Reactivation, replay, and preplay: how it might all fit together

Abstract

Sequential activation of neurons that occurs during "offline" states, such as sleep or awake rest, is correlated with neural sequences recorded during preceding exploration phases. This so-called reactivation, or replay, has been observed in a number of different brain regions such as the striatum, prefrontal cortex, primary visual cortex and, most prominently, the hippocampus. Reactivation largely co-occurs together with hippocampal sharp-waves/ripples, brief high-frequency bursts in the local field potential. Here, we first review the mounting evidence for the hypothesis that reactivation is the neural mechanism for memory consolidation during sleep. We then discuss recent results that suggest that offline sequential activity in the waking state might not be simple repetitions of previously experienced sequences. Some offline sequential activity occurs before animals are exposed to a novel environment for the first time, and some sequences activated offline correspond to trajectories never experienced by the animal. We propose a conceptual framework for the dynamics of offline sequential activity that can parsimoniously describe a broad spectrum of experimental results. These results point to a potentially broader role of offline sequential activity in cognitive functions such as maintenance of spatial representation, learning, or planning.

Figure 1

The dynamics of offline sequential activity (OSA) as a function of exposure. This schematic summarizes the results of many reactivation studies in novel and familiar environments. (a) The number of OSA within a day increases with the length of exposure (solid line segments). At the same time, the level of OSA decreases across days as the animal becomes familiar with a novel environment (dashed line). Δr represents the amount of intrinsic OSA (Δr = 0 implies that OSA are purely reactivation of prior sensory-driven sequences). The grey-shaded regions are compressed, and the dynamics within these regions is omitted here for clarity. They are shown in the next panel. (b) Dynamics of OSA within one day. The solid lines are based on experimental observations. The dashed lines represent different hypotheses about the unknown dynamics of OSA between the end of the exposure and the beginning of the sleep phase.