Sculpting memory during sleep: concurrent consolidation and forgetting

Highlights

• Broad behavioural and neurophysiological support for consolidation during sleep.

• Neurophysiological support for sleep enhancing forgetting and new learning.

• Large amounts of information at encoding lead to sleep-induced forgetting.

• At capacity limits sleep switches from consolidating details to gist abstraction.

• Predictions: manipulating memory load at encoding to influence sleep processes.

There is compelling evidence that sleep actively supports the formation of long-lasting memory representations. Experimental cuing of memories proved that neural replay of representations during sleep plays a causal role for this consolidation, which has also been shown to promote neocortical synaptic plasticity and spine formation. Concurrently, sleep has been proposed to facilitate forgetting through processes of synaptic renormalisation. This view received indirect support by findings in humans of sleep enhancing TMS-evoked plasticity and capabilities for encoding new information. First direct behavioural evidence of sleep inducing forgetting has only recently emerged after encoding large amounts of stimuli in adults. We propose forgetting complements sleep-dependent consolidation and facilitates gist abstraction especially at high memory loads, when reactivation-based consolidation reaches capacity limits.

Introduction

The formation of long-term memory relies on the two distinct processes of encoding (or learning) and consolidation. Retrieval is a third process that contributes to memory formation by re-instating the stored information. Between encoding, that is the uptake of the information, and retrieval lies the period of retention, and already at the beginning of modern memory research it was proposed that during this retention period memories are not merely passively stored but that an active process of consolidation occurs [1], which has received wide support over the past century [2]. Especially, the idea that memory is consolidated during the brain’s offline periods of deep slow wave sleep has risen to a champion of consolidation theory (Figure 1, Figure 2) [3, 4, 5]. Just recently, in the neocortex, the formation of dendritic spines was observed, during sleep after learning a motor task, as a neural substrate of memory formation, which was positively related to task performance [6^••].

At its outset, memory research mainly focused on forgetting [7]. Essentially, two forms of forgetting were proposed. The first argues that forgetting occurs due to interference, that is older memory traces are constantly being overwritten by newer encoding events. Consequently, a passive role of sleep protecting from interference has been claimed repeatedly since its first conceptualisation [8], even though this type of forgetting seems to play only a minor role for memories involving the hippocampal system [9]. The second claims that memory traces passively decay over time and this account, later on, was extended to include active decay processes [10]. Here also, sleep has been proposed to play a major role, renormalizing synaptic weights and balancing out potentiation occurring as a result of encoding information during wake (Figure 2) [11^••].

Covering mainly the period from 2013 to now, we review the latest developments regarding sleep’s role for consolidation and forgetting. Initially, it seems difficult to reconcile these two accounts. To the contrary, building on our previous reasoning [4, 12] we will present a framework, derived from novel developments in the field, to explain how consolidation and forgetting work together to sculpt lasting memories from a day’s clay of episodic experiences. Ultimately, forgetting might arise as the fourth process of memory formation that enables the long-term function of the other three processes.