Slow and fast gamma rhythms represent distinct memory processing states in the hippocampus

Bieri, Kevin Wood
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The hippocampus is central to learning and memory and participates in both the encoding of new memories and their retrieval. It is not known, however, how these dual functions are processed within the same structure without causing interference between what is actively experienced and what is remembered. Different frequencies of gamma oscillations selectively route inputs to area CA1 of the hippocampus, suggesting that gamma subtypes play a role in differentiating between streams of incoming information. Slow gamma oscillations (~25–55 Hz) couple CA1 to area CA3, a region that is thought to store neuronal representations of past events and is thus important for memory retrieval. Fast gamma oscillations (~60–100 Hz) couple CA1 to MEC, a region that supplies the hippocampus with information about ongoing experiences. In this dissertation, I use hippocampal recordings in freely behaving rats to provide evidence that such slow and fast gamma coupling supports distinct memory retrieval and encoding modes in the hippocampus. This is first examined in the principal neurons of the hippocampus, called ‘place cells’, which are thought to provide the ‘where’ component of episodic memory. It was found that place cells alternated between distinct spatial coding modes, representing upcoming locations during slow gamma and recent locations during fast gamma. This concept was explored further in ‘place cell sequences’, which represent trajectories through space, and are thought to store sequential events of an experience. Sequences coded paths sweeping ahead of the animal during slow gamma, and coded ongoing, real-time locations during fast gamma. Also, it was found that different phases of the slow gamma cycle coded specific locations, suggesting a mechanism for how slow gamma promotes retrieval of multi-item memories. Lastly, slow and fast gamma were examined during novel and familiar experiences. Fast gamma was enhanced during encoding of novel object-place associations, while slow gamma coupling between CA3 and CA1 was associated with retrieval of familiar object-place associations. Taken together, these results support the hypothesis that distinct gamma subtypes provide a novel mechanism for separating the dual “reading” and “writing” functions of the hippocampus.