MECHANISMS OF SELECTIVE LONG-TERM POTENTIATION OF EXCITATORY SYNAPSESIN STRATUM ORIENS ALVEUS INTERNEURONS OF RAT HIPPOCAMPAL SLICES/

1. We investigated long-term potentiation (LTP) of synoptic transmissi on in different populations of interneurons in the CA1 region of rat h ippocampal slices using whole cell recordings. We elicited excitatory postsynaptic currents (EPSCs) in interneurons located in stratum orien s near the alveus (O/A) or in stratum lacunosum-moleculare near the st ratum radiatum border (L-M) by electrical stimulation of nearby axons in stratum oriens and radiatum, respectively. 2. High-frequency stimul ation (100 Hz, 1 s) of axons in con junction with postsynaptic depolar ization (to -20 mV) increased the peak amplitude of test EPSCs elicite d at -80 mV in O/A interneurons. The mean peak amplitude of EPSCs was significantly potentiated relative to the control period at 10 min (39 = 7% increase, mean +/- SE; n = 11 cells) and 30 min (30 +/- 1% incre ase; = 5 cells) after tetanization. Similar stimulation did not produc e potentiation of EPSCs in L-M interneurons (n = 7 cells). 3. This sel ective LTP in O/A interneurons was reversibly blocked by the N-methyl- D-aspartate receptor antagonist (+/-)2 amino-5-phosphonopentanoic acid (AP-5). Tetanization in the presence of 25 mu M AP-5 did not increase the amplitude of EPSCs (8 cells). After washout of AP-5 (4 cells), a second tetanization resulted in long-term potentiation of EPSCs. 4. LT P was dependent on the activation of metabotropic glutamate receptors. The peak amplitude of EPSCs was not increased 5-10 or 15-20 min after tetanization during bath application of the metabotropic glutamate re ceptor antagonist (RS)-alpha-methyl-4-carboxyphenylglycine (500 mu M) (n = 5 cells). 5. Inclusion of the Ca2+ chelator ,2-bis(2-aminophenoxy )ethane-N,N,N',N'-tetraacetic acid (BAPTA; 25 mM) in the patch pipette blocked LTP in O/A interneurons. In five cells recorded with BAPTA-co ntaining electrodes, the mean peak amplitude was not significantly inc reased after tetanization. Thus a rise in postsynaptic intracellular C a2+ appeared necessary for the induction of LTP in these interneurons. 6. Incubation of slices with the inhibitor of nitric oxide synthase N omega-nitro-L-arginine methyl ester (100 mu M) before and throughout the recording session also blocked the increase in EPSC amplitude at 5 -10 min (5 cells) and 15-20 min (3 cells) after tetanization. NO synth esis may therefore be necessary for LTP in O/A interneurons. 7. These results suggest that LTP of excitatory synapses is selectively produce d in O/A but not L-M interneurons, and that this LTP shares similar ch aracteristics with LTP in hippocampal CA1 pyramidal cells. Thus differ ent types of hippocampal interneurons may possess heterogenous synapti c mechanisms coupled to glutamate, by which they may participate diffe rently in long-term synaptic plasticity in the hippocampus.