Replay and Time Compression of Recurring Spike Sequences in the Hippocampus

“Rapid reinstatement of the spatiotemporal patterns of pyramidal cell activity in the CA3–CA1 regions and deep layers of the entorhinal cortex (Chrobak and Buzsaki, 1994, 1996) is hypothesized to transfer the stored representations in the hippocampus to neocortical networks (Buzsáki, 1989; Wilson and McNaughton, 1994;…”

“, 1996; Marder and Calabrese, 1996) and vertebrate (Strehler and Lestienne, 1986; Ts’o et al., 1986; Vaadia and Abeles, 1987; Eckhorn et al., 1988; Gray and Singer, 1989; Frostig et al., 1990b; Aertsen et al., 1991; Abeles et al., 1993; Riehle et al., 1997) brains.”

“…on individual pyramidal neurons and their network interactions suggest that pyramidal cells are equipped with intrinsic oscillatory properties (Llinás, 1988; Leung and Yim, 1991; Kamondi et al., 1998) and are embedded in an oscillatory network of interneurons (Buzsáki and Chrobak, 1995;…”

“If the dynamics of cortical neurons could be described by a Poisson process (Bair and Koch, 1996; Shadlen and Newsome, 1998), then within-spike-train randomization of spike occurrences would be appropriate because this procedure does not alter the average firing rate of the individual neurons.”

“Several explanations have been proposed on theoretical grounds, including frequency coding (Sherrington, 1906; Eccles, 1957; Barlow, 1972; Georgopoulos et al., 1982), temporal coincidence coding (von der Malsburg and Bienenstock, 1986; Singer, 1993), temporal delay of spikes (O’Keefe and Recce,…”

“By now, multiple studies have shown that during many sharp-wave ripple-associated PBEs, hippocampal ‘place cells’ (O’Keefe and O’Keefe, 1976) fire in compressed sequences that reflect the firing order determined by the sequential locations of their individual place fields (Diba and Buzsáki, 2007; Foster and Wilson, 20…”

“Although evidence of replay was obtained in the hippocampus (Nadasdy et al. 1999; Skaggs and McNaughton 1996; Wilson and McNaughton 1994; reviewed in Sutherland and McNaughton 2000), whether hippocampal-driven activity is relayed by the perirhinal cortex back to neocortical storage sites has never…”

“Indeed, replay during sleep in rodents can be temporally compressed by a factor of 20 37,38 and recent evidence in humans also suggests temporal compression is at play, at least during wake 39,40 .”

“These sequences are replayed, at faster pace, during subsequent sleep or inactive wakefulness (Wilson and McNaughton, 1994; Nadasdy et al., 1999; Foster and Wilson, 2006).”

“Comparison of spontaneous neural activity to activity recorded at other times in the context of observable behavior is statistically challenging, and criteria for which analysis techniques apply and how to assess statistical significance is under active investigation (e.g., Nadasdy et al. 1999).”

“Later studies extended these findings to show that place cells that fired sequentially during waking behaviors were later replayed in the same order during sharp wave-ripples in sleep (Nádasdy et al., 1999; Lee and Wilson, 2002).”

“The existence of interesting types of neuronal activity, such as patterned firings, synchronization, oscillation, and global state transitions has been revealed by multielectrode recording and calcium imaging (Nadasdy et al., 1999; Cossart et al., 2003; Ikegaya et al., 2004; Fujisawa et al., 2006; Sakurai and Takahash…”

“…or, separately, described the phenomenon of temporal sequence replay during awake resting (Foster and Wilson, 2006; Diba and Buzsaki, 2007; Davidson et al., 2009; Karlsson and Frank, 2009) or post-Run sleep (Nadasdy et al., 1999; Lee and Wilson, 2002; Ji and Wilson, 2007; Karlsson and Frank, 2009).”

“Pyramidal cell firing during HC-SWR tends to reproduce the spatio-temporal patterns established during the preceding active periods; this “replay” is hypothesized to guide cortical activity as it consolidates memories (Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Nádasdy et al., 1999).”

“The latter are supposed to be generated by CA3 pyramidal cells (Behrens, van den Boom, de Hoz, Friedman, & Heinemann, 2005) and may reflect sequence replay (Wilson & McNaughton, 1994; Nádasdy et al., 1999; Lee & Wilson, 2002) occurring in timeslices of about 5 ms.”

“These sequences share striking similarities with those produced during replay events in mammalian hippocampus (Diba and Buzsáki, 2007; Foster and Wilson, 2006; Nádasdy et al., 1999) and in song-generating circuits in zebrafinch high vocal center (HVC; Hahnloser et al.”

“Recurring patterns of action potentials can either be generated as independent trains or a flow of activity from one neuron to another in the chain of synaptic connections [2, 26, 30, 35].”

“Such a mechanism could underlie the phenomenon of hippocampal replay during sharp-wave ripple events, in which previously experienced sequences of place cell-activity can reactivate on significantly temporally compressed timescales (57).”

“During rest periods, sharp-wave ripples (SWRs; 150–250 Hz) in the HP local field potential (LFP) occur concurrently with patterns across populations of HP neurons that depict trajectories through explored space, termed “replay” (Nádasdy et al., 1999; Foster and Wilson, 2006; Karlsson and Frank, 2009; Foster, 2017).”

“Along this line of reasoning, our results agree with concepts of sequence memory pinpointing that sequence structure is preserved during replay in the sleep state although it can occur at a faster rate than during waking [6,23,28,29].”

“The methods consist in randomly shifting individual spikes (Date et al., 1998; Nadasdy et al., 1999; Hatsopoulus et al., 2003; Shmiel et al., 2006; Stark and Abeles, 2009), patterns of spikes (Harrison and Geman, 2009), or the whole spike train (Perkel et al., 1967; Pipa et al., 2008) by an amount…”

“Indeed, a large number of studies have confirmed the reactivation of waking neuronal activity patterns during sleep, particularly during SWRs [5,9–12].”

“6, 8, 9 and 10).”

“On average 10% of pyramidal cells are active in any given ripple, and their spikes are locked to the trough of each the oscillations within a ripple event [25, 26].”

“The one normal circumstance in which prolonged action potential bursts occur frequently in hippocampal neurons in the rat is during sleep (Nadasdy et al. 1999); however, even these episodes are transient and, outside of providing a synchronizing influence, tend to mimic firing patterns that occur…”

“This allows for the repetition of new experiences and enables mechanisms supporting synaptic plasticity (Nadasdy et al. 1999; Buzsaki 2015; Jahnke et al. 2015; Sadowski et al. 2016).”

“Extensive animal research established a tight link between HC SWRs and memory consolidation in both wakefulness and sleep: SWRs accompany the sleep-associated re-activation of HC neuron ensembles that were active during the preceding awake learning experience (Nadasdy et al., 1999; Eschenko et al., 2008; Peyrache et a…”

“Subsequently, during SWS, sharp-wave ripples participate in the reactivation of neuronal networks that were most recently fired during waking, namely those representing declarative information (Pavlides and Winson 1989; Wilson and McNaughton 1994; Skaggs and McNaughton 1996; Kudrimoti et al. 1999; Nadasdy et al. 1999;…”

“In those studies, the temporal firing patterns of multiple neurons during learning are repeated either during sleep (9, 43, 44) or in the awake state (25).”

“Hippocampal place cells sequentially activated during waking on a linear track appear to fire with the same sequential relationship during the ripple events in slow wave sleep [122] [154].”

“intervals (Nádasdy et al. 1999) and the cross-correlation procedure was performed on the pseudo-random sequence.”

“…task also exhibit an increased tendency to fire together during subsequent slow-wave sleep (Wilson and McNaughton, 1994); and spike sequences of pyramidal cells during wheel running are ‘re-played’ during slow-wave sleep, though at a faster timescale than during behavior (Nadasdy et al., 1999).”

“temporal patterns has been observed to occur, both in the cortex and hippocampus, during sleep [16,19,20] and in the awake state [21–24], and it has been hypothesized that this replay may subserve memory consolidation.”

“In both HPC and mPFC, cell assemblies fire in a fine time-resolved manner (Skaggs and McNaughton, 1996; Nadasdy et al., 1999; Lee and Wilson, 2002; Euston et al., 2007; Luczak et al., 2007; Pastalkova et al., 2008; Peyrache et al., 2009; Battaglia et al., 2011).”

“The activity of various cell types is locked to ripple oscillations, but the pace-making mechanisms are unclear, although many in vivo and in vitro studies addressed this question (Ylinen et al., 1995; Draguhn et al., 1998; Nádasdy et al., 1999; Csicsvari et al., 2000; Klausberger et al., 2003, 2005; Maier et al., 200…”

“Consistent with these findings, neuroimaging studies in humans have reported re-activation of the hippocampal and mediotemporal structures during SWS following procedural (Maquet et al., 2000) and declarative (Peigneux et al., 2004) learning, which correlated with performance improvement after sleep (Peigneux et al.,…”

“With the possibility of existence of off-line learning mechanisms during sleep (Deregnaucourt et al. 2005; Margoliash 2001; Nadasdy et al. 1999), we could imagine that auditory hallucination of the BOS originating in NIf is the driving force of such memory consolidation processes.”

“Tools developed in former studies for the analysis of STPs in small populations of neurons (e.g., Prut et al., 1998; Nadasdy et al., 1999) scale poorly with the size of the data and thus cannot be applied to massively parallel spike trains (MPST).”

“This reactivation hypothesis has received considerable support in animal research with regard to the declarative, hippocampal memory system (Wilson and McNaughton, 1994; Nadasdy et al., 1999), but also with regard to other memory systems (Dave and Margoliash, 2000; Ribeiro et al.”

“While it is in line with theoretical concepts described above and in Figure 1 that SO-tDCS over the dorso-lateral PFC during SWS in humans enhanced EEG power both in the SO and spindle frequency ranges (Marshall et al., 2006), effects of SO-tDCS during waking are more difficult to reconcile.”

“During SPW-Rs, spatial memory associated theta sequences, and emotional/social memory correlates have been observed to be reactivated in a time-compressed manner (Nadasdy et al., 1999; Louie and Wilson, 2001; Cei et al., 2014; Girardeau et al., 2017; Oliva et al., 2020).”

“Triple-activation of ensembles across brain region To evaluate simultaneous reactivation across BLA, vCA1 and PL5 ensembles, we expanded CCG analyses for ensemble triplets by using a similar method previously used for spike triplet analyses (Nadasdy et al., 1999).”

“With appropriate increases in replay speed, this circuit could also underlie forward hippocampal replay occurring during slow wave sleep (Skaggs & McNaughton, 1996; Nadasdy et al., 1999) that could drive the replay shown in neocortical structures (Ribeiro et al.”

“…in memory performance is the experience-dependent reactivation of place cell activity patterns representative of previous behavior—previously defined as hippocampal replay (Wilson and McNaughton, 1994; Nadasdy et al., 1999; Louie and Wilson, 2001; Lee and Wilson, 2002; Davidson et al., 2009).”

“With improvements in analysis techniques, it became possible to observe the reactivation of more specific neuronal sequences during sleep that recapitulated awake experience (Skaggs and McNaughton 1996; Kudrimoti et al. 1999; Nadasdy et al. 1999; Lee and Wilson 2002).”

“Sequences of neural activities recorded in the hippocampus of the awake animal are also replayed during subsequent sleep sessions (Skaggs and McNaughton 1996; Nádasdy et al. 1999; Louie and Wilson 2001; Lee and Wilson 2002), giving further support to sequence learning theories.”

“Such local clustering may emerge because during sharp waves selective subgroups of CA3 pyramidal cells discharge together preferentially and consistently (Wilson and McNaughton, 1994; Kudrimoti et al., 1999; Nadasdy et al., 1999; Csicsvari et al., 2000).”

“We developed classifiers to decode visual information content based on the sequence of spiking activity within each burst using a template-matching approach 30,59 .”

“brainics@rs.kagu.tus.ac.jp”

“During slow wave sleep, hippocampal place cell firing sequences observed during recent locomotion will “replay” in a temporally ordered and faster timescale in series of sharp wave bursts (Lee and Wilson, 2002; Nádasdy et al., 1999; Skaggs and McNaughton, 1996; Wilson and McNaughton, 1994).”

“Foremost, the temporal pattern of spikes among small groups of CA1 neurons during sensory experience reoccur in a compressed time frame during subsequent sharp waves (e.g., Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Nadasdy et al., 1999; Hirase et al., 2001; Lee and Wilson, 2002).”

“During subsequent sleep, half of the subjects were re-exposed to the odor during periods of slow wave sleep (SWS), while the other half received odorless vehicle.”

“Single and en masse network recordings from these cells reveal that the firing pattern as well as temporal order is played back on a faster time scale (Nadasdy et al., 1999) during rapid-eye movement (REM) and slow wave sleep (SWS) (Poe et al.”

“A previous study of exact time interval patterns in hippocampal data used even larger bins and found many repeating patterns, but did not focus on patterns with Ն4 distinct cells (Nádasdy et al. 1999).”

“…point at which the regression slope crossed y =0 in the forward mental simulation in the positive tonegative direction (e.g., junction = 5.2 TR), with the 1 st period preceding the junction (e.g., 1 st period = [1, 2, 3, 4, 5] TR) and the 2 nd period following it (e.g., 2 nd period = [6, 7, 8] TR).”

“This idea of complementary functions of SWS and REM sleep for successful memory consolidation was revived by Diekelmann and Born (2010) who suggested an essential role of SWS for system consolidation which is complemented by synaptic consolidation taking place during REM sleep.”

“The spike content of SPW-Rs is organized and sequential, and critically it consists of a temporally compressed version of firing patterns that occur during waking experience 153–155 .”

“ISI shuffling within and across trials (Nádasdy et al. 1999; Masuda and Aihara 2003; Ikegaya et al. 2004), for example, will have similar effects as spike time randomization and trial shuffling respectively, the former flattening the rate profile to a stationary one, and the latter ignoring cross-trial nonstationariti…”

“…by: Tatjana Tchumatchenko, Max Planck Institute for Brain Research, Germany Reviewed by: Robert Rosenbaum, University of Pittsburgh, USA Arvind Kumar, University of Freiburg, Germany Raul C. Muresan, Romanian Institute of Science and Tehnology, Romania *Correspondence: Sven Jahnke,…”

“Spatio-temporal patterns in a more general sense (with different time intervals between spikes) were suggested as signatures of synfire chain activity in data of low numbers of simultaneously recorded neurons [40, 46, 47].”