Signaling properties of stratum oriens interneurons in the hippocampus of transgenic mice expressing EGFP in a subset of somatostatin‐containing cells

Abstract

GABAergic interneurons constitute a heterogeneous group of cells that exert a powerful control on network excitability and are responsible for the oscillatory behavior crucial for information processing in the brain. These cells have been differently classified according to their morphological, neurochemical, and physiological characteristics. Here, whole cell patch clamp recordings were used to further characterize, in transgenic mice expressing EGFP in a subpopulation of GABAergic interneurons containing somatostatin (GIN mice), the functional properties of EGFP-positive cells in stratum oriens of the CA1 region of the hippocampus, in slice cultures obtained from P8 old animals. These cells showed passive and active membrane properties similar to those found in stratum oriens interneurons projecting to stratum lacunosum-moleculare. Moreover, they exhibited different firing patterns that were maintained upon membrane depolarization: irregular (48%), regular (30%), and clustered (22%). Trains of action potentials in interneurons evoked in a minority of principal cells (3/45) small amplitude GABAergic currents that at 20 Hz underwent short-term depression. In contrast, excitatory connections between principal cells and EGFP-positive interneurons were highly reliable (17/55) and exhibited a frequency and use-dependent facilitation particularly in the gamma band. In addition, recordings from paired of interconnected EGFP-positive cells revealed in 47% of the cases electrical coupling, which was abolished by carbenoxolone (200 microM). On average, the coupling coefficient was 0.21 +/- 0.07. When electrical coupling was particularly strong it acted as a powerful low-pass filter, thus contributing to alter the output of individual cells. In conclusion, it appears that the dynamic interaction between cells with various firing patterns could differently affect GABAergic signaling, leading, as suggested by simulation data, to a wide range of interneuronal communication within the hippocampal network.