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,…”

“An equally serious issue is that replays during sleep are comparatively infrequent, are not very faithful to the original, are usually played several times faster, and decline rapidly during the first hour of sleep (Ji and Wilson, 2007; Kudrimoti et al., 1999; Nádasdy et al., 1999).”

“Note that the combination of spatial seconds to seconds (Abeles and Gerstein, 1988; Abeles et al., 1993; Nadasdy et al., 1999), we examined neuralreceptive fields and structured spatial behavior pro- duces a characteristic ordered pattern of ensemble ac- activity at a lower temporal resolution but…”

“We therefore confirm that spike separation is significantly more effective when multiple sites are used for unit recording (Drake et al. 1988; McNaughton et al. 1983; Nadasdy et al. 1998; Recce and O’Keefe 1989).”

“, 2006) and during slow-wave sleep after task performance (Wilson and McNaughton, 1994; Kudrimoti et al., 1999; Nadasdy et al., 1999; Lee and Wilson, 2002).”

“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).”

“Studies in rats have demonstrated the existence of hippocampal cells showing a replay of previous activation patterns during non-REM sleep (Kudrimoti et al., 1999; Nadasdy et al., 1999) and a coordination of hippocampal and neocortical reactivation (Qin et al.”

“…are compressed into the 150 ms sharp wave event than in several seconds of theta (Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Kudrimoti et al., 1999; Nádasdy et al., 1999; Lee and Wilson, 2002), creating opportunities for crossing episodes at the timescale of synaptic plasticity.”

“Complementary studies have shown that entire sequences can be replayed at high speeds14–16, 19.”

“Likewise, in humans, vibratory and neo-cortical cell assemblies during NREM sleep (Hirase et al., 2001; Kudrimoti et al., 1999; Lee and Wilstimulation of the right hand during wakefulness increases delta power in the EEG recorded over the con- son, 2002; Nadasdy et al., 1999; Qin et al., 1999; Skaggs and McNaughton, 1…”

“Pattern separation, pattern completion and replay , which are well-known properties of recurrent neural networks 100,123 , are also found in hippocampal activity 129,130 .”

“…learned neuronal sequences of place fields are spontaneously replayed during immobility and sleep-related sharp wave bursts (Wilson and McNaughton, 1994; Nadasdy et al., 1999; Lee and Wilson, 2002) without extrahippocampal influences at a time scale slightly faster than during a given theta cycle.”

“Evoked and Spontaneous Neocortical Activity precision more often than expected under shuffling manipulations (Abeles, 1991; Ikegaya et al., 2004; Nadasdy et al., 1999).”

“The presumed “reading out” in the SWR is accompanied by compression of the replay (Nadasdy et al. 1999, Euston et al. 2007, Ji & Wilson 2007); in other words, the postulated representation is played in “fast forward” (and, as noted below, under certain circumstances in “fast backward”).”

“Specifically, patterns of neuronal activity that characterize waking behaviors are reactivated during subsequent sleep periods in the hippocampus (Lee and Wilson, 2002; Nádasdy et al., 1999; Pavlides and Winson, 1989; Wilson and McNaughton, 1994) and the cortex (Euston et al.”

“…hippocampus and its hippocampo–neocortical transfer is presumably linked to a sharp wave–ripple pattern in the hippocampus (Kudrimoti et al., 1999; Nadasdy et al., 1999), which at the neocortical level occurs in temporal correlation to sleep spindles, ␦ waves, and their grouping by the slow…”

“Even sequences of three spikes during wheelrunning are repeated in subsequent slow-wave sleep (Nádasdy et al., 1999), and information about the order in which the cells were activated is maintained (Skaggs and McNaughton, 1996).”

“…the theme of pairwise reactivation (Gerrard et al. 2001, Kudrimoti et al. 1999, Skaggs & McNaughton 1996), but arguably the next breakthrough finding was that of sequenced activity across four or more cells matching behavioral sequences (Lee & Wilson 2002, Louie & Wilson 2001, Nadasdy et al. 1999).”

“…is that sleep-associated memory consolidation relies on a replay of recently encoded memories which takes place in hippocampal cells during slow-wave sleep in temporal association with sharp wave–ripples (Kudrimoti et al., 1999; Nádasdy et al., 1999; Rasch et al., 2007; Ji and Wilson, 2007).”

“In both kainic acid- and pilocarpine-induced status epilepticus, as well as a rodent model of febrile seizures, death among CA3 and CA1 pyramidal neurons is common, with CA3 neurons perhaps more vulnerable (Clifford et al., 1987; Nadler et al., 1978; Pollard et al., 1994; Toth et al., 1998).”

“…Ikegaya et al, 2004; Tang et al, 2008; Seidemann et al, 1996; Fujisawa et al, 2008; Crowe et al, 2010; Harvey, Coen & Tank, 2012], hippocampus [Nadasdy et al, 1999; Louie & Wilson, 2001; Pastalkova et al, 2008; Davidson, Kloosterman & Wilson, 2009], basal ganglia [Barnes et al, 2005; Jin,…”

“Importantly, these replay events occurred predominantly during SPWRs [45], in a temporally compressed manner compatible with the typical time windows of synaptic plasticity [46] (note that reactivations were also reported during rapid eye movement sleep at a decelerated rate [47]).”

“We therefore tested the effects of two different uncoupling agents (carbenoxolone and octanol) on SPW–R.”

“[34–36,37 ]).”

“In the hippocampal circuitry, neuronal replay of recently encoded memories occurs in conjunction with ripples typically forming sharp wave–ripple complexes (Nadasdy et al., 1999; Csicsvari et al., 2000; Diba & Buzsaki, 2007).”

“Consistent with this hypothesis, several animal studies have shown that neural activity expressed during waking behavior is reinstated during subsequent sleep (e.g., Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Qin et al., 1997; Nadasdy et al., 1999; Louie and Wilson, 2001).”

“…areas for consolidation as a tightly compressed replay (now over only tens of milliseconds) of essentially the same neuronal firing sequences activated during previous theta states (Qin et al., 1997; Siapas and Wilson, 1998; Kudrimoti et al., 1999; Nadasdy et al., 1999; Lee and Wilson, 2002).”

“…learning-related neural activity, thought to contribute to memory consolidation, has been demonstrated in the hippocampus (Louie and Wilson, 2001; Nadasdy et al., 1999; Wilson and McNaughton, 1994), neocortex (Ji and Wilson, 2007; Ribeiro et al., 2004), and birdsong circuits (Dave and…”

“…is biased by previous experience of the animal (Buzsáki, 1989; Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Kudrimoti et al., 1999; Nadasdy et al., 1999; Lee and Wilson 2002; Foster and Wilson, 2006; O’Neill et al., 2006, 2008; Diba and Buzsáki, 2007; Karlsson and Frank, 2008,…”

“An important point to emphasize here is the fact that this ensemble replay occurs preferentially during the SPW-R episodes (Nadasdy et al. 1999; Kudrimoti et al. 1999, O’Neill et al. 2006).”

“Neurons with overlapping place fields tend to fire together when the animal is located outside the place fields during later periods of sleep (Pavlides and Winson, 1989; Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Nadasdy et al., 1999; Kudrimoti et al., 1999; Louie and Wilson, 2001; Lee and Wilson, 2002;…”

“Indeed, there are indications that organized ensembles of CA3 and CA1 cells fire in SWRs (Nadasdy et al., 1999; Kudrimoti et al., 1999; Csicsvari et al., 2000; Lee and Wilson, 2002, 2004), some correlated with waking neuronal patterns (Kudrimoti et al.”

“Several authors have shown that the temporal sequence of neuronal discharges observed in hippocampal CA1 neurons during spatial exploration is repeated on a faster timescale during SWS (Nadasdy et al., 1999; Shen et al., 1998; Skaggs and McNaughton, 1996).”

“In vivo and in vitro studies (Nádasdy et al., 1999; Csicsvari et al., 2000; Klausberger et al., 2003, 2004, 2005; Maier et al., 2003; Lasztóczi et al., 2011; Lapray et al., 2012; Hájos et al., 2013) revealed the behavior of principal cells and different subtypes of inhibitory neurons during SWRs…”

“Yet, despite the extensive study of ensemble reactivation in hippocampal (Ji and Wilson, 2007; Joo and Frank, 2018; Nadasdy et al., 1999; Wilson and McNaughton, 1994), prefrontal (Peyrache et al.”

“…during sleep has been observed in rodents (Pavlides and Winson 1989; Wilson and McNaughton 1994; Skaggs and McNaughton 1996; Qin et al. 1997; Nadasdy et al. 1999; Louie and Wilson 2001; Lee and Wilson 2002), nonhuman primates (Hoffman and McNaughton 2002), humans (Maquet et al. 2000), and…”

“…the pattern of cells’ spikes corresponding to task-related Hippocampus activity were replayed in the rat hippocampus during both subsequent slow wave (SWS) (Skaggs and McNaughton, 1996; Nadasdy et al., 1999; Lee and Wilson, 2002) and rapid-eyemovement (REM) sleep periods (Louie and Wilson, 2001).”

“…or sleep, hippocampal neurons rapidly replay sequences of firing that were observed during learning (Wilson and McNaughton, 1994; Kudrimoti et al., 1999; Nádasdy et al., 1999), resulting in sharp bursts of hippocampal activity that are less common during periods of exploration (Buzsáki, 1989).”

“Importantly, the ‘content’ of the SPW events is determined by previous experience of the animal (Buzsáki, 1989; Skaggs and McNaughton, 1996; Wilson and McNaughton, 1994; Kudrimoti et al., 1999; Nadasdy et al., 1999; Lee and Wilson, 2002).”

“Importantly, assembly reactivation during SWS occurs, although at a faster speed, in the same temporal order of place cell spiking and in the same forward direction as that observed during wake encoding of the spatial task (Skaggs & McNaughton 1996, Nadasdy et al. 1999, Ji & Wilson 2007).”

“Human [1–4] and animal [5–9] studies have revealed experience-dependent reactivations of regional cerebral”