed in GABA neurons in the rat telencephalon. J. Comp. Neurol. 468 (2004) 205-216
53. Pazos A., and Palacios J.M. Quantitative autoradiographic mapping of serotonin receptors in the rat brain, I. Serotonin-1 receptors. Brain. Res. 346 (1985) 205-230
54. Pompeiano M., Palacios J.M., and Mengod G. Distribution of the serotonin 5-HT2 receptor family mRNAs: comparison between 5-HT2A and 5-HT2C receptors. Brain. Res. Mol. Brain. Res. 23 (1994) 163-178
55. Prasad K.M., Patel A.R., Muddasani S., Sweeney J., and Keshavan M.S. The entorhinal cortex in first-episode psychotic disorders: a structural magnetic resonance imaging study. Am. J. Psychiatry. 161 (2004) 1612-1619
56. Rutecki P.A., Grossman R.G., Armstrong D., and Irish-Loewen S. Electrophysiological connections between the hippocampus and entorhinal cortex in patients with complex partial seizures. J. Neurosurg. 70 (1989) 667-675
57. + channel, TRESK, is localized in the spinal cord. J. Biol. Chem. 278 (2003) 27406-27412
58. Schmitz D., Empson R.M., Gloveli T., and Heinemann U. Serotonin blocks different patterns of low Mg2+-induced epileptiform activity in rat entorhinal cortex, but not hippocampus. Neuroscience 76 (1997) 449-458
59. Schmitz D., Gloveli T., Empson R.M., Draguhn A., and Heinemann U. Serotonin reduces synaptic excitation in the superficial medial entorhinal cortex of the rat via a presynaptic mechanism. J. Physiol. 508 Pt 1 (1998) 119-129
60. Schmitz D., Gloveli T., Empson R.M., and Heinemann U. Potent depression of stimulus evoked field potential responses in the medial entorhinal cortex by serotonin. Br. J. Pharmacol. 128 (1999) 248-254
61. Shen R.Y., and Andrade R. 5-Hydroxytryptamine2 receptor facilitates GABAergic neurotransmission in rat hippocampus. J. Pharmacol. Exp. Ther. 285 (1998) 805-812
62. Sim L.J., Xiao R., and Childers S.R. In vitro autoradiographic localization of 5-HT1A receptor-activated G-proteins in the rat brain. Brain. Res. Bull. 44 (1997) 39-45
63. Spencer S.S., and Spencer D.D. Entorhinal-hippocampal interactions in medial temporal lobe epilepsy. Epilepsia 35 (1994) 721-727
64. Steffenach H.A., Witter M., Moser M.B., and Moser E.I. Spatial memory in the rat requires the dorsolateral band of the entorhinal cortex. Neuron 45 (2005) 301-313
65. Steward O., and Scoville S.A. Cells of origin of entorhinal cortical afferents to the hippocampus and fascia dentata of the rat. J. Comp. Neurol. 169 (1976) 347-370
66. Swanson T.H. The pathophysiology of human mesial temporal lobe epilepsy. J. Clin. Neurophysiol. 12 (1995) 2-22
67. Tanaka T., Saito H., and Matsuki N. Inhibition of GABAA synaptic responses by brain-derived neurotrophic factor (BDNF) in rat hippocampus. J. Neurosci. 17 (1997) 2959-2966
68. Torborg C.L., Berg A.P., Jeffries B.W., Bayliss D.A., and McBain C.J. TASK-like conductances are present within hippocampal CA1 stratum oriens interneuron subpopulations. J. Neurosci. 26 (2006) 7362-7367
69. van Haeften T., Baks-te-Bulte L., Goede P.H., Wouterlood F.G., and Witter M.P. Morphological and numerical analysis of synaptic interactions between neurons in deep and superficial layers of the entorhinal cortex of the rat. Hippocampus 13 (2003) 943-952
70. Veale E.L., Kennard L.E., Sutton G.L., MacKenzie G., Sandu C., and Mathie A. G(alpha)q-mediated regulation of TASK3 two-pore domain potassium channels: the role of protein kinase C. Mol. Pharmacol. 71 (2007) 1666-1675
71. Witter M.P., Groenewegen H.J., Lopes da Silva F.H., and Lohman A.H. Functional organization of the extrinsic and intrinsic circuitry of the parahippocampal region. Prog. Neurobiol. 33 (1989) 161-253
72. Witter M.P., Naber P.A., van Haeften T., Machielsen W.C., Rombouts S.A., Barkhof F., Scheltens P., and Lopes da Silva F.H. Cortico-hippocampal communication by way of parallel parahippocampal-subicular pathways. Hippocampus 10 (2000) 398-410
73. Woodhall G.L., Bailey S.J., Thompson S.E., Evans D.I., and Jones R.S. Fundamental differences in spontaneous synaptic inhibition between deep and superficial layers of the rat entorhinal cortex. Hippocampus 15 (2005) 232-245
74. Wright D.E., Seroogy K.B., Lundgren K.H., Davis B.M., and Jennes L. Comparative localization of serotonin1A, 1C, and 2 receptor subtype mRNAs in rat brain. J. Comp. Neurol. 351 (1995) 357-373