Selective consolidation of learning and memory via recall-gated plasticity.


Journal

eLife
ISSN: 2050-084X
Titre abrégé: Elife
Pays: England
ID NLM: 101579614

Informations de publication

Date de publication:
18 Jul 2024
Historique:
medline: 18 7 2024
pubmed: 18 7 2024
entrez: 18 7 2024
Statut: epublish

Résumé

In a variety of species and behavioral contexts, learning and memory formation recruits two neural systems, with initial plasticity in one system being consolidated into the other over time. Moreover, consolidation is known to be selective; that is, some experiences are more likely to be consolidated into long-term memory than others. Here, we propose and analyze a model that captures common computational principles underlying such phenomena. The key component of this model is a mechanism by which a long-term learning and memory system prioritizes the storage of synaptic changes that are consistent with prior updates to the short-term system. This mechanism, which we refer to as recall-gated consolidation, has the effect of shielding long-term memory from spurious synaptic changes, enabling it to focus on reliable signals in the environment. We describe neural circuit implementations of this model for different types of learning problems, including supervised learning, reinforcement learning, and autoassociative memory storage. These implementations involve synaptic plasticity rules modulated by factors such as prediction accuracy, decision confidence, or familiarity. We then develop an analytical theory of the learning and memory performance of the model, in comparison to alternatives relying only on synapse-local consolidation mechanisms. We find that recall-gated consolidation provides significant advantages, substantially amplifying the signal-to-noise ratio with which memories can be stored in noisy environments. We show that recall-gated consolidation gives rise to a number of phenomena that are present in behavioral learning paradigms, including spaced learning effects, task-dependent rates of consolidation, and differing neural representations in short- and long-term pathways.

Identifiants

pubmed: 39023518
doi: 10.7554/eLife.90793
pii: 90793
doi:
pii:

Types de publication

Journal Article

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : National Science Foundation
ID : DBI-1707398
Organisme : Department of Energy
ID : CSGF (DE-SC0020347)
Organisme : NIH HHS
ID : R01EB029858
Pays : United States

Informations de copyright

© 2023, Lindsey and Litwin-Kumar.

Déclaration de conflit d'intérêts

JL, AL No competing interests declared

Auteurs

Jack W Lindsey (JW)

Zuckerman Mind Brain Behavior Institute, Columbia University, New York, United States.

Ashok Litwin-Kumar (A)

Zuckerman Mind Brain Behavior Institute, Columbia University, New York, United States.

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Classifications MeSH