Abstract
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-gammaM; 80 Hz) occurred on theta cycle peaks, while in the dentate gyrus, fast (DG-gammaF; 110 Hz), and slow (DG-gammaS; 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-gammaF, which was largely independent from CA1 fast gamma oscillations (CA1-gammaF) of similar frequency and timing. Spike timing of units recorded in either CA1 area or dentate gyrus were modulated by CA1-gammaM. 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.
Highlights
The hippocampus receives inputs from associative cortical areas, and is a key structure for spatial navigation and episodic memory (O’Keefe and Nadel 1978; Buzsaki and Moser 2013)
Their occurrence depended on the phase of ongoing theta oscillation, and appeared strikingly different in the stratum lacunosum-moleculare of the CA1 area, and the molecular layer of the dentate gyrus (DG)
In the CA1 stratum lacunosum-moleculare, high amplitude gamma oscillation transients were often observed on the peak of theta cycles, measured in the LFP of the CA1 pyramidal cell layer
Summary
The hippocampus receives inputs from associative cortical areas, and is a key structure for spatial navigation and episodic memory (O’Keefe and Nadel 1978; Buzsaki and Moser 2013). The majority of its external afferents originate in the entorhinal cortex (EC), and reach the hippocampal formation via the temporoammonic (TA), and perforant pathways (PP), that terminate in anatomically adjacent areas, separated by the hippocampal fissure (Witter 2012). The PP is involved in contextual memory (Kitamura et al 2015), and connects layer two (L2) of the EC to the dentate gyrus (DG; van Groen et al 2003; Witter 2012). This pathway forms the very initial stage of information processing in hippocampal circuitry. The TA, which is indispensable in temporal association memory (Suh et al 2011), originates from the more upstream layer three (L3) of the EC. The TA innervates a more downstream level of the hippocampal trisynaptic loop via terminals located in the stratum lacunosum-moleculare of the CA1 area (van Groen et al 2003; Witter 2012)
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