Preplay of future place cell sequences by hippocampal cellular assemblies

Drăgoi, George; Tonegawa, Susumu

doi:10.1038/nature09633

Cited by 609 publications

(630 citation statements)

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“…The relatively rare occurrence of preplay events (11,12) may simply not provide enough (virtual) experience to consolidate place fields. If so, the opposite result may happen if the unexplored space were somehow made more attentionally salient to the animal.…”

Section: Discussionmentioning

confidence: 99%

“…First, place cells in weanling rats show some adult-like spatial tuning during the animals' first spatial experience away from their nests, suggesting that spatial firing is an innate property of the network (10). Second, ensembles of place cells representing unvisited paths (11) or spaces (12) can become active during periods of rest or sleep before direct experience, a phenomenon called "preplay." Preplay of unexplored spaces suggests that animals can mentally explore a space before physical exploration, but it remains unclear whether such mental exploration is by itself capable of forming a lasting representation.…”

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confidence: 99%

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A stable hippocampal representation of a space requires its direct experience

Rowland¹,

Yanovich

Kentros

2011

Proc. Natl. Acad. Sci. U.S.A.

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In humans and other mammals, the hippocampus is critical for episodic memory, the autobiographical record of events, including where and when they happen. When one records from hippocampal pyramidal neurons in awake, behaving rodents, their most obvious firing correlate is the animal's position within a particular environment, earning them the name "place cells." When an animal explores a novel environment, its pyramidal neurons form their spatial receptive fields over a matter of minutes and are generally stable thereafter. This experience-dependent stabilization of place fields is therefore an attractive candidate neural correlate of the formation of hippocampal memory. However, precisely how the animal's experience of a context translates into stable place fields remains largely unclear. For instance, we still do not know whether observation of a space is sufficient to generate a stable hippocampal representation of that space because the animal must physically visit a spot to demonstrate which cells fire there. We circumvented this problem by comparing the relative stability of place fields of directly experienced space from merely observed space following blockade of NMDA receptors, which preferentially destabilizes newly generated place fields. This allowed us to determine whether place cells stably represent parts of the environment the animal sees, but does not actually occupy. We found that the formation of stable place fields clearly requires direct experience with a space. This suggests that place cells are part of an autobiographical record of events and their spatial context, consistent with providing the "where" information in episodic memory.learning | plasticity | cognitive map | remapping | consolidation T he hippocampus is clearly central to mammalian learning and memory (1), and it is just as clear that an animal's position in space is by far the most obvious firing correlate of hippocampal neurons in awake, behaving rodents (2). However, the precise relationship between memory and place cells is less clear, making the study of the processes governing the formation of place fields particularly interesting. Consistent with the central role for the hippocampus in memory, the balance of experimental evidence supports the idea that place fields are constructed and stabilized by the animal's experience of that space. For example, place cells "remap" (i.e., change to unpredictable locations and/or change their firing rate) in response to even small changes in the sensory environment (3) or even changes in the animal's ongoing behavior (4, 5). Moreover, place fields are quite labile in novel environments until the animal has experienced the environment for several minutes (6, 7). Finally, inhibitors of synaptic plasticity prevent the long-term maintenance (i.e., destabilize) of place fields in novel but not familiar environments (8, 9).However, recent studies have forced a reexamination of the debate. First, place cells in weanling rats show some adult-like spatial tuning during the animals' first sp...

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Section: Discussionmentioning

confidence: 99%

mentioning

confidence: 99%

A stable hippocampal representation of a space requires its direct experience

Rowland¹,

Yanovich

Kentros

2011

Proc. Natl. Acad. Sci. U.S.A.

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“…An event was considered as preplay of the future place cell sequence (Fig. 1B, Left) when the absolute value of the corresponding temporal-spatial correlation exceeded the 97.5 percentile of a distribution of absolute correlation values calculated between the event and 500 surrogate spatial sequences created by shuffling the original spatial order of place cells (5).We used a Bayesian reconstruction algorithm (5,11,12) to decode the rat's position from the neuronal activity recorded during the first run session on the novel track or during the preceding sleep/rest session in the box. The decoded (reconstructed) position during the run was compared with the actual trajectory of the animal (Fig.…”

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confidence: 99%

Distinct preplay of multiple novel spatial experiences in the rat

Drăgoi

Tonegawa

2013

Proc. Natl. Acad. Sci. U.S.A.

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The activity of ensembles of hippocampal place cells represents a hallmark of an animal's spatial experience. The neuronal mechanisms that enable the rapid expression of novel place cell sequences are not entirely understood. Here we report that during sleep or rest, distinct sets of hippocampal temporal sequences in the rat preplay multiple corresponding novel spatial experiences with high specificity. These findings suggest that the place cell sequence of a novel spatial experience is determined, in part, by an online selection of a subset of cellular firing sequences from a larger repertoire of preexisting temporal firing sequences in the hippocampal cellular assembly network that become rapidly bound to the novel experience. We estimate that for the given context, the recorded hippocampal network activity has the capacity to preplay an extended repertoire of at least 15 future spatial experiences of similar distinctiveness and complexity.I t is a matter of debate whether specific sequences of place cells(1) encoding different novel spatial experiences in the rat are formed exclusively during the experiences (2-4) or are, in part, preconfigured in the form of correlated temporal sequences that are expressed before the experience (5-7). Previous work in mice has shown that in the naïve animal, temporal firing sequences expressed in association with sharp-wave ripples during sleep or rest can preplay future spatial sequences of place cells encoding novel environments (5). However, it remains unclear whether place cell sequences encoding a novel spatial experience are preconfigured as a dominant cluster of temporal sequences preferentially preplaying the subsequent experience or whether they are selected from an existing larger repertoire of temporally organized sequences. The latter would confer the hippocampal network with the capacity to rapidly encode multiple parallel spatial experiences, but the extent of this capacity has not been addressed experimentally. Here we investigate these two issues. Results Preplay of Future Place Cell Sequences and Spatial Trajectories.Ensembles of place cells were recorded from the CA1 area of the hippocampus in three experimentally naïve rats during sleep/ rest sessions and during subsequent first-time exploration of 1.5-m-long linear tracks (Fig. 1A). The sleep/rest sessions were conducted in a sleep/rest box surrounded by high opaque walls that blocked the rats' view of the room except for a limited portion of the ceiling. After the naïve rats went through an ∼1-h sleep/rest period, a linear track (Materials and Methods) was introduced into the room for the first time. Place cell sequence templates were computed by ordering the place cells based on the location of their place field peak firing during exploration of the linear track (Fig. 1B, Right). Spiking events were detected during sleep/rest frames (8) as epochs of multiunit activity recorded from at least six different pyramidal cells with a <100-ms interspike interval in the multiunit activity, flanked by epochs of >...

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“…Stability analysis of the stationary states A * is done by linearizing the integral equation (3). For small perturbations…”

Section: B Perturbationsmentioning

confidence: 99%

“…Although information processing in biological neuronal networks is often linked to exquisitely timed individual spikes [1][2][3], cognitive phenomena, such as short-term memory and decision making, are also reflected by slowly changing neuronal firing rates [4,5]. To act as such rate encoders, neurons have to be able to gradually and persistently elevate their firing rate over some period of time.…”

Section: Introductionmentioning

confidence: 99%

Renewal theory of coupled neuronal pools: Stable states and slow trajectories

Leibold

2011

Phys. Rev. E

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A theory is provided to analyze the dynamics of delay-coupled pools of spiking neurons based on stability analysis of stationary firing. Transitions between stable and unstable regimes can be predicted by bifurcation analysis of the underlying integral dynamics. Close to the bifurcation point the network exhibits slowly changing activities and allows for slow collective phenomena like continuous attractors.

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Preplay of future place cell sequences by hippocampal cellular assemblies

Cited by 609 publications

References 26 publications

A stable hippocampal representation of a space requires its direct experience

A stable hippocampal representation of a space requires its direct experience

Distinct preplay of multiple novel spatial experiences in the rat

Renewal theory of coupled neuronal pools: Stable states and slow trajectories

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