The Role of Plasticity in Replay: Stability Through Anti-Hebbian Rules

Abstract

Hippocampal replay is now considered to be a cornerstone of memory consolidation, yet the synaptic plasticity rules governing its dynamics remain elusive. Under the standard asymmetric Hebbian spike-timing dependent plasticity (STDP) model, the same spike patterns that promote activity propagation along one direction of sequential activation undermine propagation in the reverse direction, compromising “bidirectional” replay. On the other hand, symmetric potentiation rules, as recently proposed for region CA3, risk corrupting the memory trace by saturating synaptic weights. Using Ecker et al.'s recurrent network model of place cells that spontaneously generate replays during ripples, we systematically investigated how different STDP plasticity rules modulate offline replays. We developed a classification framework to study the mechanisms relating different STDP kernels to key replay characteristics, including directionality, speed, and stability. Our results confirmed that symmetric potentiation rules during offline states saturate synapses, inducing rigid attractors that corrupt the memory trace, and that an asymmetric Hebbian STDP kernel induces strong biases in the directionality of replay, leading to rapid replay acceleration and replay degradation. Notably, we found that an asymmetric anti-Hebbian STDP kernel preserves replay bi-directionality and stabilizes replay speed. We further identified the negative timing component of the STDP rule as the primary driver of replay speed: potentiation causes deceleration, while depression causes acceleration. These findings provide a mechanistic explanation for empirically observed replay deceleration and suggest a role for anti-Hebbian synaptic depression in stabilizing replay dynamics.