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,…”

“…wake (Foster and Wilson, 2006; Jackson et al., 2006; Diba and Buzsáki, 2007), and SWS—in both states these replay events are associated with the occurrence of hippocampal sharpwave-ripples (SWRs; Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Nadasdy et al., 1999; Lee and Wilson, 2002).”

“Many more sequences occur in SPW-Rs than could be accounted for by the forward or reverse sequences of experienced place cells (Nádasdy et al., 1999).”

“, 2000; Pavlides and Winson, 1989; Wilson and McNaughton, 1994), which may provide sufficient neuronal depolarization to activate NMDARs (Nadasky et al., 1999).”

“Finally, during sleep, sequences that occurred during wakefulness are replayed (Skaggs & McNaughton 1996; Nadasdy et al. 1999).”

“in establishing a threshold [90–93].”

“…of pattern replay and the preservation of temporal-sequence information displayed by ensembles during behavioural experiences, replay is considered an important candidate mechanism for mediating memory consolidation (Skaggs and McNaughton, 1996; Nadasdy et al., 1999; Lee and Wilson, 2002).”

“Loosing even a few hours of sleep can have detrimental effects on a wide variety of cognitive processes such as attention, language, reasoning, decision making, learning and memory.”

“Compression of a task dependent sequence of firing has been experimentally found in numerous sources ([Euston et al., 2007, Mello et al., 2015, N´adasdy et al., 1999]).”

“Inasmuch as hippocampal output during ripples originates from reactivations of newly encoded memories (Kudrimoti et al., 1999; Nádasdy et al., 1999; Diba & Buzsáki, 2007), its nesting into spindle troughs might support the enduring redistribution of these memories to neocortical circuits…”

“It is during these large-scale high-frequency events that ensembles of neurons ''replay'' the experience-induced patterns (Kudrimoti et al. 1999; Nadasdy et al. 1999; Ji and Wilson 2007; Peyrache, Khamassi, et al. 2009; Johnson et al. 2010).”

“by stereotyped firing sequences within a given neuronal ensemble [10,57-59].”

“For example, temporally structured multicell spiking patterns, organized into frames, were observed in hippocampus and cortex, and were associated to memory traces [4,5].”

“In the second approach, activity in the awake state is used to define an order template, and subsequent sleep firing patterns are searched for sequences matching the order template (Nadasdy et al., 1999; Lee and Wilson, 2002 ).”

“Second, neurons involved in recent waking experience are reactivated during post-training sleep in rodent hippocampus (Pavlides and Winson, 1989; Wilson and McNaughton, 1994; Kudrimoti et al., 1999; Nadasdy et al., 1999; Louie and Wilson, 2001) and in human cortex (Maquet et al., 2000).”

“As discussed, however, 1999; Nadasdy et al., 1999; Hirase et al., 2001; LouieDonchin et al. (2002) described consolidation (as stabiliand Wilson, 2001; Hoffman and McNaughton, 2002; Leezation) for an arm reaching task but were unable to show and Wilson, 2002).”

“[292] Nadasdy Z, Hirase H, Czurko A, Csicsvari J, Buzsáki G.”

“During SWRs, hippocampal cells fire synchronously and their temporally structured spiking can ‘‘replay’’ previous waking experience (Louie and Wilson, 2001; Nádasdy et al., 1999; Wilson and McNaughton, 1994) to support memory and planning (Buzsáki, 2015; Foster, 2017; Joo and Frank, 2018).”

“, 2011) and their sequential activity is often similar to firing sequences of the same neurons during learning and exploration (Wilson and McNaughton, 1994; Kudrimoti et al., 1999; Nádasdy et al., 1999; Lee and Wilson, 2002; Johnson and Redish, 2005; Foster and Wilson, 2006; O’Neill et al., 2006; Diba and Buzsáki, 200…”

“This idea is further substantiated by multiple demonstrations, across many species, that activity related neuronal firing sequences are replayed during sleep (Pavlides & Winson, 1989; Wilson & McNaughton, 1994; Skaggs & McNaughton, 1996; Kudrimoti et al. 1999; Nadasdy et al. 1999; Maquet et al. 2000, 2003; Dave & Marg…”

“In addition, the studies on ensemble reactivation consistently reported that sleepbased sequences were temporally compressed when compared to their corresponding waking sequences (Ji & Wilson, 2007; Lee & Wilson, 2002; N adasdy et al., 1999).”

“Many subsequent studies continued to suggest a consolidation function for replay during sleep [167,168] and during broadly-stationary waking states [169–173], where reverse replay was strikingly clear [170,171,173].”

“, 2003), cerebellum and red nucleus (Kalużny and Tarnecki, 1993) and in primary somatosensory cortex (Rosanova and Ulrich, 2005) of anesthetized cats, as well as in hippocampus of rats (Nádasdy et al., 1999).”

“Neuronal composition of the sharp-wave ripple (SPW-R) is influenced by previous experience (Buzsáki, 1989; Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Kudrimoti et al., 1999; Nádasdy et al., 1999; Lee and Wilson 2002; Foster and Wilson, 2006; O’Neill et al., 2006, 2008; Diba and Buzsáki, 2007; Karlsson a…”

“Rodent studies demonstrate that the sequences of hippocampal place cell activation observed during learning are replayed during postlearning sleep together with a reactivation in neocortical areas (Peyrache et al., 2009; Ji & Wilson, 2007; Nadasdy et al., 1999; Wilson & McNaughton, 1994).”

“Both hippocampal place cells and primary visual cortex cells in rodents reactivate a sequential pattern of the learned route of a maze during NREM [140,141].”

“F or p er so na l u se o nl y. Hippocampal replay: neuronal activity recapitulating that at learning, thought to constitute a readout of stored information as a sequence of place-cell action potentials wake (Nádasdy et al. 1999).”

“There is evidence that high-speed, top-down sequence generation occurs during the spindle stage of sleep [Lee and Wilson, 2002, N´adasdy et al., 1999].”

“During SWRs lasting 30–120 ms, place cells discharge sequentially [82–84] either in the reverse [85] or forward direction [86,87] of their temporal order during awake navigation, depending on the behavioural context.”

“HPC, known as SWRs, contain activity bursts that ‘‘replay’’ temporally compressed patterns of place cell rate modulations.(250,292,293) SWRs have been directly linked to memory performance,(253,294) with those occurring offline proposed to assist memory consolidation into the neocortex.”

“Moreover, the firing sequences of place cells during running behavior are re-expressed at an accelerated rate during subsequent slow-wave sleep (Kudrimoti et al., 1999; Nadasdy et al., 1999; Lee and Wilson, 2002) or quiet awake pauses in locomotion (Foster and Wilson, 2006; Diba and Buzsaki, 2007).”

“…©2004 by Cold Spring Harbor Laboratory Press ISSN 1072-0502/04; www.learnmem.org www.learnmem.org 1994; Skaggs and McNaughton 1996; Qin et al. 1997; Nadasdy et al. 1999; Hirase et al. 2001; Louie and Wilson 2001; Lee and Wilson 2002), nonhuman primates (Hoffman and McNaughton 2002), humans…”

“The algorithm used a recision of 1 ms and a window size T 200 ms, following adasdy et al. (1999). On average, 2993 1077 unique ig.”

“Secondly, certain firing sequences of three or more cells have been observed more than by chance during sleep, and many of these patterns resembled that of waking firing sequences (Nadasdy et al., 1999; Louie & Wilson, 2001; Lee & Wilson, 2002).”

“…approach, where surrogates are not generated by separately modifying the spike trains of individual neurons but by shuffling spikes across neurons within the same trial (Table 1 J ) (Ikegaya et al. 2004; Nadasdy et al. 1999) or by exchanging spikes across neurons (Table 1 K ) (Ikegaya et al. 2004).”

“Furthermore, the prominent role of the hippocampus in spatial functions has been partially attributed to replay, the reactivation of place cell activity patterns representing distant places or even recapitulating coherent trajectories (Foster and Wilson, 2006; Lee and Wilson, 2002; Nádasdy et al., 1999; Wilson and McN…”

“…signi cantly modulated by experimental conditions and thereby may carry information about these experimental conditions that is sensory and or motor signals Information conveyed by a population of ring neurons however may not only be a sum of mean ring rates Other statistical structures embedded…”

“A remarkable success of ensemble recordings was the demonstration that, during sleep, neural patterns of activity appearing in the immediately previous awake experience are replayed (Wilson and McNaughton 1994; Nádasdy et al. 1999; Lee and Wilson 2002; Ji and Wilson 2006).”

“This idea is supported by observations of replay of recently active neural ensemble patterns in hippocampus(Kudrimoti et al., 1999; Nádasdy et al., 1999; Pavlides and Winson, 1989; Skaggs and McNaughton, 1996; Wilson and McNaughton, 1994) and neocortex(Euston et al., 2007; Hoffman and McNaughton,…”

“Replay events, which occur during HPC sharp-wave ripple oscillations, consist of temporally compressed firing of place cell sequences that encode recently visited spatial locations (Lee and Wilson, 2002; Nádasdy et al., 1999; Skaggs and McNaughton, 1996) and are generated locally in the hippocampus (Buzsáki et al.”

“In various guises, jitter and related spike resampling methods are in common use (Abeles and Gat 2001; Amarasingham 2004; Baker and Lemon 2000; Butts et al. 2007; Date et al. 1999; Dragoi and Buzsáki 2006; Fujisawa et al. 2008; Furukawa and Middlebrooks 2002; Gerstein 2004; Grün 2009; Grün et al. 2009; Gütig et al. 20…”

“In support of this idea, there is now much evidence of replay in slow-wave sleep (Pennartz et al. 2002, 2004) and waking (Abeles et al. 1995; Seidemann et al. 1996; Nadasdy et al. 1999) at multiple levels of the central nervous system.”

“It has been claimed that replayed sequences are compressed in time by a factor of about 20 relative to the sensory-driven sequences [73, 63].”

“Tasks with repetitive spatial components have been used to study reactivation of spatially dependent firing patterns during slow-wave sleep (Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Kudrimoti et al., 1999; Nádasdy et al., 1999; Lee and Wilson, 2002).”

“Experimental data suggest that time-compressed replay of the recent trajectory may occur during sharp waves in sleep and wake states (Nadasdy et al. 1999; Louie and Wilson 2001; Lee and Wilson 2002; Buzsaki et al. 2003).”

“…is reactivated during SWS in both the hippocampus (Wilson & McNaughton, 1994; Skaggs & McNaughton, 1996; Kudrimoti, Barnes & McNaughton, 1999; Nádasdy et al., 1999; Hirase et al., 2001; Lee & Wilson, 2002; Pennartz et al., 2002; see also Pavlides & Winson, 1989) and neocortex (Hoffman &…”

“Neuronal firing sequences established during wake are reexpressed only intermittently during rodent NREM sleep, with low fidelity and on a faster timescale than the original experience.(30,31) Similarly, only intermittent fragments of recent episodicmemories appear in sleep mentation, intermingled with remote and sema…”

“The hippocampus stores traces of the details of recent experiences and replays these experiences during non-REM sleep, often within sharp wave ripples (Nádasdy, Hirase, Czurkó, Csicsvari, & Buzsáki, 1999), which are temporally correlated with spindle events in cortex (Staresina et al., 2015).”

“Such reactivation of event-specific activity is known as replay and occurs during brief high-frequency bursts in the hippocampus, that is known as sharp wave-ripples (Karlsson and Frank, 2008; Kudrimoti et al., 1999; Nádasdy et al., 1999).”

“Links to computational models Learning, storing, inferring and executing sequences is a key topic in experimental [71–79], and theoretical neurosciences [80– 82]; and robotics [83–86].”

“Although these methods are not designed to evaluate temporal sequences, we used a 250 ms time window to capture coactivation on the timescale of sharp-wave ripples during which replay sequences are observed (Nádasdy et al., 1999; Buzsáki, 2015).”

“IEEE Trans Biomed Eng 58(5):1216–1223.”