1. Intracellular current-clamp recordings obtained from neurons of the basolateral nucleus of the amygdala (BLA) were used to characterize postsynaptic potentials elicited through stimulation of the stria terminalis (ST) or the lateral amygdala (LA). The contribution of glutamatergic receptor subtypes to excitatory postsynaptic potentials (EPSPs) were analyzed by the use of the non N-methyl-D-aspartate (non-NMDA) antagonist, 6-cyano-7-nitro-quinoxaline-2,3-dione (CNQX), and the NMDA antagonist, (DL)-2-amino-5-phosphonovaleric acid (APV). 2. Basic membrane properties of BLA neurons determined from membrane responses to transient current injection showed that at the mean resting membrane potential (RMP; -67.2 mV) the input resistance (R(N)) and time constant for membrane charging (tau) were near maximal, and that both values were reduced with membrane hyperpolarization, suggesting an intrinsic regulation of synaptic efficacy. 3. Responses to stimulation of the ST or LA consisted of an EPSP followed by either a fast inhibitory postsynaptic potential (f-IPSP) only, or by a fast- and subsequent slow-IPSP (s-IPSP). The EPSP was graded in nature, increasing in amplitude with increased stimulus intensity, and with membrane hyperpolarization after DC current injection. Spontaneous EPSPs were also observed either as discrete events or as EPSP/IPSP waveforms. 4. In physiological Mg2+ concentrations (1.2 mM), at the mean RMP, the EPSP consisted of dual, fast and slow, glutamatergic components. The fast-EPSP (f-EPSP) possessed characteristics of kainate/quisqualate receptor activation, namely, the EPSP increased in amplitude with membrane hyperpolarization, was insensitive to the NMDA receptor antagonist, APV (50-mu-M), and was blocked by the non-NMDA receptor antagonist, CNQX (10-mu-). In contrast, the slow-EPSP (s-EPSP) decreased in amplitude with membrane hyperpolarization, was insensitive to CNQX (10-mu-M), and was blocked by APV (50-mu-M), indicating mediation by NMDA receptor activation. 5. In the presence of CNQX (10-mu-M), ST stimulation evoked an APV-sensitive s-EPSP. In contrast, LA stimulation evoked a f-IPSP, which when blocked by subsequent addition of bicuculline methiodide (BMI; 30-mu-M) revealed a temporally overlapping APV-sensitive s-EPSP. These data suggest that EPSP amplitude and duration are determined, in part, by the shunting of membrane conductance caused by a concomitant IPSP. 6. Superfusion of either CNQX or APV in BLA neurons caused membrane hyperpolarization and blockade of spontaneous EPSPs and IPSPs, suggesting that these compounds may act to block tonic excitatory amino acid (EAA) release within the nucleus, and that a degree of feed-forward inhibition occurs within the nucleus. 7. The presence of action potentials occurring during the hyperpolarizing phase of both spontaneous and evoked f-IPSPs indicated that an EAA synapse might be present at a site remote from the cell soma that is capable of overcoming synaptic inhibition. 8. These experiments provide evidence for the existence of two electrophysiologically distinct EPSPs in the BLA that can contribute to synaptic transmission in physiological Mg2+ concentrations. The degree of expression of these two EPSPs is determined, in part, by a concomitant f-IPSP. Furthermore, a tonic EAA release within the BLA may contribute to the RMP of BLA neurons, and an EPSP that is generated in a region remote from the soma is capable of initiating action potential generation in the presence of strong inhibitory potentials. This would suggest that the BLA nucleus is exquisitely sensitive to alterations in excitatory/inhibitory drive and may account for the susceptibility of the nucleus to epileptogenesis.
