Forward and reverse delay-driven hippocampal replay without symmetric plasticity

Abstract

Hippocampal replay is a phenomenon observed in mammals and songbirds where neural activation sequences experienced during wakeful periods are repeated during rest or sleep. This mechanism is believed to play a crucial role in episodic memory consolidation, retrieval, and planning. Interestingly, replay can occur in both forward and reverse temporal orders and across a wide range of increased speeds. The learning of activation sequences has traditionally been modeled by temporally asymmetric Hebbian plasticity rules, which explain replay as a chain of activity. The inability of such rules to strengthen backward connections has led to the widespread belief that they cannot account for bidirectional replay. Existing theoretical work therefore explains reverse replay through symmetric connections, which would be formed through symmetric plasticity rules. We propose a delay-coupled neural field model of CA3, where activity propagates as a wave in a ring, and replays occur both forwards and backwards at different speeds. Our model can learn bidirectional replay after a single noisy exposure to a stimulus with either symmetric or asymmetric plasticity. We derive a low-dimensional description of the dynamics and analyze the stability of possible replay speeds.