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.”

“Previous studies have taken advantage of the joint tuning of many CA1 cells to running direction and location on the linear track (McNaughton et al., 1983; Muller et al., 1994) to demonstrate that spiking sequences can be replayed in either the forward or reverse temporal order (Diba and Buzsáki, 2007; Foster and Wil…”

“Hippocampal replay has been proposed to contribute to memory consolidation during sleep (Buzsáki, 1989; Marshall and Born, 2007; Stickgold, 2005).”

“To determine if significant replay events represented forward or reverse replay, we computed a ‘‘replay order’’ score as the difference between the mean likelihoods that the estimated running direction on the trajectory was in the same or opposite direction as the actual replayed trajectory (see Supplemental Experimen…”

“Such trains have been noted since the first reports of ripples (Buzsáki et al., 1983; O’Keefe and Nadel, 1978; Suzuki and Smith, 1987), but no function has previously been ascribed to this phenomenon.”

“…occur during periodic increases in neocortical population activity (‘‘up states’’) (Battaglia et al., 2004; Clemens et al., 2007; Mölle et al., 2006; Sirota et al., 2003) associated with slow oscillations in the cortical EEG (Isomura et al., 2006; Steriade, 2006; Wolansky et al., 2006).”

“In this respect, awake replay is similar to sequence reactivation during slow-wave sleep (Ji and Wilson, 2007; Lee and Wilson, 2002).”

“During pauses in locomotion and during slow-wave sleep, many place cells are recruited in intermittent population bursts, which are accompanied by ripples in the hippocampal local field potential (Buzsáki et al., 1992; Chrobak and Buzsáki, 1996).”

“There are significantly more remote replay events than the number of false positives expected to be generated by our replay detection procedure (52 of 1656 events; p < 10 11 under a binomial distribution, using false-positive rate of 1%).”

“These effects each lasted 50 ms, which is comparable to the duration of single sharp-wave ripple complexes as described previously (Ylinen et al., 1995).”

“Previous studies have taken advantage of the joint tuning of many CA1 cells to running direction and location on the linear track (McNaughton et al., 1983; Muller et al., 1994) to demonstrate that spiking sequences can be replayed in either the forward or reverse temporal order (Diba and Buzsáki,…”

“…sleep, cortical inputs may bias or otherwise influence memory reactivation (Ji and Wilson, 2007), given the complex bidirectional interactions between the hippocampus and neocortex (Isomura et al., 2006; Mölle et al., 2006; Siapas and Wilson, 1998; Sirota et al., 2003; Wolansky et al., 2006).”

“…with weak place-related firing (peak rate in tuning curve <3 Hz), leaving 47, 34, 23, 32, and 21 spatially tuned single units in rats 1–5 (cluster quality measures: L ratio 0.12 ± 0.17; isolation distance 17 ± 9; calculated using peak amplitude on each channel [Schmitzer-Torbert et al., 2005]).”

“We reasoned that during reactivation of previous experience the position estimate would deviate systematically from the actual position (Johnson and Redish, 2007).”

“We also observed many significant replay trajectories that began at remote locations (Figure 3F; see examples in Figures 3B, 4C, and 4D).”

“Replay events have consistently been found to co-occur with ripple oscillations in the hippocampal local field potential (Diba and Buzsáki, 2007; Foster and Wilson, 2006; Ji and Wilson, 2007; Lee and Wilson, 2002; Nádasdy et al., 1999).”

“…sleep, cortical inputs may bias or otherwise influence memory reactivation (Ji and Wilson, 2007), given the complex bidirectional interactions between the hippocampus and neocortex (Isomura et al., 2006; Mölle et al., 2006; Siapas and Wilson, 1998; Sirota et al., 2003; Wolansky et al., 2006).”

“…replayed spatial memory sequences, we employed a probabilistic neural decoding strategy to estimate the animal’s position on the track from the ensemble of spike trains (Brown et al., 1998; Wilson and Neuron 63, 497–507, August 27, 2009 ª2009 Elsevier Inc. 497 McNaughton, 1993; Zhang et al., 1998).”

“Hippocampal replay has been proposed to contribute to memory consolidation during sleep (Buzsáki, 1989; Marshall and Born, 2007; Stickgold, 2005).”

“There are significantly more remote replay events than the number of false positives expected to be generated by our replay detection procedure (52 of 1656 events; p < 10 11 under a binomial distribution, using false-positive rate of 1%).”

“During pauses in locomotion and during slow-wave sleep, many place cells are recruited in intermittent population bursts, which are accompanied by ripples in the hippocampal local field potential (Buzsáki et al., 1992; Chrobak and Buzsáki, 1996).”

“…replayed spatial memory sequences, we employed a probabilistic neural decoding strategy to estimate the animal’s position on the track from the ensemble of spike trains (Brown et al., 1998; Wilson and Neuron 63, 497–507, August 27, 2009 ª2009 Elsevier Inc. 497 McNaughton, 1993; Zhang et al., 1998).”

“One possible mechanism for the generation of trains of subsequences is provided by the re-entrant loops in the hippocampal-entorhinal circuitry (Canto et al., 2008; Kloosterman et al., 2004).”

“Interestingly, groups of ripples are also present during slowwave sleep, where they predominantly occur during periodic increases in neocortical population activity (‘‘up states’’) (Battaglia et al., 2004; Clemens et al., 2007; Mölle et al., 2006; Sirota et al., 2003) associated with slow oscillations in the cortical…”

“…sleep, cortical inputs may bias or otherwise influence memory reactivation (Ji and Wilson, 2007), given the complex bidirectional interactions between the hippocampus and neocortex (Isomura et al., 2006; Mölle et al., 2006; Siapas and Wilson, 1998; Sirota et al., 2003; Wolansky et al., 2006).”

“…studies have taken advantage of the joint tuning of many CA1 cells to running direction and location on the linear track (McNaughton et al., 1983; Muller et al., 1994) to demonstrate that spiking sequences can be replayed in either the forward or reverse temporal order (Diba and Buzsáki, 2007;…”

“…are also present during slowwave sleep, where they predominantly occur during periodic increases in neocortical population activity (‘‘up states’’) (Battaglia et al., 2004; Clemens et al., 2007; Mölle et al., 2006; Sirota et al., 2003) associated with slow oscillations in the cortical EEG…”

“…sleep, cortical inputs may bias or otherwise influence memory reactivation (Ji and Wilson, 2007), given the complex bidirectional interactions between the hippocampus and neocortex (Isomura et al., 2006; Mölle et al., 2006; Siapas and Wilson, 1998; Sirota et al., 2003; Wolansky et al., 2006).”

“…structure of replayed trajectories in a statistically rigorous manner and makes optimal use of the spatial information contained in hippocampal spikes, including the activity of cells with irregularly shaped place fields (such as those with multiple firing fields [Fenton et al., 2008]; Figure S8).”

“This last possibility, while speculative, is lent some support by the recent finding of specific reactivation of hippocampal neurons during free recall in humans (GelbardSagiv et al., 2008) and by specific activation of the hippocampus during sequence recall tasks in humans (Lehn et al., 2009).”

“There are significantly more remote replay events than the number of false positives expected to be generated by our replay detection procedure (52 of 1656 events; p < 10 11 under a binomial distribution, using false-positive rate of 1%).”

“We used a variation of Skaggs’ (Skaggs et al., 2007) ripple-detection procedure, which allows for the detection of closely spaced ripples.”

“Such trains have been noted since the first reports of ripples (Buzsáki et al., 1983; O’Keefe and Nadel, 1978; Suzuki and Smith, 1987), but no function has previously been ascribed to this phenomenon.”

“One possible mechanism for the generation of trains of subsequences is provided by the re-entrant loops in the hippocampal-entorhinal circuitry (Canto et al., 2008; Kloosterman et al., 2004).”

“Previous studies have taken advantage of the joint tuning of many CA1 cells to running direction and location on the linear track (McNaughton et al., 1983; Muller et al., 1994) to demonstrate that spiking sequences can be replayed in either the forward or reverse temporal order (Diba and Buzsáki, 2007; Foster and Wil…”

“…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).”

“In larger experimental environments, both forward and reverse replay can occur over multiple SW-R events thereby covering longer distances (268).”

“However, we now know that reactivations occur outside of sleep, i.e., in quiet wakefulness (Davidson et al., 2009; Diba and Buzsáki, 2007; Foster and Wilson, 2006; Karlsson and Frank, 2009; Kudrimoti et al., 1999), during initial learning (Singer et al., 2013), and during many states of cortical…”

“(Davidson et al., 2009; Wu and Foster, 2014), and the needed SPW-R clusters were prevented by the light stimulus.”

“…assembly replay during rest and sleep occurs in snippets and is faster, often compressed by at least a factor of ten compared to the behavioral timescale of neuronal activation (Davidson et al., 2009; Diba andBuzsáki, 2007; Euston et al., 2007; Foster and Wilson, 2006; Nádasdy et al., 1999).”

“, 2010) and animals (Louie and Wilson, 2001; Foster and Wilson, 2006; Karlsson and Frank, 2009; Davidson et al., 2009) have shown that hippocampal neuronal ensembles ‘‘replay’’ specific event representations following learning.”