A tale of two algorithms: Structured slots explain prefrontal sequence memory and are unified with hippocampal cognitive maps

Remembering events is crucial to intelligent behavior. Flexible memory retrieval requires a cognitive map and is supported by two key brain systems: hippocampal episodic memory (EM) and prefrontal working memory (WM). Although an understanding of EM is emerging, little is understood of WM beyond simple memory retrieval. We develop a mathematical theory relating the algorithms and representations of EM and WM by unveiling a duality between storing memories in synapses versus neural activity. This results in a formalism of prefrontal WM as structured, controllable neural subspaces (activity slots) representing dynamic cognitive maps without synaptic plasticity. Using neural networks, we elucidate differences, similarities, and trade-offs between the hippocampal and prefrontal algorithms. Lastly, we show that prefrontal representations in tasks from list learning to cue-dependent recall are unified as controllable activity slots. Our results unify frontal and temporal representations of memory and offer a new understanding for dynamic prefrontal representations of WM.

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Publication Details

Journal
Neuron
Published
2024-11-21
DOI
https://doi.org/10.1016/j.neuron.2024.10.017
Citations
19
Primary Topic
Memory and Neural Mechanisms
Type
article
Field-Weighted Citation Impact
6.51
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article

A tale of two algorithms: Structured slots explain prefrontal sequence memory and are unified with hippocampal cognitive maps

Mohamady El-Gaby, William Dorrell, Timothy E.J. Behrens, James C. R. Whittington et al.
19 citations
Neuron
Memory and Neural Mechanisms
6.51
article

A tale of two algorithms: Structured slots explain prefrontal sequence memory and are unified with hippocampal cognitive maps

Mohamady El-Gaby, William Dorrell, Timothy E.J. Behrens, James C. R. Whittington, Surya Ganguli
article en
19 citations

Abstract

Remembering events is crucial to intelligent behavior. Flexible memory retrieval requires a cognitive map and is supported by two key brain systems: hippocampal episodic memory (EM) and prefrontal working memory (WM). Although an understanding of EM is emerging, little is understood of WM beyond simple memory retrieval. We develop a mathematical theory relating the algorithms and representations of EM and WM by unveiling a duality between storing memories in synapses versus neural activity. This results in a formalism of prefrontal WM as structured, controllable neural subspaces (activity slots) representing dynamic cognitive maps without synaptic plasticity. Using neural networks, we elucidate differences, similarities, and trade-offs between the hippocampal and prefrontal algorithms. Lastly, we show that prefrontal representations in tasks from list learning to cue-dependent recall are unified as controllable activity slots. Our results unify frontal and temporal representations of memory and offer a new understanding for dynamic prefrontal representations of WM.

NeuronVol. 113(2)
Wellcome Centre for Human Neuroimaging (GB), Palo Alto University (US), University of Oxford (GB), Wellcome Centre for Integrative Neuroimaging (GB), Oxford Centre for Computational Neuroscience (GB), University College London (GB), Stanford University (US)
Reduced inequalities
Openalex Percentile: Top 3%
Memory and Neural Mechanisms
6.51
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A tale of two algorithms: Structured slots explain prefrontal sequence memory and are unified with hippocampal cognitive maps — Mohamady El-Gaby, William Dorrell, et al. · Neuron (2024) | TGRS Research Map | TGRS