Self-organized reactivation maintains and reinforces memories despite synaptic turnover
Abstract
Long-term memories are believed to be stored in the synapses of cortical neuronal networks. However, recent experiments report continuous creation and removal of cortical synapses, which raises the question how memories can survive on such a variable substrate. Here, we study the formation and retention of associative memory in a computational model based on Hebbian cell assemblies in the presence of both synaptic and structural plasticity. During rest periods, such as may occur during sleep, the assemblies reactivate spontaneously, reinforcing memories against ongoing synapse removal and replacement. Brief daily reactivations during rest-periods suffice to not only maintain the assemblies, but even strengthen them, and improve pattern completion, consistent with offline memory gains observed experimentally. While the connectivity inside memory representations is strengthened during rest phases, connections in the rest of the network decay and vanish thus reconciling apparently conflicting hypotheses of the influence of sleep on cortical connectivity.
Data availability
All data generated or analysed during this study are included in the manuscript and supporting files. The source code zip archive (Source code 1) contains the model simulation code and the stimulation file used to generate Figure 2, 3, 4B&C, 5 and 6 as well as Figure 4-figure supplements 1 and 2.
Article and author information
Author details
Funding
Deutsche Forschungsgemeinschaft (FA 1471/1-1 and 2-1)
- Michael Jan Fauth
Engineering and Physical Sciences Research Council (EP/R030952/1)
- Mark CW van Rossum
The funders had no role in study design, data collection and interpretation, or the decision to submit the work for publication.
Reviewing Editor
- Frances K Skinner, Krembil Research Institute, University Health Network, Canada
Version history
- Received: November 19, 2018
- Accepted: April 30, 2019
- Accepted Manuscript published: May 10, 2019 (version 1)
- Version of Record published: June 3, 2019 (version 2)
Copyright
© 2019, Fauth & van Rossum
This article is distributed under the terms of the Creative Commons Attribution License permitting unrestricted use and redistribution provided that the original author and source are credited.
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Further reading
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- Neuroscience
Probing memory of a complex visual image within a few hundred milliseconds after its disappearance reveals significantly greater fidelity of recall than if the probe is delayed by as little as a second. Classically interpreted, the former taps into a detailed but rapidly decaying visual sensory or ‘iconic’ memory (IM), while the latter relies on capacity-limited but comparatively stable visual working memory (VWM). While iconic decay and VWM capacity have been extensively studied independently, currently no single framework quantitatively accounts for the dynamics of memory fidelity over these time scales. Here, we extend a stationary neural population model of VWM with a temporal dimension, incorporating rapid sensory-driven accumulation of activity encoding each visual feature in memory, and a slower accumulation of internal error that causes memorized features to randomly drift over time. Instead of facilitating read-out from an independent sensory store, an early cue benefits recall by lifting the effective limit on VWM signal strength imposed when multiple items compete for representation, allowing memory for the cued item to be supplemented with information from the decaying sensory trace. Empirical measurements of human recall dynamics validate these predictions while excluding alternative model architectures. A key conclusion is that differences in capacity classically thought to distinguish IM and VWM are in fact contingent upon a single resource-limited WM store.
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- Neuroscience
Our ability to recall details from a remembered image depends on a single mechanism that is engaged from the very moment the image disappears from view.