Plasticity of the GABAergic phenotype of the "glutamatergic" granule cells of the rat dentate gyrus

Journal of Neuroscience

Volumn 23, Issue 13, 2003, Pages 5594-5598

  Gutiérrez, Rafael ^a   Romo Parra, Héctor ^a   Maqueda, Jasmín ^a   Vivar, Carmen ^a   Ramírez, Mónica ^a   Morales, Miguel A ^b   Lamas, Mónica ^a  

^a DEPARTAMENTO DE FÍSICA   (Mexico)

^b UNIVERSIDAD NACIONAL AUTÓNOMA DE MÉXICO   (Mexico)

Author keywords

CA3; Dentate gyrus; Development; GABA; Glutamate; Granule cells; Mossy fibers; Plasticity

Indexed keywords

4 AMINOBUTYRIC ACID; CARRIER PROTEIN; GLUTAMATE DECARBOXYLASE; GLUTAMATE RECEPTOR ANTAGONIST; MESSENGER RNA; METABOTROPIC RECEPTOR;

ADOLESCENT; ANIMAL TISSUE; ARTICLE; CELL ACTIVATION; CONTROLLED STUDY; DENTATE GYRUS; DOWN REGULATION; ELECTROPHYSIOLOGY; GABAERGIC SYSTEM; GRANULE CELL; HIPPOCAMPUS; IMMUNOHISTOLOGY; INTERNEURON; MOSSY FIBER; NERVE CELL PLASTICITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PYRAMIDAL NERVE CELL; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SYNAPTIC TRANSMISSION;

EID: 1642377843     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.23-13-05594.2003     Document Type: Article

References (36)

1. Altman J, Bayer SA (1990) Migration and distribution of two populations of hippocampal granule cell precursors during the perinatal and postnatal periods. J Comp Neurol 301:365-381.
2. Amaral DG, Dent JA (1981) Development of the mossy fibers of the dentate gyrus. I. A light and electron microscopic study of the mossy fibers and their expansions. J Comp Neurol 195:51-86.
3. Bayer SA (1980) Development of the hippocampal region in the rat. II. Morphogenesis during embryonic and early postnatal life. J Comp Neurol 190:115-134.
4. Ben-Ari Y (2001) Developing networks play a similar melody. Trends Neurosci 24:353-360.
5. Ben-Ari Y, Cherubini E, Corradetti R, Gaiarsa JL (1989) Giant synaptic potentials in immature rat CA3 hippocampal neurones. J Physiol (Lond) 416:303-325.
6. Ben-Ari Y, Tseeb V, Raggozzino D, Khazipov R, Gaiarsa JL (1994) gamma-Aminobutyric acid (GABA): a fast excitatory transmitter which may regulate the development of hippocampal neurones in early postnatal life. Prog Brain Res 102:261-273.
7. Ben-Ari Y, Khazipov R, Leinekugel X, Caillard O, Gaiarsa JL (1997) GABAA, NMDA and AMPA receptors: a developmentally regulated "ménage a trois." Trends Neurosci 20:523-529.
8. Cao Y, Wilcox KS, Martin CE, Tachinsky TL, Eberwine J, Dichter MA (1996) Presence of mRNA for glutamic acid decarboxylase in both excitatory and inhibitory neurons. Proc Natl Acad Sci USA 93:9844-9849.
9. Dupuy ST, Houser CR (1996) Prominent expression of two forms of glutamate decarboxylase in the embryonic and early postnatal rat hippocampal formation. J Neurosci 16:6919-6932.
10. Dupuy ST, Houser CR (1997) Developmental changes in GABA neurons of the rat dentate gyrus: an in situ hybridization and birthdating study. J Comp Neurol 389:402-418.
11. Gaarskjaer FB (1985) The development of the dentate area and the hippocampal mossy fiber projection of the rat. J Comp Neurol 241:154-170.
12. Gaiarsa JL, McLean H, Congar P, Leinekugel X, Khazipov R, Tseeb V, Ben-Ari Y (1995) Postnatal maturation of gamma-aminobutyric acid-A and B-mediated inhibition in the CA3 hippocampal region of the rat. J Neurobiol 26:339-349.
13. Ganguly K, Schinder AF, Wong ST, Poo M (2001) GABA itself promotes the developmental switch of neuronal GABAergic responses from excitation to inhibition. Cell 105:521-532.
14. Gómez-Lira G, Trillo E, Ramírez M, Asai M, Sitges M, Gutiérrez R (2002) Expression of GABAergic transmission in the mossy fiber synapse coincides with the seizure-induced expression of GABA in mossy fiber synaptosomes. Exp Neurol 177:276-283.
15. Gutiérrez R (2000) Seizures induce simultaneous GABAergic and glutamatergic neurotransmission in the dentate gyrus-CA3 system. J Neurophysiol 84:3088-3090.
16. Gutiérrez R (2002) Activity-dependent expression of simultaneous glutamatergic and GABAergic neurotransmission from the mossy fibers in vitro. J Neurophysiol 87:2562-2570.
17. Gutiérrez R, Heinemann U (2001) Kindling induces transient fast inhibition in the dentate gyrus - CA3 projection. Eur J Neurosci 13:1371-1379.
18. Haas KZ, Sperber EF, Opanashuk LA, Stanton PK, Moshe SL (2001) Resistance of immature hippocampus to morphologic and physiologic alterations following status epilepticus or kindling. Hippocampus 11:615-625.
19. Hennou S, Khalilov I, Diabira D, Ben-Ari Y, Gozlan H (2002) Early sequential formation of functional GABAA and glutamatergic synapses on CA1 interneurons of the rat foetal hippocampus. Eur J Neurosci 6:197-208.
20. Henze DA, Card JP, Barrionuevo G, Ben-Ari Y (1997) Large amplitude miniature excitatory postsynaptic currents in hippocampal CA3 pyramidal neurons are of mossy fiber origin. J Neurophysiol 77:1075-1086.
21. Holmes GL, Sarkisian M, Ben-Ari Y, Chevassus-Au-Louis N (1999) Mossy fiber sprouting after recurrent seizures during early development in rats. J Comp Neurol 404:537-553.
22. Lamas M, Gómez-Lira G, Gutiérrez R (2001) Vesicular GABA transporter mRNA expression in the dentate gyrus and in mossy fiber synaptosomes. Mol Brain Res 93:209-214.
23. 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.
24. 2+ oscillations mediated by the synergistic excitatory actions of GABA(A) and NMDA receptors in the neonatal hippocampus. Neuron 18:243-255.
25. McIntire SL, Reimer RJ, Schuske K, Edwards RH, Jorgensen EM (1997) Identification and characterization of the vesicular GABA transporter. Nature 389:870-876.
26. 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.
27. Ramirez M, Gutiérrez R (2001) Activity-dependent expression of GAD67 in the granule cells of the rat hippocampus. Brain Res 917:139-146.
28. Rao A, Cha EM, Craig AM (2000) Mismatched appositions of presynaptic and postsynaptic components in isolated hippocampal neurons. J Neurosci 20:8344-8353.
29. Ribak CE, Navetta MS (1994) An immature mossy fiber innervation of hilar neurons may explain their resistance to kainite-induced cell death in 15-day-old rats. Dev Brain Res 79:47-62.
30. Ribak CE, Seress L (1983) Five types of basket cells in the hippocampal dentate gyrus: a combined Golgi and electron microscopic study. J Neurocytol 12:577-597.
31. Ribak CE, Seress L (1988) The development of GABAergic neurons in the rat hippocampal formation. An immunocytochemical study. Dev Brain Res 44:197-209.
32. Romo-Parra H, Vivar C, Maqueda J, Morales MA, Gutiérrez R (2003) Activity-dependent induction of multitransmitter signaling onto pyramidal cells and interneurons of hippocampal area CA3. J Neurophysiol 89:3155-3167.
33. Sandler R, Smith AD (1991) Coexistence of GABA and glutamate in mossy fiber terminals of the primate hippocampus: an ultrastructural study. J Comp Neurol 303:177-192.
34. Schwarzer C, Sperk G (1995) Hippocampal granule cells express glutamic acid decarboxylase 67 after limbic seizure in the rat. Neuroscience 69:705-709.
35. 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.
36. Walker MC, Ruiz A, Kullmann DM (2001) Monosynaptic GABAergic signaling from dentate to CA3 with a pharmacological and physiological profile typical of mossy fiber synapses. Neuron 29:703-715.