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Fast and Slow Gamma Rhythms Are Intrinsically and Independently Generated in the Subiculum

Gamma rhythms are essential for memory encoding and retrieval. Despite extensive study of these rhythms in the entorhinal cortex, dentate gyrus, CA3, and CA1, almost nothing is known regarding their generation and organization in the structure delivering the most prominent hippocampal output: the subiculum. Here we show using a complete rat hippocampal preparation in vitro that the subiculum intrinsically and independently generates spontaneous slow (25–50 Hz) and fast (100–150 Hz) gamma rhythms during the rising phase and peak of persistent subicular theta rhythms. These two gamma frequencies are phase modulated by theta rhythms without any form of afferent input from the entorhinal cortex or CA1. Subicular principal cells and interneurons phase lock to both fast and slow gamma, and single cells are independently phase modulated by each form of gamma rhythm, enabling selective participation in neural synchrony at both gamma frequencies at different times. Fast GABAergic inhibition is required for the generation of fast gamma, whereas slow gamma is generated by excitatory and inhibitory mechanisms. In addition, the transverse subicular axis exhibits gamma rhythm topography with faster gamma coupling arising in the distal subiculum region. The subiculum therefore possesses a unique intrinsic circuit organization that can autonomously regulate the timing and topography of hippocampal output synchronization. These results suggest the subiculum is a third spontaneous gamma generator in the hippocampal formation (in addition to CA3 and the entorhinal cortex), and these gamma rhythms likely play an active role in mediating the flow of information between the hippocampus and multiple cortical and subcortical brain regions.