Skip to main content
U.S. Department of Energy
Office of Scientific and Technical Information

Selective consolidation of learning and memory via recall-gated plasticity

Journal Article · · eLife
DOI:https://doi.org/10.7554/eLife.90793· OSTI ID:2404443

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.

Sponsoring Organization:
USDOE
OSTI ID:
2404443
Alternate ID(s):
OSTI ID: 2404444
OSTI ID: 2471921
Journal Information:
eLife, Journal Name: eLife Vol. 12; ISSN 2050-084X
Publisher:
eLife Sciences Publications, Ltd.Copyright Statement
Country of Publication:
United States
Language:
English

References (53)

Considerations arising from a complementary learning systems perspective on hippocampus and neocortex journal January 1996
Hippocampal mediation of stimulus representation: A computational theory journal October 1993
Knowledge Distillation: A Survey journal March 2021
The time window hypothesis: Spacing effects journal January 1995
Short-term, intermediate-term, and long-term memories journal November 1993
Retrograde amnesia and memory consolidation: a neurobiological perspective journal April 1995
The Molecular and Systems Biology of Memory journal March 2014
Systems memory consolidation in Drosophila journal February 2013
The Role of Hippocampal Replay in Memory and Planning journal January 2018
Spaced training enhances memory and prefrontal ensemble stability in mice journal September 2021
Cascade Models of Synaptically Stored Memories journal February 2005
Traces of Drosophila Memory journal April 2011
Sparseness and Expansion in Sensory Representations journal September 2014
Motor Cortex Is Required for Learning but Not for Executing a Motor Skill journal May 2015
Actor–critic models of the basal ganglia: new anatomical and computational perspectives journal June 2002
Limitations to the Spacing Effect journal January 2005
Distributed practice in verbal recall tasks: A review and quantitative synthesis. journal January 2006
Why there are complementary learning systems in the hippocampus and neocortex: Insights from the successes and failures of connectionist models of learning and memory. journal July 1995
Hippocampal replay in the awake state: a potential substrate for memory consolidation and retrieval journal January 2011
Computational principles of synaptic memory consolidation journal October 2016
The organization of recent and remote memories journal February 2005
Brain-inspired replay for continual learning with artificial neural networks journal August 2020
Remembrance of things practiced with fast and slow learning in cortical and subcortical pathways journal December 2020
Computational models of episodic-like memory in food-caching birds journal May 2023
Adaptive stimulus selection for consolidation in the hippocampus journal December 2021
The basal ganglia control the detailed kinematics of learned motor skills journal July 2021
A basal ganglia-forebrain circuit in the songbird biases motor output to avoid vocal errors journal July 2009
Rapid and independent memory formation in the parietal cortex journal November 2016
The neural circuit linking mushroom body parallel circuits induces memory consolidation in Drosophila journal July 2019
Neural networks and physical systems with emergent collective computational abilities. journal April 1982
The space of interactions in neural network models journal January 1988
Stochastic Consolidation of Lifelong Memory preprint August 2021
Organizing memories for generalization in complementary learning systems preprint January 2023
The Role of Experience in Prioritizing Hippocampal Replay preprint March 2023
Dynamics of striatal action selection and reinforcement learning preprint February 2024
The basal ganglia can control learned motor sequences independently of motor cortex preprint November 2019
Spacing Effects in Learning journal November 2008
Disengagement of motor cortex from movement control during long-term learning journal October 2019
Mechanisms and time course of vocal learning and consolidation in the adult songbird journal October 2011
Learning in Neural Networks with Material Synapses journal September 1994
Efficient Partitioning of Memory Systems and Its Importance for Memory Consolidation journal July 2013
Hebbian plasticity in parallel synaptic pathways: A circuit mechanism for systems memory consolidation journal December 2021
System-Like Consolidation of Olfactory Memories in Drosophila journal June 2013
Performance-Dependent Consolidation of Learned Vocal Changes in Adult Songbirds journal January 2022
Learning Performance of Normal and MutantDrosophilaafter Repeated Conditioning Trials with Discrete Stimuli journal April 2000
Disengagement of Motor Cortex during Long-Term Learning Tracks the Performance Level of Learned Movements journal July 2021
Hippocampal Sharp Waves and Reactivation during Awake States Depend on Repeated Sequential Experience journal November 2006
Neuromodulated Spike-Timing-Dependent Plasticity, and Theory of Three-Factor Learning Rules journal January 2016
The neuronal architecture of the mushroom body provides a logic for associative learning journal December 2014
Rules and mechanisms for efficient two-stage learning in neural circuits journal April 2017
Learning multiple variable-speed sequences in striatum via cortical tutoring journal May 2017
Can sleep protect memories from catastrophic forgetting? journal August 2020
The connectome of the adult Drosophila mushroom body provides insights into function journal December 2020

Similar Records

Selective consolidation of learning and memory via recall-gated plasticity
Journal Article · Thu Jul 18 00:00:00 EDT 2024 · eLife · OSTI ID:2404460

Related Subjects