Distribution of neurones expressing inwardly rectifying and Ca2+-permeable AMPA receptors in rat hippocampal slices

1. Current-voltage (I-V) relationships and Ca2+ permeability of receptor channels activated by bath application of kainate, a non-desensitizing agonist of alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptors, were examined in various types of neurones in hippocampal slices of 5- to 13-day-old rats by using the tight-seal patch clamp recording technique. 2. Three types of responses were observed: type I response with outwardly rectifying I-V relationship, type II response with I-V relationship of marked inward rectification, and intermediate response with I-V relationship of weaker inward rectification. Neurones with type I, type II and intermediate I-V relationships of kainate responses were referred to as type I, type II and intermediate neurones, respectively. 3. Permeability of Ca2+ ions was estimated by the reversal potential of kainate response in the outside-out patch in Na+-free extracellular solution containing 100 mM Ca2+. The reversal potentials were -44.4 +/- 14.0 mV (mean +/- s.D) for type I (n = 7), +11.8 +/- 3.6 mV for type II (n = 5), and -8.7 +/- 7.4 mV for the intermediate neurones (n = 7). The values of P-Ca/P-Cs, the ratios of the permeability coefficients of Ca2+ and Cs+, estimated according to the constant-field equation were 0.08 for type I, 1.71 for type II, and 0.50 for the intermediate neurones. 4. Type II and intermediate responses were observed mainly in non-pyramidal neurones in various areas of the hippocampus, most frequently observed in the stratum moleculare of the dentate gyrus and in the stratum radiatum and the stratum lacunosum-moleculare of both the CA1 and CA3 regions. Both type II and intermediate neurones stained with biocytin had round- or ellipsoidal-shaped somata and issued divergent axonal projections to the surrounding structures. 5. Excitatory postsynaptic currents (EPSCs) recorded in type II neurones had 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX)-sensitive fast and D-2-amino-5-phosphonovalerate (APV)-sensitive slow components. The I-V relationship of the fast component showed a strong inward rectification, indicating that inwardly rectifying AMPA receptors are involved in excitatory synaptic transmission.