Membrane properties and synaptic currents evoked in CA1 interneuron subtypes in rat hippocampal slices.

Abstract

1. Intrinsic membrane properties and pharmacologically isolated excitatory and inhibitory postsynaptic currents (EPSCs and IPSCs, respectively) were characterized with the use of whole cell current- and voltage-clamp recordings, in combination with biocytin labeling, in different subtypes of CA1 interneurons and pyramidal cells in rat hippocampal slices. 2. Three classes of interneurons were selected on the basis of their soma location in the CA1 region: 1) in stratum (str.) oriens near the alveus (O/A), 2) near str. pyramidale, and 3) near the border of str. radiatum and lacunosum-moleculare. Each class of biocytin-labeled cells demonstrated specific cellular morphology. The somata of all interneurons were nonpyramidal in shape and usually multipolar. However, the pattern of dendritic and axonal arborizations of labeled interneurons differed in each class. 3. In current-clamp recordings, all interneuron subtypes had shorter-duration and smaller-amplitude action potentials than pyramidal cells. Fast- and medium-duration afterhyperpolarizations were larger in amplitude in interneurons. Cell input resistance was greater and membrane time constant was faster in all interneuron subtypes than in pyramidal cells. 4. Depolarizing current pulses evoked regular firing in all classes of interneurons, whereas burst firing was observed in 50% of pyramidal cells. With hyperpolarizing current pulses, all nonpyramidal and pyramidal cell types displayed inward rectification followed by anodal break excitation. 5. Electrical stimulation of nearby afferents evoked excitatory postsynaptic potentials (EPSPs) in all cells. EPSPs were of short duration and usually followed by inhibitory postsynaptic potentials (IPSPs). EPSPs were mediated by glutamate, because they were blocked by non-N-methyl-D-aspartate (non-NMDA) and NMDA antagonists [6-cyano-7-nitroquinoxaline-2,3-dione (CNQX) and (+/-)-2-amino-5-phosphonopentanoic acid (AP5), respectively]. In the presence of these antagonists, IPSPs were evoked in isolation and reversed near -72 mV. 6. In voltage-clamp recordings, non-NMDA EPSCs were isolated pharmacologically in the presence of AP5 and the gamma-aminobutyric acid-A (GABAA) antagonist bicuculline (BIC). Their properties were similar in all interneuron subtypes and pyramidal cells. Current-voltage (I-V) relations were linear, and mean reversal potentials were near 5 mV. Non-NMDA EPSCs were reversibly antagonized by CNQX. 7. NMDA EPSCs were pharmacologically isolated during CNQX and BIC application and were observed in all cell types. I-V relations of NMDA EPSCs demonstrated a region of negative slope at membrane potentials between -80 and -20 mV and their reversal potential was near 7 mV. The rise time of NMDA EPSCs was significantly slower in O/A interneurons than in other cell types. NMDA EPSCs were reversibly antagonized by AP5. 8. GABAA IPSCs were pharmacologically isolated in AP5 and CNQX and their properties were similar in all cell types. I-V relations of GABAA IPSCs were linear with mean reversal potentials near -32 mV. GABAA IPSCs were reversibly blocked by BIC. 9. In conclusion, morphologically different subtypes of interneurons located in O/A, near str. pyramidale, and near the str. radiatum/lacunosum-moleculare border displayed intrinsic membrane properties that were distinct from pyramidal cells, but were similar among them. In contrast, the properties of non-NMDA, NMDA, and GABAA postsynaptic currents were similar between interneurons and pyramidal cells, except for NMDA EPSCs, which had slower rise times in O/A interneurons.