The GABAergic projection of the dentate gyrus to hippocampal area CA3 of the rat: Pre- and postsynaptic actions after seizures

Journal of Physiology

Volumn 567, Issue 3, 2005, Pages 939-949

  Treviño, Mario ^a   Gutiérrez, Rafael ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

Author keywords

[No Author keywords available]

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR; BICUCULLINE; METABOTROPIC RECEPTOR; METABOTROPIC RECEPTOR ANTAGONIST; GLUTAMATE RECEPTOR ANTAGONIST;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN SLICE; CONTROLLED STUDY; DENDRITE; DENTATE GYRUS; EXCITATORY POSTSYNAPTIC POTENTIAL; FACILITATION; GABAERGIC TRANSMISSION; HIPPOCAMPUS; IN VITRO STUDY; IN VIVO STUDY; INHIBITORY POSTSYNAPTIC POTENTIAL; NERVOUS SYSTEM ELECTROPHYSIOLOGY; NONHUMAN; PRESYNAPTIC POTENTIAL; PRIORITY JOURNAL; RAT; SEIZURE; STATISTICAL ANALYSIS; STATISTICAL SIGNIFICANCE; SYNAPTIC INHIBITION; ADULT; ANTIDROMIC STIMULATION; COLLATERAL CIRCULATION; CURRENT DENSITY; DEFAULT MODE NETWORK; EVOKED SOMATOSENSORY RESPONSE; HIPPOCAMPAL CA3 REGION; LONG TERM POTENTIATION; MATHEMATICAL ANALYSIS; NERVE CELL MEMBRANE CONDUCTANCE; NERVE STIMULATION; PATHOGENESIS; POSTSYNAPTIC POTENTIAL; PRESYNAPTIC NERVE; RECEPTOR POTENTIAL; STRATUM LUCIDUM; STRATUM PYRAMIDALE;

ANIMALS; DENTATE GYRUS; EXCITATORY AMINO ACID ANTAGONISTS; GAMMA-AMINOBUTYRIC ACID; HIPPOCAMPUS; MOSSY FIBERS, HIPPOCAMPAL; RATS; RATS, WISTAR; RECEPTORS, GABA-A; RECEPTORS, GLUTAMATE; SEIZURES; SYNAPTIC TRANSMISSION;

EID: 25844441600     PISSN: 00223751     EISSN: None     Source Type: Journal    
DOI: 10.1113/jphysiol.2005.092064     Document Type: Article

References (45)

1. Acsády L, Kamondi A, Sik A, Freund T & Buzsáki G (1998). GABAergic cells are the major postsynaptic targets of mossy fibres in the hippocampus. J Neurosci 18, 3386-3403.
2. Amaral DG & Witter MP (1989). The three-dimensional organization of the hippocampal formation: a review of anatomical data. Neuroscience 31, 571-591.
3. Aradi I, Santhakumar V, Chen K & Soltesz I (2002). Postsynaptic effects of GABAergic synaptic diversity: Regulation of neuronal excitability by changes in IPSC variance. Neuropharmacology 43, 511-522.
4. Aradi I & Soltesz I (2002). Modulation of network behaviour by changes in variance in interneuronal properties. J Physiol 538, 227-251.
5. A receptors at hippocampal mossy fibre synapses. Eur J Neurosci 18, 931-941.
6. Cohen I, Navarro V, Clemenceau S, Baulac M & Miles R (2002). On the origin of interictal activity in human temporal lobe epilepsy in vitro. Science 298, 1418-1421.
7. Crawford IL & Connor JD (1973). Localization and release of glutamic acid in relation to the hippocampal mossy fibre pathway. Nature 244, 442-443.
8. Freeman JA & Nicholson C (1975). Experimental optimization of current source-density technique for anuran cerebellum. J Neurophysiol 38, 369-382.
9. Gómez-Lira G, Trillo E, Ramírez M, Asai M, Sitges M & Gutiérrez R (2002). Expression of GABAergic transmission in the mossy fibre synapse coincides with the seizure-induced expression of GABA in mossy fibre synaptosomes. Exp Neurol 177, 276-283.
10. Gutiérrez R (2000). Seizures induce simultaneous GABAergic and glutamatergic neurotransmission in the dentate gyrus-CA3 system. J Neurophysiol 84, 3088-3090.
11. Gutiérrez R (2002). Activity-dependent expression of simultaneous glutamatergic and GABAergic neurotransmission from the mossy fibres in vitro. J Neurophysiol 87, 2562-2570.
12. Gutiérrez R (2003). The GABAergic phenotype of the 'glutamatergic' granule cells of the dentate gyrus. Prog Neurobiol 71, 337-358.
13. Gutiérrez R (2005). The dual glutamatergic-GABAergic phenotype of the hippocampal granule cells. Trends Neurosci 28, 297-303.
14. Gutiérrez R & Heinemann U (2001). Kindling induces transient fast inhibition in the dentate gyrus - CA3 projection. Eur J Neurosci 13, 1371-1379.
15. Gutiérrez R, Romo-Parra R, Maqueda J, Vivar C, Ramírez M, Morales MA & Lamas M (2003). Plasticity of the GABAergic phenotype of the 'glutamatergic' granule cells of the rat dentate gyrus. J Neurosci 23, 5594-5598.
16. Henze DA, Urban NN & Barrionuevo G (1997). Origin of the apparent asynchronous activity of hippocampal mossy fibres. J Neurophysiol 78, 24-30.
17. Kasyanov AM, Safiulina VF, Voronin LL & Cherubini E (2004). GABA-mediated giant depolarizing potentials as coincidence detectors for enhancing synaptic efficacy in the developing hippocampus. Proc Natl Acad Sci U S A 101, 3967-3972.
18. Kwan HC & Murphy JT (1974). Extracellular current density analysis of responses in cerebellar cortex to mossy fiber activation. J Neurophysiol 37, 947-953.
19. Lamas M, Gómez-Lira G & Gutiérrez R (2001). Vesicular GABA transporter mRNA expression in the dentate gyrus and in mossy fibre synaptosomes. Mol Brain Res 93, 209-214.
20. Lanthorn TH, Ganong AH & Cotman CW (1984). 2-Amino-4-phosphonobutyrate selectively blocks mossy fibre-CA3 responses in guinea pig but not rat hippocampal neurons. Brain Res 290, 174-178.
21. Lehmann H, Ebert U & Löscher W (1996). Immunocytochemical localization of GABA immunoreactivity in dentate granule cells of normal and kindled rats. Neurosci Lett 212, 41-44.
22. A and NMDA receptors in the neonatal hippocampus. Neuron 18, 243-255.
23. Lie AA, Becker A, Behle K, Beck H, Malitschek B, Conn PJ, Kuhn R, Nitsch R, Plaschke M, Schramm J, Elger CE, Wiestler OD & Blumcke I (2000). Up-regulation of the metabotropic glutamate receptor mGluR4 in hippocampal neurons with reduced seizure vulnerability. Ann Neurol 47, 26-35.
24. Manzoni O, Castillo PE & Nicoll RA (1995). Pharmacology of metabotropic glutamate receptors at the mossy fibre synapses of the guinea pig hippocampus. Neuropharmacology 34, 965-971.
25. 65, is constitutively expressed during development and transiently overexpressed by activity in the granule cells of the rat. Neurosci Lett 353, 69-71.
26. Min MY, Rusakov DA & Kullmann DM (1998). Activation of AMPA, kainate, and metabotropic receptors at hippocampal mossy fibre synapses: role of glutamate diffusion. Neuron 21, 561-570.
27. Mitzdorf U (1985). Current source-density method and application in cat cerebral cortex: investigation of evoked potentials and EEG phenomena. Physiol Rev 65, 30-100.
28. Ohishi H, Akazawa C, Shigemoto R, Nakanishi S & Mizuno N (1995). Distributions of the mRNAs for L-2-amino-4-phosphonobutyrate-sensitive metabotropic glutamate receptors, mGluR4 and mGluR7, in the rat brain. J Comp Neurol 360, 555-570.
29. Ohishi H, Shigemoto R, Nakanishi S & Mizuno N (1993). Distribution of the mRNA for a metabotropic glutamate receptor (mGluR3) in the rat brain: an in situ hybridization study. J Comp Neurol 335, 252-266.
30. 67 in the granule cells of the rat hippocampus. Brain Res 917, 139-146.
31. Regehr WG, Delaney KR & Tank DW (1994). The role of presynaptic calcium in short-term enhancement at the hippocampal mossy fiber synapse. J Neurosci 14, 523-537.
32. Rivera C, Voipio J, Thomas-Crusells J, Li H, Emri Z, Spila S, Payne JA, Minichiello L, Saarma M & Kaila K. (2004). Mechanism of activity-dependent downregulation of the neuron-specific K-Cl contransporter KCC2. J Neurosci 24, 4683-4691.
33. Romo-Parra R, Vivar C, Maqueda J, Morales MA & Gutiérrez R (2003). Activity-dependent induction of multitransmitter signaling onto pyramidal cells and interneurons of area CA3 of the rat hippocampus. J Neurophysiol 89, 3155-3167.
34. A receptors at hippocampal mossy fibres. Neuron 39, 961-973.
35. Salin PA, Scanziani M, Malenka RC & Nicoll RA (1996). Distinct short-term plasticity at two excitatory synapses in the hippocampus. Proc Natl Acad Sci U S A 93, 13304-13309.
36. Sandler R & Smith AD (1991). Coexistence of GABA and glutamate in mossy fibre terminals of the primate hippocampus: an ultrastructural study. J Comp Neurol 303, 177-192.
37. Schmitz D, Mellor J, Frerking M & Nicoll RA (2001). Presynaptic kainate receptors at hippocampal mossy fibre synapses. Proc Natl Acad Sci U S A 98, 11003-11008.
38. Schwarzer C & Sperk G (1995). Hippocampal granule cells express glutamic acid decarboxylase-67 after limbic seizures in the rat. Neuroscience 69, 705-709.
39. Shigemoto R, Kinoshita A, Wada E, Nomura S, Ohishi H, Takada M, Flor PJ, Neki A, Abe T, Nakanishi S & Mizuno N (1997). Differential presynaptic localization of metabotropic glutamate receptor subtypes in the rat hippocampus. J Neurosci 17, 7503-7522.
40. Shigemoto R, Kulik A, Roberts JD, Ohishi H, Nusser Z, Kaneko T & Somogyi P (1996). Target-cell-specific concentration of a metabotropic glutamate receptor in the presynaptic active zone. Nature 381, 523-525
41. Sloviter RS, Dichter MA, Rachinsky TL, Dean E, Goodman JH, Sollas AL & Martin DL (1996). Basal expression and induction of glutamate decarboxylase and GABA in excitatory granule cells of the rat and monkey hippocampal dentate gyrus. J Comp Neurol 373, 593-618.
42. Tong G, Malenka RC & Nicoll RA (1996). Long-term potentiation in cultures of single hippocampal granule cells: a presynaptic form of plasticity. Neuron 16, 1147-1157.
43. Vogt KE & Nicoll RA (1999). Glutamate and γ-aminobutyric acid mediate a heterosynaptic depression at mossy fibre synapses in the hippocampus. Proc Natl Acad Sci U S A 96, 1118-1122.
44. Vogt KE & Regehr WG (2001). Cholinergic modulation of excitatory synaptic transmission in the CA3 area of the hippocampus. J Neurosci 21, 75-83.
45. Walker MC, Ruiz A & Kullmann DM (2001). Monosynaptic GABAergic signaling from dentate to CA3 with a pharmacological and physiological profile typical of mossy fibre synapses. Neuron 29, 703-715.