Spatial Memory Sequence Encoding and Replay During Modeled Theta and Ripple Oscillations

Abstract

Spatial learning involves the storage and replay of temporally ordered spatial information. The hippocampus is a key brain structure involved in spatial learning in rats. Temporally ordered spatial memories are encoded and replayed by the firing rate and phase of hippocampal pyramidal cells and inhibitory interneurons with respect to ongoing network theta and ripple oscillations paced by intra- and extrahippocampal areas. Theta oscillations (4–7 Hz) may contribute to memory formation, whereas fast ripple oscillations to temporally compressed forward and reverse replay of previously stored memories. Different classes of CA1 excitatory and inhibitory neurons and medial septal inhibitory neurons have been shown to differentially phase their activities with respect to theta and ripples. Understanding how the different hippocampal and extrahippocampal areas and their neuronal classes interact during these network oscillations and how they facilitate the storage and replay of spatiotemporal memories is of great importance. A computational model of the hippocampal CA1 microcircuit that uses biophysical representations of the major cell types, including pyramidal cells and four types of inhibitory interneurons, is extended. Inputs to the network come from the entorhinal cortex (EC), the CA3 Schaffer collaterals and the medial septum. A biophysical mechanism of spike timing-dependent plasticity (STDP) is used for learning spatial memory patterns in the correct order. The model addresses two important issues: (1) How are the storage and replay (forward and reverse) of temporally ordered memory patterns controlled in the CA1 microcircuit during theta and ripples? (2) What roles do the various types of inhibitory interneurons play in these processes?