Distinct gamma oscillations in the distal dendritic fields of the dentate gyrus and the CA1 area of mouse hippocampus

The molecular layer of the dentate gyrus and the anatomically adjacent stratum lacunosum-moleculare of CA1 area, represent afferent areas at distinct levels of the hippocampal trisynaptic loop. Afferents to the dentate gyrus and CA1 area originate from different cell populations, including projection cells in entorhinal cortex layers two and three, respectively. To determine the organization of oscillatory activities along these terminal fields, we recorded local field potentials from multiple sites in the dentate gyrus and CA1 area of the awake mice, and localized gamma frequency (30–150 Hz) oscillations in different layers by means of current source density analysis. During theta oscillations, we observed different temporal and spectral organization of gamma oscillations in the dendritic layers of the dentate gyrus and CA1 area, with a sharp transition across the hippocampal fissure. In CA1 stratum lacunosum-moleculare, transient mid-frequency gamma oscillations (CA1-gamma(M); 80 Hz) occurred on theta cycle peaks, while in the dentate gyrus, fast (DG-gamma(F); 110 Hz), and slow (DG-gamma(S); 40 Hz) gamma oscillations preferentially occurred on troughs of theta waves. Units in dentate gyrus, in contrast to units in CA1 pyramidal layer, phase-coupled to DG-gamma(F), which was largely independent from CA1 fast gamma oscillations (CA1-gamma(F)) of similar frequency and timing. Spike timing of units recorded in either CA1 area or dentate gyrus were modulated by CA1-gamma(M). Our experiments disclosed a set of gamma oscillations that differentially regulate neuronal activity in the dentate gyrus and CA1 area, and may allow flexible segregation and integration of information across different levels of hippocampal circuitry.