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,…”

“The standard memory replay hypothesis states that patterns of brain activity that occurred during waking states are replayed during sleep and that this replay may be critical for the process of memory consolidation (Louie and Wilson, 2001; Nadasdy et al., 1999; Wilson and Mcnaughton, 1994).”

“For declarative memories, a central component of consolidation is the repeated reactivation of learning-associated neuronal activity patterns originating in the hippocampus (Pavlides and Winson 1989; Wilson and McNaughton 1994; Nádasdy et al. 1999).”

“Many approaches to this problem are supervised, that is, they take patterns occurring concurrently with a known event, such as the delivery of a stimulus for sensory neurons or the traversal of a running track for hippocampal place fields, as a “template” and then search for repetitions of the same template in spiking…”

“The pivotal role of SWRs in the process of memory consolidation is supported by studies showing that SWRs can replay neuronal activity that which contain information about recent active behavior (Kudrimoti et al.,1999; Nádasdy et al., 1999; Lee andWilson, 2002).”

“001), while flexible units carry more information in spike timing compared to rigid units (t(5) = 7.”

“These fi ndingshavebeen interpretedin termsofalocalreorganization of synaptic weight distributions as a result of repeated activation with an input sequence 7,34,35,37,38 .”

“Structures in birds, such as area HVC, that apparently sequence song [55], or the hippocampus of rodents with its rich forms of on-line and off-line activation of neurons in behaviourally-relevant sequences [56, 57], or the temporal pole and posterior orbitofrontal cortex of humans [58], whose activity apparently incr…”

“…replay of premotor bursts has been observed in RA (Dave and Margoliash, 2000) and may play similar roles in other systems (Wilson and McNaughton, 1994; Qin et al., 1997; Nadasdy et al., 1999; Hoffman and McNaughton, 2002; Pennartz et al., 2004; Ji and Wilson, 2007; Peyrache et al., 2009).”

“…patterns, sleep and cognitive function (Pavlides and Winson, 1989; Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Kudrimoti et al., 1999; Nadasdy et al., 1999; Peigneux et al., 2004; Foster and Wilson, 2006; Diba and Buzsaki, 2007; Ji and Wilson, 2007; O'Neill et al., 2008; Davidson et…”

“…methods (Luczak et al. 2007; Sakata and Harris 2009) and were further characterized by identifying temporally precise spike sequences, which have been proposed as a signature for the flow of activity within neural networks (Abeles and Gerstein 1988; Sun et al. 2010; Nadasdy et al. 1999).”

“, 1999; Lee & Wilson, 2002) and were generally implied to represent a replay of a previous similar experience when expressed before a now familiar environment (Kudrimoti et al., 1999; Nadasdy et al., 1999).”

“…the patterns of activity during the preceding waking period more than expected by chance, but unlike the reactivation during REM, the reactivation during LIA is highly compressed in time (Nádasdy et al. 1999; Pavlides and Winson 1989; Skaggs and McNaughton 1996; Wilson and McNaughton 1994).”

“This result was later extended (Skaggs and McNaughton, 1996; Kudrimoti et al., 1999; Nadasdy et al., 1999; Lee and Wilson, 2002) to include the key concept of reactivation, that assemblies of cells can fire during slow wave and REM (Louie and Wilson, 2001) sleep in the same temporal order they…”

“Several researchers have also reported spike patterns at a coarser timescale in the cortex, on the order of 25+ msec (Nadasdy et al., 1999; Hahnloser et al., 2002).”

“However, debates leading up to 2011 revolved around whether hippocampal activity during the sleep or rest preceding a re-exposure to a familiar context was correlated 31,61 or not 30 with the activity patterns that would be re-expressed during that re-exposure.”

“More importantly, only a small subset of pyramidal neurons are active during individual SPW-ripple events 15 .”

“PE occurrence is independent of prior events at the timescale of seconds Assembly occurrence in brain regions other than the visual cortex, such as hippocampus, has been associated with replay of past events and other memoryrelated phenomena (Wilson and McNaughton, 1994; Nádasdy et al., 1999; Lee and Wilson, 2002; Gir…”

“, the discharge probability increases independent of whether a neuron is part of a spatiotemporal spike sequence or not”, as suggested for ripple busts (40, 52).”

“The experience-specific reactivation is strongest during SPW-Rs in slow-wave sleep and quiet wakefulness (Kudrimoti et al., 1999; N adasdy et al., 1999), and in the occasional SPW-Rs during exploration (O’Neill et al., 2006; Davidson et al., 2009).”

“correlated with activity in those same areas during subsequent slow wave sleep (SWS), suggesting a replaying of events to strengthen memories (Ji and Wilson, 2007; Nádasdy et al., 1999; Pavlides and Winson, 1989; Skaggs and McNaughton, 1996; Wilson and McNaughton, 1994).”

“The propagation of neural spiking activity has been observed in various parts of the brain, including neocortex (Mao et al., 2001; Ikegaya et al., 2004; Pinto et al., 2005) and hippocampus (Miles et al., 1988; Nádasdy et al., 1999; Buhry et al., 2011; Cheng, 2013).”

“realized by local feed-forward structures [13,14,16,60], possible”

“fragments of sequential activation (Wilson and McNaughton, 1994; Nádasdy et al., 1999; Lee and Wilson, 2002; Pfeiffer and Foster, 2013).”

“The spike sequences recorded in the awake animal appear to be ‘replayed’ on a faster time scale during sleep which may serve to consolidate information [66, 82, 95].”

“Other techniques, such as chronically implanted multielectrode arrays [21] and optogenetics [22] enable recording and control, respectively, of large numbers of neurons in deep regions of the brain [23, 24].”

“Second is the replay/preplay phenomenon (Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Nádasdy et al., 1999; Diba and Buzsáki, 2007; Pastalkova et al., 2008; Girardeau et al., 2009; reviewed by Carr et al., 2011; Figure 10), where there is a relation between firing sequences of…”

“In this study we are concerned with possibilities of inducing deep temporal structures without fading memory in recurrent networks of spiking neurons.”

“The activity generated during waking in the hippocampus is reproduced in sequence during rapid eye movement (REM) sleep with the same time scale as the original experiences, lasting tens of seconds to minutes (Louie & Wilson, 2001), or is compressed during slowwave sleep (Nádasdy et al. 1999).”

“…also facilitate involvement of the particular PCs in neuronal ensemble reactivation and depolarization of specific downstream CA1 targets during the animal’s rest cycle and period of sharp waves in the HC electroencephalogram (Csicsvari et al. 1999; Kudrimoti et al. 1999; Nadasdy et al. 1999).”

“SWR are oscillatory events that coincide with the replay of previously encoded information (N ´ adasdy et al., 1999) (Fig.”

“…result, the output pattern sequences of the CA3 are similar in both theta and SPW states (Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Nádasdy et al., 1999 Although in the model the layer V to layer II synapses are assigned as the neuronal substrate of LTM, it is also assumed in the…”

“During sharp wave ripples, hippocampal place cells that fire in discrete locations of an environment [50], reactivate such that co-active place cell activity, representing a discrete environmental location, or sequences of place cell activity, representing a trajectory through an environment, are replayed [71,46,36,20…”

“Temporally structured replay of spatiotemporal patterns have been observed to occur during sleep, both in the cortex and hippocampus [1–4], and it has been hypothesized that this replay may subserve memory consolidation.”

“With the help of computationally-intensive searches, there have been several studies that have claimed to demonstrate the existence of surprisingly precise and intricate patterns of repeating activity in neuronal circuits from in vivo preparations [7–13], intact slices [1,7,14,15], dissociated neuronal cultures [16–18…”

“Cell firing during subsequent sleep states reflects recently experienced memories rather than the current location of the animal (Wilson and McNaughton, 1994; Kudrimoti et al., 1999; Nádasdy et al., 1999; Sutherland and McNaughton, 2000; Hoffmann and McNaughton, 2002; Lee and Wilson, 2002).”

“…shown that power in the 30–50-Hz slow g band of the local-field potential reflects the strength of coupling of CA3 to CA1 (Csicsvari et al. 2000; Colgin et al. 2009; Nakashiba et al. 2009), whereas power in the 50–100-Hz fast g band reflects the strength of EC3–CA1 coupling (Colgin et al. 2009).”

“It should be noted that replay often coincides with ripple oscillations; namely, any specific neuronal firing pattern is embedded in ripple oscillations (Kudrimoti et al., 1999; Nadasdy et al., 1999; Lee & Wilson, 2002; Buzsaki, 2015).”

“…of an environment, when the hippocampus shows theta activity, and later reactivated or replayed both during sleep (Wilson and McNaughton, 1994; Nadasdy et al., 1999; Lee and Wilson, 2002) and in the awake state (Kudrimoto et al., 1999; Foster and Wilson, 2006; Csicsvari et al., 2007; Diba and…”

“…and quiet wakefulness, recently active place cells have been shown to reactivate in a way that can reflect recently traveled trajectories (Pavlides and Winson, 1989; Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Nádasdy et al., 1999; Foster and Wilson, 2006; Diba and Buzsáki, 2007).”

“Another intensively studied electrophysiological phenomenon, the so-called replay or reactivation of activewaking neuronal activity both in the hippocampus (Pavlides and Winson, 1989; Wilson and McNaughton, 1994; Skaggs and McNaughton, 1996; Kudrimoti et al., 1999; Nádasdy et al., 1999) and in neocortex (Qin et al.”

“…was found to result in impaired long-term memory performance 7 days after training, which was accompanied by reduced synaptic pruning in CA1 pyramidal cells, while short-term memory performance 2 days after training was intact (Katche et al., 2010, 2012; Nakayama et al., 2015).”

“This compression rate is in agreement with the observations in vivo (~ 5 to 20 times; Nádasdy et al., 1999; Lee and Wilson, 2002; Ji and Wilson 2007).”

“In general, sequence replay is faster than the sequence presentation during learning, consistent with sequence compression and fast replay observed in hippocampus [46–48] and neocortex [6,49].”

“…findings that cellular activity underlying new learning is reactivated (Buzsáki, 1989; Pavlides & Winson, 1989; Wilson & McNaughton, 1994)—and even replayed in a similar spatiotemporal pattern (Ji & Wilson, 2007; Lee & Wilson, 2002; Nádasdy et al., 1999)—during post-learning sleep.”

“Although recurring spike patterns have been subject of research for a long time (Abeles et al., 1993; Wilson and McNaughton, 1994; Nádasdy et al., 1999; Dave and Margoliash, 2000; Hoffman and McNaughton, 2002; Hahnloser et al., 2003; Luczak et al., 2007; Madhavan et al., 2007; Rolston et al., 2007;…”

“For example, temporally-structured multicell spiking patterns were observed in the hippocampus and cortex, and were associated to memory traces (Nádasdy et al., 1999; Ji and Wilson, 2007) while the coding of information in the phases of spikes relative to a background oscillation has been observed in many brain region…”

“There can be systematic differences between states in the rate that processes evolve; these differences are not accounted for by the templates (Wilson & McNaughton, 1994; Nádasdy et al., 1999; Dave & Margoliash, 2000; Louie & Wilson, 2001).”

“…there has been much progress in understanding the role of theta oscillations in organizing neuronal activity in animals (O‘Keefe and Dostrovsky, 1971; O‘Keefe and Recce, 1993; Skaggs et al., 1996; Skaggs and McNaughton, 1996; Nádasdy et al., 1999; Huerta and Lisman, 1993; Montgomery et al., 2008).”

“Spontaneous replays of such events in sharp-wave ripples, however, are independent of such speeds, stopping times or locations of the animal (Wilson and McNaughton, 1994; Nádasdy et al., 1999; Geisler et al., 2007; Davidson et al., 2009; Yamamoto and Tonegawa, 2017), as well during sleep (Wilson and McNaughton, 1994;…”

“It has been argued that Hebbian plasticity during replay might strengthen connections among neurons [53], which could facilitate the formation of new assemblies.”