Properties and dynamics of inhibitory synaptic communication within the CA3 microcircuits of pyramidal cells and interneurons expressing parvalbumin or cholecystokinin

Kohus, Zsolt and Káli, Szabolcs and Rovira Esteban, Laura and Schlingloff, Dániel and Papp, Orsolya and Freund, Tamás and Hájos, Norbert and Gulyás, Attila (2016) Properties and dynamics of inhibitory synaptic communication within the CA3 microcircuits of pyramidal cells and interneurons expressing parvalbumin or cholecystokinin. JOURNAL OF PHYSIOLOGY - LONDON, 594 (13). pp. 3745-3774. ISSN 0022-3751

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Abstract

Different hippocampal activity patterns are determined primarily by the interaction of excitatory cells and different types of interneurons. To understand the mechanisms underlying the generation of different network dynamics the properties of synaptic transmission need to be uncovered. Perisomatic inhibition has been shown to be critical for the generation of sharp wave-ripples, gamma oscillations as well as pathological epileptic activities. Therefore, we decided to quantitatively and systematically characterize the temporal properties of the synaptic transmission between perisomatic inhibitory neurons and pyramidal cells in the CA3 area of mouse hippocampal slices, using action potential patterns recorded during physiological and pathological network states. PV+ and CCK+ interneurons had distinct intrinsic physiological features. Interneurons of the same type formed reciprocally connected subnetworks, while the connectivity between interneuron classes was sparse. The characteristics of unitary interactions depended on the identity of both synaptic partners, while the short-term plasticity of synaptic transmission depended mainly on the presynaptic cell type. PV+ interneurons showed frequency-dependent depression, while more complex dynamics characterized the output of CCK+ interneurons. We quantitatively captured the dynamics of transmission at these different types of connection with simple mathematical models, and described in detail the response to physiological and pathological discharge patterns. Our data suggest that the temporal propeties of PV+ interneuron transmission may contribute to sharp wave-ripple generation. These findings support the view that intrinsic and synaptic features of PV+ cells make them ideally suited for the generation of physiological network oscillations, while CCK+ cells implement more subtle, graded control in the hippocampus. This article is protected by copyright. All rights reserved.

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