The reorganization and reactivation of hippocampal maps predict spatial memory performance

Dupret, David; O’Neill, Joseph; Pleydell-Bouverie, Barty; Csicsvari, Jozsef

doi:10.1038/nn.2599

Cited by 647 publications

(815 citation statements)

References 48 publications

Supporting

Mentioning

725

Contrasting

Order By: Relevance

“…However, the newly made fields simply do not appear to get "burned in" without NMDA receptor-dependent plasticity: the outer box cells had either entirely new firing fields in the second session, or none at all. This brings to mind a recent study showing that CPP specifically destabilizes only the place fields that remap in response to a novel behavioral task, sparing the previously learned representation of the task space (5). Taken together, these data suggest that the hippocampal representation of a space is a continuously updated record of the animal's "first-person" experience of its environment, which is recalled as the animal reexperiences that space, and that NMDA-dependent plasticity is required more for the stabilization of place fields rather than for their initial formation.…”

Section: Discussionmentioning

confidence: 99%

“…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).…”

mentioning

confidence: 99%

See 1 more Smart Citation

A stable hippocampal representation of a space requires its direct experience

Rowland¹,

Yanovich

Kentros

2011

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

View full text Add to dashboard Cite

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...

show abstract

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.

View full text Add to dashboard Cite

show abstract

“…Memory consolidation is thought to involve post-encoding reactivation of the activity patterns present during initial experience (activity replay) (Girardeau et al, 2009;Dupret et al, 2010). The frequency of activity replay decreases after the learning experience; replay is most frequent in the minutes following an experience (Tatsuno et al, 2006) but may persist for 18-24 h (Kudrimoti et al, 1999).…”

Section: Ic++ Silencing Of Creb-overexpressing Dg Neurons Shortly Aftmentioning

confidence: 99%

Neuronal Allocation to a Hippocampal Engram

Park

Kramer

Mercaldo

et al. 2016

Neuropsychopharmacol

153

113

View full text Add to dashboard Cite

The dentate gyrus (DG) is important for encoding contextual memories, but little is known about how a population of DG neurons comes to encode and support a particular memory. One possibility is that recruitment into an engram depends on a neuron's excitability. Here, we manipulated excitability by overexpressing CREB in a random population of DG neurons and examined whether this biased their recruitment to an engram supporting a contextual fear memory. To directly assess whether neurons overexpressing CREB at the time of training became critical components of the engram, we examined memory expression while the activity of these neurons was silenced. Chemogenetically (hM4Di, an inhibitory DREADD receptor) or optogenetically (iC++, a light-activated chloride channel) silencing the small number of CREB-overexpressing DG neurons attenuated memory expression, whereas silencing a similar number of random neurons not overexpressing CREB at the time of training did not. As post-encoding reactivation of the activity patterns present during initial experience is thought to be important in memory consolidation, we investigated whether post-training silencing of neurons allocated to an engram disrupted subsequent memory expression. We found that silencing neurons 5 min (but not 24 h) following training disrupted memory expression. Together these results indicate that the rules of neuronal allocation to an engram originally described in the lateral amygdala are followed in different brain regions including DG, and moreover, that disrupting the post-training activity pattern of these neurons prevents memory consolidation.

show abstract

“…Structured ensemble activity during these events is thought to underlie memory consolidation during sleep [83], and may also contribute to rapid processing underpinning consolidation or refinement of encoding during learning itself [84,85].…”

Section: Selecting Circuits Within Circuits: Who Does What When?mentioning

confidence: 99%

Updating hippocampal representations: CA2 joins the circuit

Jones

McHugh

2011

Trends in Neurosciences

114

106

View full text Add to dashboard Cite

The hippocampus integrates the encoding, storage and recall of memories, binding the spatiotemporal and sensory information that constitutes experience and keeping episodes in their correct context. The rapid and accurate processing of such daunting volumes of continuouslychanging data relies on dynamically assigning different aspects of mnemonic processing to specialized, interconnected networks corresponding to the anatomical subfields of dentate gyrus (DG), CA3 and CA1. However, differentially processed information ultimately has to be reintegrated into conjunctive representations, and this is unlikely to be achieved by unidirectional, sequential steps through a DG-CA3-CA1 loop. In this Review, we highlight recently discovered anatomical and physiological features that are likely to necessitate updates to the hippocampal circuit diagram, particularly by incorporating the oft-neglected CA2 region.3

show abstract

The reorganization and reactivation of hippocampal maps predict spatial memory performance

Cited by 647 publications

References 48 publications

A stable hippocampal representation of a space requires its direct experience

A stable hippocampal representation of a space requires its direct experience

Neuronal Allocation to a Hippocampal Engram

Updating hippocampal representations: CA2 joins the circuit

Contact Info

Product

Resources

About