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.”

“The particular ‘‘pauses’’ in the Purkinje cell firing to the deep cerebellar nuclei could be facilitated by the 4–12 Hz rhythm across the cerebellar cortex (De Schutter and Steuber, 2009), favoring synchronicity of firing towards the nuclei (Jaeger, 2011).”

“Unlike the extended reactivations of Davidson et al. (2009), the putative VTE sweeps of Johnson and Redish (2007) were not associated with SW-R events.”

“In particular, sequential replay of nonlocal trajectories during sharp-wave ripples in the Preprint hippocampal place cell system [1, 2, 3, 4, 5, 6] (and similar events else-where [7, 8, 9]) serve as a tantalizing example suggesting some kind of navigation-related computation [10, 5, 11, 12, 13,…”

“9, 13 , These replay occur rapidly ( 150– 29 Edward Tolman wrote, ‘‘ Learning what to avoid . may occur exclusively during the period after the shock ’’ .”

“Longer duration events are increased during demanding mnemonic tasks and are thought to facilitate the transfer of more relevant information possibly via increasing the number of embedded ripple events [56, 57].”

“The response of a population of place cells hence encodes the position of an animal in an environment and a spatial trajectory of this animal is represented by a sequence of active place cells (e.g. Dragoi and Buzsáki 2006; Davidson et al. 2009).”

“An additional, possibly clearer analysis would have been the prediction of the objects’ locations based on the recall responses (or similarity scores), similar to an analysis by Davidson et al. (2009).”

“On the further supposition that retrospective inference is implemented using filtering and smoothing as described above, this leads to the hypothesis that forward and backward sweeps through recently encountered states, as are known to occur in the hippocampus (Diba and Buzsáki, 2007; Pastalkova et al., 2008; Davidson…”

“Because replays have a characteristic speed of approximately 10 m/s [10], we define our continuous state transition (not to be confused with the continuous trajectory state) as:”

“Moreover, during periods of inactivity, although the replay of either of these sequences in the hippocampus is known to occur in both the forward and reverse direction, forward replay is significantly more frequent than reverse replay (Diba and Buzsáki, 2007; Davidson et al., 2009), thus again avoiding the collapse of…”

“760 Theta Sequence Validation: Sequence Scores 761 For every putative theta sequence and every trajectory decoding template, the slope/line 762 fitting procedure from (Davidson et al., 2009; Kloosterman et al., 2014; Feng et al., 2015) was 763 used.”

“For replay analysis 73,74 , we identified candidate events during post-maze NREM sleep as intervals in which the population firing rate exceeded 2 s.d. above the mean.”

“Both of these solutions are partially inspired by some features of the hippocampal episodic memory in biological systems, in particular the known phenomenon of the acquisition, retention and replay of stored behavioural sequences 16 .”

“Replay of exploration-associated hippocampal activity during rest is an important aspect of spatial learning (Davidson et al., 2009; Karlsson and Frank, 2009; Skaggs and McNaughton, 1996).”

“…of the filtered LFP. Spikes that occurred during the SWR and during the 250 ms before and after the ripples were classified as SWR spikes because population spiking related to SWRs (such as replay events) often extends before and after the SWR itself (Davidson et al. 2009; Dragoi and Tonegawa 2011).”

“…to the transfer and integration of information from the hippocampus to the neocortex that yields memory consolidation (McClelland et al., 1995; Davidson et al., 2009; Gupta et al., 2010; Klinzing et al., 2019), with some recent models suggesting replay’s time-compressed nature plays a core…”

“…expert and lesioned expert mouse. k. Average movement variability (standard deviation from mean trajectory) across the four subsequence trajectories for novice mice (n = 8 mice, n = 18 sessions) and expert mice before and after lesion to DLS (paired t-test; p = 0.0085, n = 5 mice). decoding 35-38 .”

“More recent approaches involve using either decoding to determine whether the place cell sequence represents a meaningful trajectory (Karlsson & Frank, 2009; Davidson, Kloosterman, & Wilson, 2009) or use of high-throughput temporal data mining algorithms (Laxman, Sastry, & Unnikrishnan, 2007).”

“It is shown that trajectory episodes are functionally similar to the SWR associated events and are repeating episode sequences (replay) [5,6,9,10].”

“The presence of the animal at a goal location is associated with awake SWR-associated hippocampal replay events that include (Davidson et al., 2009; Diba & Buzsáki, 2007; Foster & Wilson, 2006; Pfeiffer & Foster, 2013), but are not limited to, representations of immediate past and future…”

“…wave ripple complexes consisting of transient, brief, high-frequency network oscillations), a phenomenon known as hippocampal replay (Carr et al., 2011; Davidson et al., 2009; Diba & Buzsáki, 2007; Foster & Wilson, 2006; MacDonald et al., 2011; O'Keefe & Dostrovsky, 1971; Pfeiffer & Foster, 2013).”

“Time-compressed versions of these sequences are also seen during hippocampal sharp-wave ripple (SWR) events (Lee and Wilson, 2002; Foster and Wilson, 2006; Davidson et al., 2009; Karlsson and Frank, 2009).”

“They may also reflect synaptic reorganization that occurs during behavior (Foster and Wilson, 2006; Csicsvari et al., 2007; Davidson et al., 2009; Atherton et al., 2015; Buzsáki, 2015; Ambrose et al., 2016; Deng et al., 2016; Cazin et al., 2020), although some findings have challenged that hypothetical role of reactiv…”

“[ 96 ]).”

“…at speeds above 5 cm/s (RUN), because previous studies have demonstrated that the hippocampal neurons had very different response profiles when the animal was resting or moved at very slow speeds (STOP) (Ahmed and Mehta, 2012; Davidson et al., 2009; Geisler et al., 2007; Ólafsdóttir et al., 2017).”

“…to replay activity patterns observed during previous spatial navigation experiences ( Foster and Wilson, 2006 ; O’Neill et al., 2006 ; Diba and Buzsáki, 2007 ) and can even be predictive of activity during future experiences ( Davidson et al., 2009 ; Gupta et al., 2010 ; Karlsson and Frank, 2009 ).”

“This might be related to observations in rodents showing that hippocampocortical replay occurs not only during sleep but also during awake rest and consummatory behaviours (Foster and Wilson, 2006; Davidson et al., 2009; Karlsson and Frank, 2009).”

“Moreover, temporally extended or increasingly rich experiences could be represented by multiple concatenated subsequences 93,139,165 and spiking sequences may also be used to selectively activate specific dendritic segments, shifting the locus of computation in human neurons to the dendrite 166,167…”

“We quanti fi ed replay fi delity, duration, and temporal compression of each replay event using protocols similar to previously published procedures (Davidson et al., 2009; Karlsson and Frank, 2009; Hwaun and Colgin, 2019).”

“…suggesting that the hippocampus processes temporal order information during sequence learning irrespective of the nature of the items (e.g., letters, odors, objects and movements; [15,16,18,27] and the type of memory (i.e., motor versus non-motor: [15,16]; spatial versus non-spatial: [28,29]).”

“…trajectories during extended SPW-R events are not predictive of upcoming path and that reverse replay events do not preferentially reflect the path just taken by the animal (Davidson et al., 2009) are also consistent with an interpretation that is not directly linked to spatial trajectories.”

“A replay score that represents the estimated likelihood of an experienced trajectory by using a linear fitting algorithm was calculated as previously described (Davidson et al., 2009).”

“In our model, SWRs occur stochastically, with long stochastic pauses in between packets of events, consistent with in vivo findings (Davidson et al. 2009).”

“…spatial representations suggestive of the planning of specific paths within a cognitive map (Johnson and Redish, 2007; Diba and Buzsáki, 2007; Davidson et al., 2009; Karlsson and Frank, 2009; Pfeiffer and Foster, 2013; Wikenheiser and Redish, 2015; Mou et al., 2022; Widloski and Foster,…”

“This decoder reliably estimated the animal’s position (with a median error of 9.0 cm, and 95% CI of 8.2 − 9.8 cm), comparable to results from prior studies [Davidson et al., 2009, Farooq and Dragoi, 2019].”

“We found that the decoded position closely tracks the animal ’ s actual position ( fi vefold cross-validation; with the distance difference between the actual and decoded location having a median of 9.0 cm, and 95% CI of 8.2 − 9.8 cm), which is comparable to previous studies 35,82 .”

“48,49 Consistent with these works in rodents, SPW-Rs in humans are strongly suggested to play an important role in the initiation of self-generated recall events with anticipation.”

“Place cells exhibit multiple place fields in a large-scale environment (Fenton et al. 2008; Kjelstrup et al. 2008; Davidson et al. 2009; Rich et al. 2014).”

“Previously stored information reactivation is strongly observed during SPWRs in immobile state, slow-wave sleep [10,11] and rarely during searching [12,13].”

“Such correlates include but are not limited to measurements of spatial navigation (O’Keefe and Dostrovsky, 1971; O’Keefe and Nadel, 1978; Wilson and McNaughton, 1993) and decision-making (Foster and Wilson, 2006; Csicsvari et al., 2007; Diba and Buzsáki, 2007; Davidson et al., 2009; Karlsson and Frank, 2009; Gupta et…”

“Clearly, our analysis is best-suited to identify mesoscopic interactions that are related to the generation of sustained rhythms, of sequences of burst events and, generally, of large irregular activity (Davidson et al., 2009; Palmigiano et al., 2017; van Ede et al., 2018; Fernández-Ruiz et al., 2019; Zich et al., 202…”

“Examples for such intrinsic activities are the recurring sequences of neuronal activity patterns in the hippocampus (Wilson and McNaughton, 1994; Nadasdy et al., 1999; Lee and Wilson, 2002; Davidson et al., 2009); see Buhry et al. (2011); Wikenheiser and Redish (2012) for review.”

“…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;…”