Hippocampal Replay of Extended Experience

“Place cells in the hippocampal formation fire selectively when an animal moves through particular locations (‘‘place fields’’) in the environment (O’Keefe and Dostrovsky, 1971; Wilson and McNaughton, 1993).”

“…replay detection in the decoded spatial domain affords advantages over methods that examine firing order across individual units, such as pair-wise correlation (Wilson and McNaughton, 1994) and spike-sequence detection (Diba and Buzsáki, 2007; Foster and Wilson, 2006; Lee and Wilson, 2004).”

“This interpretation of the functional role of awake replay is also consistent with work suggesting a high degree of overlap in the cognitive processes supporting both episodic recall and the evaluation of future events in humans (Buckner and Carroll, 2007; Schacter et al., 2007).”

“Place cells in the hippocampal formation fire selectively when an animal moves through particular locations (‘‘place fields’’) in the environment (O’Keefe and Dostrovsky, 1971; Wilson and McNaughton, 1993).”

“For example, the reverse replay event in Figure 4D proceeds in the B/A direction (from 7.5 to 2.5 m on the track) but uses the hippocampal ensemble code associated with running in the opposite A/B direction, as indicated by the blue color.”

“An isolated ripple has a limited duration and therefore its neural content consists of a sequence of limited number of place cells with place fields covering routes with a limited length (Davidson et al., 2009).”

“However, it seems that awake replay can be initiated at remote locations on the track [24] and may correspond to a different track altogether [58].”

“5 SD of the mean.(16) HFO power in the ripple and fast ripple band were calculated using a power spectral density function.”

“As such, slow oscillations are indirectly linked to the reactivation and consolidation of memory in hippocampal–cortical circuits (Carr et al., 2011; Davidson et al., 2009; Foster & Wilson, 2006; Gupta et al., 2010; Karlsson & Frank, 2009).”

“Ensembles of hippocampal place cells have been shown to fire sequentially along trajectories from an animal’s physical location, which may be important for the association between distal locations (Diba and Buzsaki, 2007; Johnson and Redish, 2007; Davidson et al., 2009).”

“…to periods when the animals’ speed remained below 3cm/s. Place cell activity during reactivations was analysed using a Bayesian decoding approach(Davidson et al., 2009; Olafsdottir et al., 2016b; Zhang et al., 1998) to calculate the probability of an animal’s location on the track given the…”

“During exploration, the reactivation seen in transient SWRassociated network bursts tends to occur when animals stop briefly (Davidson et al., 2009; Foster andWilson, 2006).”

“The phenomenon has been extensively replicated [53,54,55 ,56 ,57].”

“To evaluate neural representations at the ensemble level, Bayesian decoding was implemented as previously described (Davidson et al., 2009; Shin et al., 2019; Tang et al., 2017; Zhang et al., 1998): a memoryless Bayesian decoder was built for different trajectory types (for outbound, C-to-L vs.”

“For example, prospection has been seen in the hippocampus: rats will not only think about portions of the environment that they recently experienced but will also project into parts of the environment that are in front of them [66].”

“Such an encoded sequence is evident in spontaneous replays of place cell spiking during quiescent (Muller and Kubie, 1989; Davidson et al., 2009; Karlsson and Frank, 2009; Carr et al., 2011; Dragoi and Tonegawa, 2011; Zeithamova et al., 2012) and sleep states (Skaggs and McNaughton, 1996; Louie and…”

“Proc Natl Acad Sci USA 104(19):8149–8154.”

“Reactivation during such pauses in behaviour can occur in a forward order, as in sleep, as well as in reverse order (Csicsvari et al., 2007; Diba & Buzsáki, 2007; Davidson et al., 2009; Foster & Wilson, 2006; Gupta et al., 2010).”

“The posterior probability at bin xj conditioned on the activity vector k ! (with the i element as ki) is given by Bayes rule (assuming Poisson spiking noise statistics, independence between neurons, and a uniform spatial prior (Davidson et al., 2009)):”

“Abolished Spatial Information Content of Reactivation Events in Calcineurin KO It has been demonstrated that awake SWR events are associated with temporally sequenced activity patterns of hippocampal place cells, referred to as ‘‘replay’’ due to the resemblance to spatial activity patterns in prior behavioral experien…”

“…decoder was used to calculate the probability of the animal’s location given the firing rate templates of the neurons that fired and their spikes that occurred in each time window (Zhang et al., 1998; Davidson et al., 2009; Karlsson and Frank, 2009; Gupta et al., 2012; Pfeiffer and Foster, 2013).”

“This assumption is not necessarily true or known to be true, for example, if the goal is to decode a hidden stimulus with unknown temporal dynamics (Davidson et al. 2009; Kloosterman 2012).”

“During this period, ensembles of pyramidal neurons become briefly reactivated (Wilson and McNaughton 1994; Skaggs and McNaughton 1996; Kudrimoti et al. 1999; Foster and Wilson 2006; Jackson et al. 2006; Diba and Buzsaki 2007; Davidson et al. 2009).”

“Because reactivation events can span SWRs in a chain (Davidson et al., 2009), we included chained SWR events (although exclusion of chains did not change the results).”

“883 Instances of reactivation have also been described during quiet wakefulness (Foster & Wilson 2006; 884 Diba & Buzsáki 2007; Davidson et al. 2009; Karlsson & Frank 2009) and REM sleep (Louie & Wilson 885 2001).”

“When at rest, or during pauses in exploration of a track, place cells in the rat hippocampus fire in sequences corresponding to portions of the route already traveled or about to be traveled (75).”

“…relevant physiological data currently includes spiking forward sweep events (Johnson and Redish, 2007; Pfeiffer and Foster, 2013) and sharp wave ripple events (Foster and Wilson, 2006; Davidson et al., 2009; Louie and Wilson, 2001; Jadhav et al., 2012) observed during goal directed spatial tasks.”

“Sequences replayed by the hippocampus can diverge substantially from behavior (Davidson et al., 2009; Karlsson and Frank, 2009; Gupta et al., 2010), and are influenced by cognitive factors such as novelty (Hirase et al., 2001; Cheng and Frank, 2008), learning (Jackson et al., 2006) and…”

“Such replay of recent learning has been replicated across several studies (Louie and Wilson, 2001; Davidson, Kloosterman, & Wilson, 2009) and in other brain regions (Peyrache, Khamassi, Benchenane, Wiener, & Battaglia, 2009; Ji & Wilson, 2007).”

“We detected HSEs in which many cells fired action potentials together (see STAR Methods; Davidson et al., 2009).”

“A number of studies have shown that ripple-coincident neural firing during sleep is reminiscent of neural activity patterns associated with previous experiences (Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Nádasdy et al., 1999; Lee and Wilson, 2002; Davidson et al., 2009).”

“We next analyzed replay of spatial trajectories [14, 25] by fitting the best trajectory to the maximum-a-posteriori position estimates using weighted isotonic regression (see STAR Methods).”

“One possibility is that successive SWRs convey related messages, as observed during awake replay events [145], and thus need orchestration at a slower timescale for coherent consolidation of extended memories.”

“Hippocampal place cells are reactivated in a compressed time frame during SWRs in a manner that recapitulates spatial experience (Nádasdy et al. 1999; Lee & Wilson, 2002; Davidson et al. 2009; Karlsson & Frank, 2009).”

“These events typically happen during rest 27,31,33 , but also during pauses in a behavioural task 148 .”

“In contrast, the demonstration of preplay sequences indicated that the hippocampal network of naïve mice and rats was preconfigured before the novel experience and further argued that the firing sequences on the novel track were not entirely created de novo in response to the external stimuli (Figure 3b) [24,34,39].”

“consolidation with or without partial external input (Buzsaki, 1989; Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Nadasdy et al., 1999; Lee and Wilson, 2002; Foster and Wilson, 2006; Diba and Buzsaki, 2007; Ji and Wilson, 2007; Gelbard-Sagiv et al., 2008; Davidson et al., 2009; Karlsson and Frank, 2009; C…”

“Coordinated firing of neuronal ensembles during initial encoding has been observed to spontaneously reoccur during ripples (Wilson and McNaughton, 1994; Ji and Wilson, 2007; Davidson et al., 2009), with ripples instigating information transfer from the hippocampus to the cortex when phase locked to SOs and sleep spind…”

“…awake states, such as brief pauses during exploration, these SPW-Rs do not appear to be involved in memory consolidation, but in different, complementary functions, such as memory-guided decision making (Foster and Wilson, 2006; Diba and Buzsáki, 2007; Carr et al., 2011; Jadhav et al., 2012).”

“…track or in a 2D environment, bursting activity occasionally spans sequences which cover—on a compressed time scale—a possible trajectory of the animal (Foster and Wilson, 2006; Diba and Buzsaki, 2007; Davidson et al., 2009; Karlsson and Frank, 2009; Gupta et al., 2010; Pfeiffer and Foster, 2013).”

“296 This level of accuracy is comparable to that of other studies (Davidson et al., 2009; Shin et al., 297 2019; Farooq and Dragoi, 2019), and reflects in part the presence of "theta sequences" (Dragoi 298 and Buzsáki, 2006; Foster and Wilson, 2007) where position deviates behind and ahead of the 299 animal across ind…”

“We used a previously established criterion (Davidson et al., 2009) to detect these MUA bursts and examined the associated hippocampal ensemble spiking activity.”

“The sequences of activity are replayed in a further compressed manner, while the animal rests and sleeps (Wilson and McNaughton, 1994; Nadasdy et al., 1999; Lee and Wilson, 2002; Pastalkova et al., 2008; Davidson et al., 2009).”

“more prevalent in the awake state (Ambrose et al., 2016; Davidson et al., 2009; Diba & Buzs aki, 2007; Foster & Wilson, 2006; Grosmark & Buzs aki, 2016).”

“The ability of the hippocampus to " look ahead " or bind locations together is exemplified by sequential firing of ensembles of place cells along trajectories from an animal's location (Davidson et al., 2009; Diba and Buzsaki, 2007; Johnson and Redish, 2007a;).”

“During this nonlocal firing, the place cells are activated in behaviorally relevant sequences that can represent trajectories the rat previously traversed or could traverse (Davidson et al. 2009; Foster and Wilson 2007; Gupta et al. 2010, 2012; Pfeiffer and Foster 2013; Skaggs and McNaughton 1996).”

“In addition, replay events (chained together; Davidson, Kloosterman, & Wilson, 2009) can last longer than 120 ms, potentially covering longer trajectories, suggesting that the order of magnitude estimate for the timescales in the model is consistent with published data.”

“Extensive research in animals [29] [30] has found that neuronal activity associated with past experiences occurs in the MTL, and in humans spontaneous replay of BOLD signal associated with an item has been shown to support later memory [31], possibly through memory consolidation to neocortical…”

“Differences have also been found in representations during wake and sleep states [56], with wake states showing flexible sequences [32,34,47] more likely to be involved in some sort of analytical processing than consolidation, but with sleep states being more consistent with a consolidation hypothesis.”

“More complex and extended mazes can be built with much greater effort but are still restricted to the lab scale (Davidson et al. 2009; Rich et al. 2014).”

“, 2017), or even be initiated at remote locations (Davidson et al., 2009; Karlsson and Frank, 2009; Gupta et al., 2010).”

“In early work, replay was found to correspond to sequences of locations starting near and projecting ahead of the animal, just prior to running along that same path in the linear maze, consistent with anticipation of upcoming experience [74,79,80].”

“Such neural replay has also been reported in awake states, for instance, when rodents pause in exploring a maze [28,29].”

“the animal holds a particular location in space (Jackson et al., 2006; Davidson et al., 2009; Karlsson and Frank, 2009).”

“Furthermore, sequential replay of spatial trajectories occurs in the dorsal hippocampus of rodents (Davidson et al. 2009; Gupta et al. 2010).”

“…on the reactivation of neuronal ensembles that have been activated during exploration in a temporally compressed fashion (Lee and Wilson, 2002; Davidson et al., 2009; Karlsson and Frank, 2009), thereby stabilizing the synaptic connections between ensemble members (Markram et al., 1997) not…”

“ORIGINAL RESEARCH ARTICLE published: 04 December 2012 doi: 10.3389/fnbeh.2012.00084 Disrupting neural activity related to awake-state sharp wave-ripple complexes prevents hippocampal learning”

“…1989; Wilson and McNaughton 1994), have been shown to generate spike sequences that predict to-be-visited places and delayed actions or a chaining of past and expected events (Diba and Buzsáki 2007; Davidson et al. 2009; Gupta et al. 2010; cf., Carr et al. 2011; Buzsáki and Lopes da Silva 2012).”

“Replay of memory sequences during wakefulness is compressed in time, being embedded within high-frequency oscillations (ripples), and occurs in a temporally reversed order (Foster and Wilson, 2006; Davidson et al., 2009).”

“In the dorsal hippocampus, forward replay is significantly more frequent than reverse replay [54, 55], which contributes to the spike sequence consistency between online theta cycles and offline ripples [56].”

“, Bayesian decoding (Davidson et al., 2009; Karlsson and Frank, 2009; Zhang et al., 1998), is the most comprehensive statistical method to assess the ability of spontaneous network patterns (i.”

“…resonates with the discovery in rodents of rest-associated hippocampal replay of experienced trajectories as well as of trajectories that were never travelled during actual exploration (O’Keefe et al., 1998; Davidson et al., 2009; Harvey et al., 2009; Gupta et al., 2010; Wills et al., 2010).”

“To test whether replay events were compressed or expanded in time (Csicsvari et al., 2007; Davidson et al., 2009; Diba and Buzsáki, 2007; Euston et al., 2007; Foster and Wilson, 2006; Ji and Wilson, 2007; Karlsson and Frank, 2009; Lansinket al., 2009; Lee and Wilson, 2002; Louie and Wilson, 2001; Wilber et al., 2017),…”

“This corresponds to a compression factor of about 15 to 20 relative to the original behaviour [102].”

“It represents the reactivation of hippocampal memory representations and have been proposed as a cognitive biomarker for episodic memory [37].”

“The reactivated patterns during SWRs closely resembled the compressed structure of encoded memory observed within individual cycles of the theta rhythm during awake behavior in the hippocampus [12,50].”

“As the proportion of hippocampal SPW-Rs that can be decoded as replay events is small in the hippocampus (5%–20%; Davidson et al., 2009; Dragoi and Tonegawa, 2011; Foster and Wilson, 2006; Grosmark and Buzsáki, 2016; Karlsson and Frank, 2009; Michon et al., 2019; Wu and Foster, 2014), we reasoned that perhaps some nav…”