Phenotype-dependent Ca2+ dynamics in single boutons of various anatomically identified GABAergic interneurons in the rat hippocampus

Abstract

Interneurons (INs) of the hippocampus exert versatile inhibition on pyramidal cells by silencing the network at different oscillation frequencies. Although IN discharge can phase-lock to various rhythms in the hippocampus, under high-frequency axon firing, the boutons may not be able to follow the fast activity. Here, we studied Ca2+ responses to action potentials (APs) in single boutons using combined two-photon microscopy and patch clamp electrophysiology in three types of INs: non-fast-spiking (NFS) neurons showing cannabinoid 1 receptor labelling and dendrite targeting, fast-spiking partially parvalbumin-positive cells synapsing with dendrites (DFS), and parvalbumin-positive cells with perisomatic innervation (PFS). The increase in [Ca2+]i from AP trains was substantially higher in NFS boutons than in DFS or PFS boutons. The decay of bouton Ca2+ responses was markedly faster in DFS and PFS cells compared with NFS neurons. The bouton-to-bouton variability of AP-evoked Ca2+ transients in the same axon was surprisingly low in each cell type. Importantly, local responses were saturated after shorter trains of APs in NFS cells than in PFS cells. This feature of fast-spiking neurons might allow them to follow higher-frequency gamma oscillations for a longer time than NFS cells. The function of NFS boutons may better support asynchronous GABA release. In conclusion, we demonstrate several neuron-specific Ca2+ transients in boutons of NFS, PFS and DFS neurons, which may serve differential functions in hippocampal networks. Using single stimulation the Δ[Ca2+]i measured in botons show phenotype-dependent differences (A). At train stimulation (5APs at 60 Hz) the differences are much larger (B). Note that the kinetics of the firs component in FS cells are markedly faster (C).