Local Sleep Oscillations: Implications for Memory Consolidation

Abstract

Accumulating evidence suggests that sleep is important for plasticity and memory consolidation (Maquet, 2001; Walker and Stickgold, 2004; Datta and Maclean, 2007; Diekelmann and Born, 2010; Tononi and Cirelli, 2014; Dudai et al., 2015)—the transformation of new labile memories encoded in wakefulness into stable representations that integrate into long-term memory networks. A central model accounting for memory consolidation during sleep is that of coupling between hippocampal (HC) and neocortical networks (Buzsaki, 1996). According to this two-stage model of memory formation [also termed the hippocampal—neocortical dialogue model (Buzsaki, 1989)], the dominant direction of information flow across the brain differs between wake and sleep periods. During wakefulness, acquisition of sensory information mainly drives signal propagation from cortex to hippocampus (HC) (Buzsaki, 1998; Mormann et al., 2008). By contrast, during subsequent non-rapid eye movement (NREM) sleep, this model suggests a central role for information flow from HC to cortex especially around sharp-wave ripples (SWRs) events (Buzsaki, 1998). Accordingly, slow waves that originate in the neocortex repeatedly reactivate the newly encoded HC information when SWRs occur, driving subsequent activity in select cortical circuits (Siapas and Wilson, 1998). However, it is clear that information flow is not strictly unidirectional (Wagner et al., 2010) and may involve complex loops (Rothschild et al., 2017). HC reactivation tends to co-occur with sleep spindles that optimize plasticity (Seibt et al., 2017), resulting in long-term modification of synaptic efficacy. Thus, hippocampal–neocortical coupling requires interregional cross-frequency coordination between sleep oscillations, including slow waves and sleep spindles in thalamo-cortical circuits as well as HC ripples. \n \nThe underlying prevalent assumption is that sleep oscillations (slow waves in particular) are global events that co-occur nearly simultaneously across different brain regions. But in fact, they have been described as traveling waves propagating from anterior-to-posterior cortex (Massimini et al., 2004), and they typically occur out of phase across different cortical sites (Nir et al., 2011; Vyazovskiy et al., 2011; Malerba et al., 2019). How can we reconcile models requiring co-occurrence of sleep oscillations with accumulating evidence of non-uniform timing of oscillations across the brain? In this article, we first review the current data that sheds light on this question, and highlight recent studies that link regional coupling of sleep oscillations with consolidation of specific memories. Then, we highlight the gap between sleep and memory theory and experimental evidence. Based on studies that monitor and manipulate specific cortical circuits, we propose that coupling can occur between sleep oscillations in general, and between HC and cortex specifically, but that such coupling likely involves different brain regions at each point in time, contributing to memory consolidation in select circuits.