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.”

“Spontaneous replays of such events in sharp-wave ripples, however, are independent of such speeds, stopping times or locations of the animal (Wilson and McNaughton, 1994; Nádasdy et al., 1999; Geisler et al., 2007; Davidson et al., 2009; Yamamoto and Tonegawa, 2017), as well during sleep (Wilson and McNaughton, 1994;…”

“Several studies performing position decoding on rodent hippocampus data have used a split between training and testing data (e.g., Zhang et al. 1998; Rutishauser et al. 2006; Davidson et al. 2009; Resnik et al. 2012; Agarwal et al. 2014), but this practice has not been consistently applied in this field.”

“This cognitive discrepancy should be further elucidated using electrophysiological methods probing into the MTL (Davidson et al., 2009; Foster and Wilson, 2006; Karlsson and Frank, 2009; Diba and Buzsáki, 2007) and the neocortices (Naya et al., 2017).”

“Our finding that replay duration is nearly constant across spatial scales that span an order of magnitude is in clear contrast with experimental results in rodents, in which replay duration has been reported to scale linearly with the length of spatial behaviour 5,20 .”

“For example, replay studies have shown that most (50–90%) candidate hippocampal replay events do not express coherent spatial trajectories [58,71,72].”

“This approach is similar in many ways to previous studies of spatial navigation, position decoding, and replay detection in rodent hippocampus 17,75 .”

“…corridors) and event along the journey could be represented separately as a ‘neural word’ and such words would be concatenated, perhaps via sharp wave ripples (Foster and Wilson 2006; Davidson et al. 2009; Wu and Foster 2014), to represent the entire journey from the beginning to the end.”

“It is known that place cell activities during running are replayed within ripples during normal immobility on the track (awake replay), which can be quantified by a pattern analysis like Bayesian decoding that requires a large number of place cells (Davidson et al., 2009; Karlsson and Frank, 2009; Zhang et al., 1998).”

“Population spike activities from hippocampal place cell assemblies provide a readout of the rat’s spatial location (Zhang et al., 1998; Davidson et al., 2009; Kloosterman et al., 2014; Grosmark and Buzsáki, 2016; Hu et al., 2018; Ciliberti et al., 2018).”

“In these applications, the yaw is tracked through an overhead video camera imaging two LEDs of different colors (e.g., red and green), mounted over the head stage of the neuronal recording system and placed along the anteroposterior axis of the head.”

“Moreover, the hippocampus in many species has been implicated in both the encoding and recall of memory episodes, and spontaneous hippocampal neural dynamics have been associated with sequence prediction (23, 24, 26, 28).”

“3 Maximum likelihood estimation (MLE) for position decoding In addition to OLE, we also employed MLE for position decoding (Zhang et al., 2018; Davidson et al., 2009).”

“For each frame, we decoded the location represented by spiking activity using a Bayesian decoding method used in previous experimental studies (Davidson et al., 2009; Pfeiffer and Foster, 2013).”

“…random input in the present study, but injecting location-specific offline input biases replay starts to that location, consistent with experimental observations 14,15,93 , suggesting that simple modifications of our model may lend themselves easily to studies of replay in these distinct states.”

“…the behavioral exploration (Lee and Wilson, 2002; Harris et al., 2003; Foster and Wilson, 2006; Frontiers in Neural Circuits www.frontiersin.org June 2013 | Volume 7 | Article 112 | 1 NEURAL CIRCUITS O’Neill et al., 2006; Diba and Buzsaki, 2007; Pastalkova et al., 2008; Davidson et al., 2009).”

“The navigation of this graph can be flexible in that it may involve shortcuts (Tolman, 1948), as well as combining and recombining snippets of trajectories (Davidson et al., 2009; Gupta et al., 2010).”

“…and NREM sleep in the hippocampus of rodents where they are important for memory consolidation (10, 12, 54) and less frequent during waking periods where they are important for memory-guided decision-making (55–57), or maze navigation where they predict future navigational behavior (17, 58–60).”

“Furthermore, bundled hippocampal SWRs, which support replay of prolonged experience (Davidson et al., 2009), tend to occur during more extended neocortical UP states than isolated SWRs, suggesting that a longer temporal window is available for bundled SWRs for”

“For instance, an SWR may start at the location where the previous one ended, a.k.a. ‘ chaining ’ , thereby creating long sequences or even shortcuts that were not directly experienced [10,18].”

“It has been recently suggested that a function of such sequences or clusters of SWRs may be to keep in memory and express later prolonged experiences of several individual events that occur in a path along the space (Davidson et al., 2009).”

“Interestingly, the replay can be speeded or time-reversed relative to the original sequence (Davidson et al., 2009); it can also precede action rather than recalling it (Muller and Kubie, 1989; Dragoi and Tonegawa, 2013).”

“In these cases, multiple ripples tend to occur 21,41 – 44 , suggesting that ripples may be building blocks of replay.”

“IF is a Sloan Foundation Fellow, a Searle Scholar, a McKnight Scholar, and acknowledges funding from the Office of Naval Research, through ONR MURI award N00014-10-1-0936.”

“Hippocampal SWRs have been previously associated with replay and memory consolidation and may well be a hallmark of offline memory retrieval and storage processes (Carr, Jadhav, & Frank, 2011; Davidson et al., 2009; Kudrimoti et al., 1999; Pennartz et al., 2004).”

“, hippocampal sharp-wave ripples or neocortical spindles or slow waves; (Ji & Wilson, 2007; Davidson et al., 2009).”

“…ArchT-dHPC and ArchT-vHPC groups, regardless of whether light was delivered during the sample phase (Fig 3C To examine coding of relative position at the population level, we used a Bayesian decoder [52,53] to predict the animal’s position from the activity of simultaneously recorded PFC neurons.”

“Parallel recordings of multiple identified units in behaving rats suggest that well defined neurons are activated in precisely ordered patterns during such states (Davidson et al., 2009; Ji and Wilson, 2007; Wilson and McNaughton, 1994).”

“A Bayesian classifier was employed to predict the spatial bin occupied by the rat on the basis of the temporally binned neural data (Davidson et al., 2009).”

“Moreover, because SWRs often emerge as consecutive chains of multiple SWRs that persist for hundreds of milliseconds (Davidson et al. 2009), the unique properties of gRSC L2/3 neurons may allow them to respond more sensitively to multiple SWR chains and facilitate the propagation of hippocampal…”

“The limited duration of SWRs could be a way of constraining themaximallength (horizon)of optimisingfor thesequential structure of replay 43 , and indeed extending the duration of SWRs has been shown to lead to improved memory performance 44 .”

“Replay in the rat hippocampus coincides with high-frequency " ripple " oscillations, which do not last long enough to represent long treks through the rat's environment, but, as shown by Davidson et al. (2009), are composed combinatorially, thus altering the behavioral meaning of the entire event.”

“For example, in hippocampal CA3, sequential firing of neurons on the timescale of 100–300 ms (or up to (cid:2) 500 ms in extended replay; Davidson et al., 2009) reoccurs during behavior and during periods of quiescence (replay or re-activation, and preplay; Na´dasdy et al., 1999; Louie and Wilson,…”

“, 2009), the hippocampus (Nádasdy et al., 1999; Pastalkova et al., 2008; Louie and Wilson, 2001; Davidson et al., 2009; MacDonald et al., 2013) and the HVC area in songbirds (Hahnloser et al.”

“…occur when an animal is resting (i.e., sleeping, eating, drinking, or pausing) and have been found to replay rats’ past trajectories through a maze (Davidson et al., 2009; Foster & Wilson, 2006) and to preplay possible future trajectories (Dragoi & Tonegawa, 2011, 2013), including paths that…”

“Carr et al. (2012) did not distinguish between forward and reverse replay, but it is likely that most of their measurements were taken during forward replay events, considering that forward replay occurs more often than reverse replay (Diba and Buzsáki, 2007; Davidson et al., 2009).”

“2007; Karlsson & Frank 2009; Davidson et al, 2009; Gupta et al, 2010; Wu et al, 2017), suggesting a role for these firings in representing the experienced sequence of the location.”

“During periods of wakefulness, place cells exhibit rapid, sequenced reactivations known as awake replays 63 – 67 , which have been linked to planning 66,68 and structural inference 69 .”

“The hippocampus, forming and replaying sequences of place representations (Davidson et al., 2009), may be in a position to retrieve a sequence linking the animal’s present location or situation with that of a future location or situation.”

“... techniques have been developed and widely used in many electrophysiological research studies (Wilson & McNaughton, 1993; Riehle, Grun, Diesmann, & Aertsen, 1997; Chapin, Moxon, Markowitz, & Nicolelis, 1999; Hampson, Simeral, & Deadwyler, 1999; Kudrimoti, Barnes, & McNaughton, 1999; Laubach, Wessberg, & Nicolelis,…”

“versions of place cell sequences that correspond to preceding trajectories of the animals, particularly during sharp-wave ripples, has been reported (Lee and Wilson, 2002; Diba and Buzsaki, 2007; Davidson et al., 2009).”

“40,43,52,53 Similarly, fPRAT has a sequential structure where clockwise visits can be reinforced at six spatially distinct ports with variable reward contingencies.”

“ORIGINAL RESEARCH ARTICLE published: 24 February 2014 doi: 10.3389/fncir.2014.00011 Information-geometric measures estimate neural interactions during oscillatory brain states”

“In particular, hippocampal recordings in rats indicate that brief sequences of prior experience are replayed both in the awake resting state and during sleep, both of which conditions are linked to memory consolidation and learning (Foster & Wilson, 2006; Davidson et al., 2009; Gupta et al., 2010).”

“…reactivation of a large proportion of place cells within a short time window (more than typically occurs during active behavior), a substantial increase in multiunit activity during immobility also provides a reasonable criterion for detecting candidate replay events (Davidson et al., 2009).”

“Hippocampal neuronal ensembles depict de-novo linear trajectories during sleep and awake rest after sphere-rearing During sleep and rest, neuronal sequences replay experienced 19,25,26 and preplay future novel 9,10 extended linear animal trajectories in a time-compressed manner.”

“2nd column: An example of hippocampal ensemble spikes during a post-SWS candidate event detected from hippocampal ripples, and decoded spatial or state sequences from a receptive-field based decoding method (3rd column, [7, 9]) and our proposed unsupervised HDP-HMM method (4th column).”