In olfactory bulb slices from young rats, the field potential evoked in the glomerular layer by stimulation in the olfactory nerve layer consisted of two negative components: an early component (N1) which was blocked by bath application of the kainate/amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid (AMPA) receptor antagonist 6-cyano-7-nitroquinoxaline-2,3-dione (CNQX, 10 microM), and a late, prolonged component (N2; duration > or = 350 msec) which was unaffected by CNQX, was enhanced by reduction of Mg2+ in the medium, and was blocked by the N-methyl-D-aspartate receptor antagonist DL-2-amino-5-phosphonovalerate (50 microM). A comparison of the glomerular field potentials before and after knife cuts that isolated the glomerular layer from the deeper layers of the olfactory bulb indicated that both N1 and N2 were produced by currents generated, for the most part, within the glomeruli. A laminar analysis of the field potential profiles evoked by olfactory nerve stimulation in standard medium, or in the presence of CNQX, showed that N1 and N2 reversed polarity in the external plexiform and mitral cell layers, suggesting that both components reflected synaptic responses in the distal, apical dendrites of mitral/tufted cells. Simultaneous field potential recordings in the glomerular layer and intracellular recordings in the mitral cell layer showed that: (i) N1 is associated with a brief, short-latency spiking activity of mitral cells, and (ii) N2 is associated with prolonged mitral cell spiking, since N2 and the late cell firing had similar time-courses, and both were blocked by bath applied DL-2-amino-5-phosphonovalerate. Application of the GABA(A) receptor antagonist bicuculline methiodide (10 microM) to standard medium selectively enhanced N2. The enhanced N2 was significantly reduced by DL-2-amino-5-phosphonovalerate. Strychnine, an antagonist of glycine receptors, had similar effects to those of bicuculline, but only at high concentrations that have been previously shown to block GABA(A) receptors; at low concentrations strychnine had no effect. The effects of all drugs tested were reversible. In the rat olfactory bulb, activation of the olfactory nerve evokes a kainate/AMPA receptor-mediated response in the distal, apical dendrites of mitral/tufted cells, followed by a slow N-methyl-D-aspartate receptor-mediated response which triggers prolonged discharge of mitral cells. GABA(A) receptor-mediated inhibition appears to suppress, preferentially, this N-methyl-D-aspartate receptor-mediated component. The presence of prolonged N-methyl-D-aspartate receptor-mediated postsynaptic activity at the primary synapses of the olfactory system may play a key role in olfactory processing by facilitating synaptic integration and plasticity.