Geometry and dynamics of representations in a precisely balanced memory network related to olfactory cortex

Biological memory networks are thought to store information by experience-dependent changes in the synaptic connectivity between assemblies of neurons. Recent models suggest that these assemblies contain both excitatory and inhibitory neurons (E/I assemblies), resulting in co-tuning and precise bala...

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Main Authors: Claire Meissner-Bernard, Friedemann Zenke, Rainer W Friedrich
Format: Article
Language:English
Published: eLife Sciences Publications Ltd 2025-01-01
Series:eLife
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Online Access:https://elifesciences.org/articles/96303
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author Claire Meissner-Bernard
Friedemann Zenke
Rainer W Friedrich
author_facet Claire Meissner-Bernard
Friedemann Zenke
Rainer W Friedrich
author_sort Claire Meissner-Bernard
collection DOAJ
description Biological memory networks are thought to store information by experience-dependent changes in the synaptic connectivity between assemblies of neurons. Recent models suggest that these assemblies contain both excitatory and inhibitory neurons (E/I assemblies), resulting in co-tuning and precise balance of excitation and inhibition. To understand computational consequences of E/I assemblies under biologically realistic constraints we built a spiking network model based on experimental data from telencephalic area Dp of adult zebrafish, a precisely balanced recurrent network homologous to piriform cortex. We found that E/I assemblies stabilized firing rate distributions compared to networks with excitatory assemblies and global inhibition. Unlike classical memory models, networks with E/I assemblies did not show discrete attractor dynamics. Rather, responses to learned inputs were locally constrained onto manifolds that ‘focused’ activity into neuronal subspaces. The covariance structure of these manifolds supported pattern classification when information was retrieved from selected neuronal subsets. Networks with E/I assemblies therefore transformed the geometry of neuronal coding space, resulting in continuous representations that reflected both relatedness of inputs and an individual’s experience. Such continuous representations enable fast pattern classification, can support continual learning, and may provide a basis for higher-order learning and cognitive computations.
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spelling doaj-art-d78a0f32cce847908e36563351aaa9342025-01-13T17:51:42ZengeLife Sciences Publications LtdeLife2050-084X2025-01-011310.7554/eLife.96303Geometry and dynamics of representations in a precisely balanced memory network related to olfactory cortexClaire Meissner-Bernard0https://orcid.org/0009-0007-2038-8398Friedemann Zenke1https://orcid.org/0000-0003-1883-644XRainer W Friedrich2https://orcid.org/0000-0001-9107-0482Friedrich Miescher Institute for Biomedical Research, Basel, SwitzerlandFriedrich Miescher Institute for Biomedical Research, Basel, Switzerland; University of Basel, Basel, SwitzerlandFriedrich Miescher Institute for Biomedical Research, Basel, Switzerland; University of Basel, Basel, SwitzerlandBiological memory networks are thought to store information by experience-dependent changes in the synaptic connectivity between assemblies of neurons. Recent models suggest that these assemblies contain both excitatory and inhibitory neurons (E/I assemblies), resulting in co-tuning and precise balance of excitation and inhibition. To understand computational consequences of E/I assemblies under biologically realistic constraints we built a spiking network model based on experimental data from telencephalic area Dp of adult zebrafish, a precisely balanced recurrent network homologous to piriform cortex. We found that E/I assemblies stabilized firing rate distributions compared to networks with excitatory assemblies and global inhibition. Unlike classical memory models, networks with E/I assemblies did not show discrete attractor dynamics. Rather, responses to learned inputs were locally constrained onto manifolds that ‘focused’ activity into neuronal subspaces. The covariance structure of these manifolds supported pattern classification when information was retrieved from selected neuronal subsets. Networks with E/I assemblies therefore transformed the geometry of neuronal coding space, resulting in continuous representations that reflected both relatedness of inputs and an individual’s experience. Such continuous representations enable fast pattern classification, can support continual learning, and may provide a basis for higher-order learning and cognitive computations.https://elifesciences.org/articles/96303autoassociative memoryassemblyolfactory cortexcomputational modelzebrafishneural manifold
spellingShingle Claire Meissner-Bernard
Friedemann Zenke
Rainer W Friedrich
Geometry and dynamics of representations in a precisely balanced memory network related to olfactory cortex
eLife
autoassociative memory
assembly
olfactory cortex
computational model
zebrafish
neural manifold
title Geometry and dynamics of representations in a precisely balanced memory network related to olfactory cortex
title_full Geometry and dynamics of representations in a precisely balanced memory network related to olfactory cortex
title_fullStr Geometry and dynamics of representations in a precisely balanced memory network related to olfactory cortex
title_full_unstemmed Geometry and dynamics of representations in a precisely balanced memory network related to olfactory cortex
title_short Geometry and dynamics of representations in a precisely balanced memory network related to olfactory cortex
title_sort geometry and dynamics of representations in a precisely balanced memory network related to olfactory cortex
topic autoassociative memory
assembly
olfactory cortex
computational model
zebrafish
neural manifold
url https://elifesciences.org/articles/96303
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AT friedemannzenke geometryanddynamicsofrepresentationsinapreciselybalancedmemorynetworkrelatedtoolfactorycortex
AT rainerwfriedrich geometryanddynamicsofrepresentationsinapreciselybalancedmemorynetworkrelatedtoolfactorycortex