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J Neurophysiol 81: 2095-2102, 1999;
0022-3077/99 $5.00
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The Journal of Neurophysiology Vol. 81 No. 5 May 1999, pp. 2095-2102
Copyright ©1999 by the American Physiological Society

Glutamate Controls the Induction of GABA-Mediated Giant Depolarizing Potentials Through AMPA Receptors in Neonatal Rat Hippocampal Slices

Sonia Bolea,1 Elena Avignone,2 Nicola Berretta,2 Juan V. Sanchez-Andres,1 and Enrico Cherubini2

 1Departamento de Fisiologia, Instituto de Bioingenieria, Universidad Miguel Hernandez, Campus de San Juan, 03550 San Juan, Alicante, Spain; and  2Neuroscience Program and Istituto Nazionale Fisica della Materia Unit, International School for Advanced Studies, 34014 Trieste, Italy

Bolea, Sonia, Elena Avignone, Nicola Berretta, Juan V. Sanchez-Andres, and Enrico Cherubini. Glutamate Controls the Induction of GABA-Mediated Giant Depolarizing Potentials Through AMPA Receptors in Neonatal Rat Hippocampal Slices. J. Neurophysiol. 81: 2095-2102, 1999.Glutamate controls the induction of GABA-mediated giant depolarizing potentials through AMPA receptors in neonatal rat hippocampal slices. Giant depolarizing potentials (GDPs) are generated by the interplay of the depolarizing action of GABA and glutamate. In this study, single and dual whole cell recordings (in current-clamp configuration) were performed from CA3 pyramidal cells in hippocampal slices obtained from postnatal (P) days P1- to P6-old rats to evaluate the role of ionotropic glutamate receptors in GDP generation. Superfusion of 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) (10-40 µM) completely blocked GDPs. However, in the presence of CNQX, it was still possible to re-induce the appearance of GDPs with GABA (20 µM) or (RS)-alpha -amino-3-hydroxy-5-methyl-4-isoxadepropionate (AMPA) (5 µM). This effect was prevented by the more potent and selective AMPA receptor antagonist GYKI 53655 (50-100 µM). In the presence of GYKI 53655, both kainic or domoic acid (0.1-1 µM) were unable to induce GDPs. In contrast, bath application of D-(-)-2-amino-5-phosphonopentanoic acid (50 µM) or (+)-3-(2carboxy-piperazin-4-yl)-propyl-L-phosphonic acid (20 µM) produced only a 37 ± 9% (SE) and 36 ± 11% reduction in GDPs frequency, respectively. Cyclothiazide, a selective blocker of AMPA receptor desensitization, increased GDP frequency by 76 ± 14%. Experiments were also performed with an intracellular solution containing KF to block GABAA receptor-mediated responses. In these conditions, a glutamatergic component of GDP was revealed. GDPs could still be recorded synchronous with those detected simultaneously with KCl-filled electrodes, although their amplitude was smaller. Similar results were found in pair recordings obtained from minislices containing only a small portion of the CA3 area. These data suggest that GDP generation requires activation of AMPA receptors by local release of glutamate from recurrent collaterals.




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