The hippocampal sharp wave–ripple in memory retrieval for immediate use and consolidation

Abstract

Various cognitive functions have long been known to require the hippocampus. Recently, progress has been made in identifying the hippocampal neural activity patterns that implement these functions. One such pattern is the sharp wave-ripple (SWR), an event associated with highly synchronous neural firing in the hippocampus and modulation of neural activity in distributed brain regions. Hippocampal spiking during SWRs can represent past or potential future experience, and SWR-related interventions can alter subsequent memory performance. These findings and others suggest that SWRs support both memory consolidation and memory retrieval for processes such as decision-making. In addition, studies have identified distinct types of SWR based on representational content, behavioural state and physiological features. These various findings regarding SWRs suggest that different SWR types correspond to different cognitive functions, such as retrieval and consolidation. Here, we introduce another possibility — that a single SWR may support more than one cognitive function. Taking into account classic psychological theories and recent molecular results that suggest that retrieval and consolidation share mechanisms, we propose that the SWR mediates the retrieval of stored representations that can be utilized immediately by downstream circuits in decision-making, planning, recollection and/or imagination while simultaneously initiating memory consolidation processes.

Hippocampal ensembles represent sequential relationships among discrete nonspatial events

“…However, the specific prefrontal mechanisms remain to be demonstrated. Finally, it remains to be determined whether the novel forms of sequence coding reported here are 5/24 present in other medial temporal lobe structures, and how these "online" theta-associated representations interact with "offline" sharp-wave-ripple-associated representations related to upcoming behavior or goals observed during reward consumption, quiescence, or sleep 15,16 . Figure 1.…”

“…First, hippocampal ensemble activity tends to exhibit sequential firing fields during the presentation of individual stimuli or inter-stimulus intervals (also known as "time cell" activity) 11,12 , which has been shown to provide a strong temporal signal within such task events 13,14 . Second, hippocampal neurons have been shown to code for sequences of spatial locations under different experimental conditions 6,15,16 . Of particular interest here is evidence that hippocampal activity can represent sequences of past, current, and upcoming locations when animals run on a maze [17][18][19][20] or pause at a decision point (vicarious trial-and-errors) 21 , conditions in which the hippocampal network displays prominent theta oscillations and is thought to be engaged in online processing of upcoming decisions and goals 6,9 .…”

Regular cycling between representations of alternatives in the hippocampus

“…Importantly, generative thinking has been found to activate and require the hippocampus 18,19 , a brain region traditionally linked to memory and spatial navigation. Indeed, recent work on spatially selective hippocampal neurons (place cells) has found activity patterns encoding single generative scenarios in the form of single hypothetical spatial paths [11][12][13][14][15][16][17] . Yet despite this advance, these generative activity patterns have been found to occur only intermittently (~1 Hz or slower), and thus cannot implement the speed and constant operation required by natural behavior.…”

“…Previous work has identified candidate patterns of neural activity encoding possible future scenarios, but these patterns have been found to occur only intermittently and in association with relatively slow (~1 Hz or less), overtly deliberative behaviors, namely head scanning 11,12 and immobility [13][14][15][16][17] . As a consequence, it has remained unknown how the brain is capable of representing possible future scenarios both quickly and constantly.…”

Awake hippocampal-prefrontal replay mediates spatial learning and decision making

“…During replay, temporally compressed sequences of place cells reactivate spatial trajectories that span parts of the entire environment in either forward or reverse order (Ambrose et al, 2016;Csicsvari et al, 2007;Davidson et al, 2009;Diba and Buzsáki, 2007;Farooq and Dragoi, 2019;Foster and Wilson, 2006;Gupta et al, 2010;Ólafsdóttir et al, 2017;Pfeiffer and Foster, 2013;Tang et al, 2017;Xu et al, 2019). Awake hippocampal replay, seen prominently during pauses in exploration and consummatory behavior, is known to be necessary for spatial learning, especially for spatial working memory tasks (Jadhav et al, 2012), and has been proposed to potentially provide neural correlates of various memory processes, notably memory consolidation, recall, and decision making (Buzsáki, 2015;Carr et al, 2011;Foster, 2017;Joo and Frank, 2018;Tang and Jadhav, 2018).…”