Abstract
Hippocampal place cells are activated sequentially as an animal explores its environment. These activity sequences are internally recreated ('replayed'), either in the same or reversed order, during bursts of activity (sharp wave-ripples [SWRs]) that occur in sleep and awake rest. SWR-associated replay is thought to be critical for the creation and maintenance of long-term memory. In order to identify the cellular and network mechanisms of SWRs and replay, we constructed and simulated a data-driven model of area CA3 of the hippocampus. Our results show that the chain-like structure of recurrent excitatory interactions established during learning not only determines the content of replay, but is essential for the generation of the SWRs as well. We find that bidirectional replay requires the interplay of the experimentally confirmed, temporally symmetric plasticity rule, and cellular adaptation. Our model provides a unifying framework for diverse phenomena involving hippocampal plasticity, representations, and dynamics, and suggests that the structured neural codes induced by learning may have greater influence over cortical network states than previously appreciated.
Highlights
The hippocampal region plays a pivotal role in spatial and episodic memory (O’Keefe and Nadel, 1978; Morris et al, 1982)
The complete network consisted of 8000 excitatory pyramidal cells (PCs) and 150 inhibitory parvalbumin-containing basket cells (PVBCs), corresponding roughly to the size of the
Connections of all types (PC-PC, PC-PVBC, PVBC-PC, PVBC-PVBC) were established randomly using connection type-specific probabilities estimated from anatomical studies
Summary
The hippocampal region plays a pivotal role in spatial and episodic memory (O’Keefe and Nadel, 1978; Morris et al, 1982). Are associated with distinct brain states, and are characterized by distinct oscillatory patterns of the hippocampal local field potential (LFP) (Buzsáki et al, 1983; Colgin, 2016) When rodents explore their environment, place cells of the hippocampus are activated in a sequence that corresponds to the order in which the animal visits their preferred spatial locations (place fields) (O’Keefe and Dostrovsky, 1971). The same sequences of firing activity can be identified, on a faster time scale, during individual cycles of the 4-10 Hz theta oscillation that dominates the hippocampal LFP in this state (O’Keefe and Recce, 1993; Dragoi and Buzsáki, 2006; Foster and Wilson, 2007) These compressed sequences are thought to be optimal for learning via activity-dependent synaptic plasticity (Jensen and Lisman, 2005; Foster and Wilson, 2007). Awake replay is predominantly in the “forward” direction near choice points during navigation (Diba and Buzsáki, 2007; Pfeiffer and Foster, 2013), while it is mainly “backward” when the animal encounters a reward (Diba and Buzsáki, 2007)
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