The Journal of Neurophysiology Vol. 79 No. 6 June 1998, pp. 3229-3237
Copyright ©1998 The American Physiological Society

Synaptic Connectivity of Distinct Hilar Interneuron Subpopulations

Matteo Forti and Hillary B. Michelson

Department of Pharmacology, State University of New York Health Science Center at Brooklyn, Brooklyn, New York 11203

Forti, Matteo and Hillary B. Michelson. Synaptic connectivity of distinct hilar interneuron subpopulations. J. Neurophysiol. 79: 3229-3237, 1998. Dual intracellular recordings of hilar interneurons and CA3 pyramidal cells were performed in transverse slices of guinea pig hippocampus in the presence of the convulsant compound 4-aminopyridine (4-AP) and ionotropic glutamate receptor antagonists. Under these conditions, interneurons burst fire synchronously, producing synchronized inhibitory postsynaptic potentials (sIPSPs) in pyramidal cells. Three different hilar interneuron subpopulations that contributed to the sIPSP were identified based on their projection properties and morphology. These three types were pyramidal-like stellate interneurons, spheroid interneurons, and oviform interneurons. Physiologically, pyramidal-like stellate interneurons could be differentiated from the other interneuron subpopulations because they generated short synchronized bursts of action potentials coincident with the hyperpolarizing and depolarizing -aminobutyric acid-A (GABA_A)-mediated inhibitory postsynaptic potentials (IPSPs) recorded in pyramidal cells. The bursts in pyramidal-like stellate cells were abolished by theGABA_A-receptor blocker, bicuculline. In contrast, spheroid interneurons of the dentate-hilus (D-H) border and oviform hilar interneurons exhibited prolonged bicuculline-resistant bursts that occurred coincident with the GABA_B pyramidal cell sIPSPs. Pyramidal-like stellate interneurons likely did not contribute to the generation of synchronized GABA_B responses in hippocampal pyramidal cells. Spheroid interneurons were unique among these subpopulations of interneurons in that the bicuculline-resistant bursts in spheroid interneurons were sustained by a synaptic depolarization that persisted in the presence of antagonists of ionotropic glutamate, GABA_A and GABA_B receptors [6-cyano-7-nitroquinoxaline-2,3-dione, 20 µM; 3-3(2-carboxipiperazine-4-yl)propyl-1-phosphonate, 20 µM; bicuculline, 10-15 µM; CGP 55845A, 20 µM]. This novel depolarizing potential reversed between 30 and 0 mV. No noticeable synaptic depolarization sustaining burst firing could be isolated in oviform interneurons, suggesting that firing in this interneuron subpopulation was synchronized by nonsynaptic mechanisms. The results of the present study indicate that the hilar inhibitory circuit is composed of at least three different subpopulations of interneurons, distinguishable by their morphological characteristics and synaptic inputs and outputs. These findings give further support to the hypothesis that there are distinct populations of interneurons producing GABA_A and GABA_B responses with defined functional roles within the hippocampal inhibitory circuit. Notably, we found that spheroid interneurons were unique among the hilar interneurons studied, in that the synchronized bursts observed in these cells are sustained by a novel ionotropic glutamate and GABA receptor-independent synaptic depolarization.

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