Stepwise synaptic plasticity events drive the early phase of memory consolidation

Goto, Akihiro; Bota, Ayaka; Miya, Ken; Wang, Jingbo; Tsukamoto, Suzune; Jiang, Xinzhi; Hirai, Daichi; Murayama, Miyuki; Matsuda, Takehisa; McHugh, Thomas J.; Nagai, Takeharu; Hayashi, Yasunori

doi:10.1126/science.abj9195

Cited by 102 publications

(58 citation statements)

References 40 publications

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“…This strategy is slow because it relies on these continued reminders over time about the distribution of information from the environment. But sleep-dependent memory consolidation, including integration of new information with existing knowledge, can occur quite quickly, over one night or several nights of sleep (6,7,(25)(26)(27)(28). The CLS framework fails in non-stationary environments because the environment no longer provides those required reminders of old information.…”

Section: Introductionmentioning

confidence: 99%

A model of autonomous interactions between hippocampus and neocortex driving sleep-dependent memory consolidation

Singh

Norman

Schapiro

2022

Preprint

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How do we build up our knowledge of the world over time? Many theories of memory formation and consolidation have posited that the hippocampus stores new information, then "teaches" this information to neocortex over time, especially during sleep. But it is unclear, mechanistically, how this actually works — how are these systems able to interact during periods with virtually no environmental input to accomplish useful learning and shifts in representation? We provide a framework for thinking about this question, with neural network model simulations serving as demonstrations. The model contains hippocampus and neocortical areas, which replay memories and interact with one another completely autonomously during simulated sleep. Oscillations are leveraged to support error-driven learning that leads to useful changes in memory representation and behavior. The model has a non-Rapid Eye Movement (NREM) sleep stage, where dynamics between hippocampus and neocortex are tightly coupled, with hippocampus helping neocortex to reinstate high-fidelity versions of new attractors, and a REM sleep stage, where neocortex is able to more freely explore existing attractors. We find that alternating between NREM and REM sleep stages, which alternately focuses the model’s replay on recent and remote information, facilitates graceful continual learning. We thus provide an account of how the hippocampus and neocortex can interact without any external input during sleep to drive useful new cortical learning and to protect old knowledge as new information is integrated.

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Section: Introductionmentioning

confidence: 99%

A model of autonomous interactions between hippocampus and neocortex driving sleep-dependent memory consolidation

Singh

Norman

Schapiro

2022

Preprint

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“…These results were in line with a recent study showing that memory recall is impaired when LTP is optically erased selectively during sleep. 15 Third, we separately blocked the Hebbian and non-Hebbian forms of long-term excitatory synaptic plasticity in our model and verified that each was essential for memory encoding and consolidation (Extended Data Fig. 6).…”

Section: Mainmentioning

confidence: 56%

Dynamic and selective engrams emerge with memory consolidation

Tomé

Zhang

Aida

et al. 2022

Preprint

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Episodic memories are encoded by sparse populations of neurons activated during an experience1. These neural ensembles constitute memory engrams that are both necessary and sufficient for inducing recall even long after memory acquisition2. This suggests that following encoding, engrams are stabilized to reliably support memory retrieval. However, little is known about the temporal evolution of engrams over the course of memory consolidation or how it impacts mnemonic properties. Here we employed computational and experimental approaches to examine how the composition and selectivity of engrams change with memory consolidation. We modeled engram cells using a spiking recurrent neural network that yielded three testable predictions: memories transition from unselective to selective as neurons are removed from and added to the engram, inhibitory activity during recall is essential for memory selectivity, and inhibitory synaptic plasticity during memory consolidation is critical for engrams to become selective. Using the Cal-Light system to tag activated neurons in vivo with high spatiotemporal precision3 as well as optogenetic and chemogenetic techniques, we conducted contextual fear conditioning experiments that supported each of our model's predictions. Our results reveal that engrams are dynamic even within hours of memory consolidation and that changes in engram composition mediated by inhibitory synaptic plasticity are crucial for the emergence of memory selectivity. These findings challenge classical theories of stable memory traces and point to a close link between engram state and memory expression.

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“…This is quite reasonable because the early phase of L-LTP can last for several hours, and structural changes are likely to occur on a faster time course ( Fukazawa et al, 2003 ). Indeed, recent results indicate that changes in F-actin occur within minutes after the induction of LTP ( Goto et al, 2021 ). This scenario also might explain why such structural changes might be necessary for the maintenance of L-LTP.…”

Section: Discussionmentioning

confidence: 99%

Conditions for Synaptic Specificity during the Maintenance Phase of Synaptic Plasticity

Huertas¹,

Newton

McDougal

et al. 2022

eNeuro

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Activity-dependent modifications of synaptic efficacies are a cellular substrate of learning and memory. Experimental evidence shows that these modifications are synapse specific and that the long-lasting effects are associated with the sustained increase in concentration of specific proteins like PKM ζ . However, such proteins are likely to diffuse away from their initial synaptic location and spread out to neighboring synapses, potentially compromising synapse specificity. In this article, we address the issue of synapse specificity during memory maintenance. Assuming that the long-term maintenance of synaptic plasticity is accomplished by a molecular switch, we carry out analytical calculations and perform simulations using the reaction-diffusion package in NEURON to determine the limits of synapse specificity during maintenance. Moreover, we explore the effects of the diffusion and degradation rates of proteins and of the geometrical characteristics of dendritic spines on synapse specificity. We conclude that the necessary conditions for synaptic specificity during maintenance require that molecular switches reside in dendritic spines. The requirement for synaptic specificity when the molecular switch resides in spines still imposes strong limits on the diffusion and turnover of rates of maintenance molecules, as well as on the morphologic properties of synaptic spines. These constraints are quite general and apply to most existing models suggested for maintenance. The parameter values can be experimentally evaluated, and if they do not fit the appropriate predicted range, the validity of this class of maintenance models would be challenged.

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Stepwise synaptic plasticity events drive the early phase of memory consolidation

Cited by 102 publications

References 40 publications

A model of autonomous interactions between hippocampus and neocortex driving sleep-dependent memory consolidation

A model of autonomous interactions between hippocampus and neocortex driving sleep-dependent memory consolidation

Dynamic and selective engrams emerge with memory consolidation

Conditions for Synaptic Specificity during the Maintenance Phase of Synaptic Plasticity

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