The modular and hierarchical organization of the brain is believed to support the coexistence of segregated (specialization) and integrated (binding) information processes. A relevant question is yet to understand how such architecture naturally emerges and is sustained over time, given the plastic nature of the brain’s wiring. Following evidences that the sensory cortices organize into assemblies under selective stimuli, it has been shown that stable neuronal assemblies can emerge due to targeted stimulation, embedding various forms of synaptic plasticity in presence of homeostatic and/or control mechanisms. Here, we show that simple spike-timing-dependent plasticity (STDP) rules, based only on pre- and post-synaptic spike times, can also lead to the stable encoding of memories in the absence of any control mechanism. We develop a model of spiking neurons, trained by stimuli targeting different sub-populations. The model satisfies some biologically plausible features: (i) it contains excitatory and inhibitory neurons with Hebbian and anti-Hebbian STDP; (ii) neither the neuronal activity nor the synaptic weights are frozen after the learning phase. Instead, the neurons are allowed to fire spontaneously while synaptic plasticity remains active. We find that only the combination of two inhibitory STDP sub-populations allows for the formation of stable modules in the network, with each sub-population playing a distinctive role. The Hebbian sub-population controls for the firing activity, while the anti-Hebbian neurons promote pattern selectivity. After the learning phase, the network settles into an asynchronous irregular resting-state. This post-learning activity is associated with spontaneous memory recalls which turn out to be fundamental for the long-term consolidation of the learned memories. Due to its simplicity, the introduced model can represent a test-bed for further investigations on the role played by STDP on memory storing and maintenance.

Emergence and maintenance of modularity in neural networks with Hebbian and anti-Hebbian inhibitory STDP

Torcini, Alessandro;
2025

Abstract

The modular and hierarchical organization of the brain is believed to support the coexistence of segregated (specialization) and integrated (binding) information processes. A relevant question is yet to understand how such architecture naturally emerges and is sustained over time, given the plastic nature of the brain’s wiring. Following evidences that the sensory cortices organize into assemblies under selective stimuli, it has been shown that stable neuronal assemblies can emerge due to targeted stimulation, embedding various forms of synaptic plasticity in presence of homeostatic and/or control mechanisms. Here, we show that simple spike-timing-dependent plasticity (STDP) rules, based only on pre- and post-synaptic spike times, can also lead to the stable encoding of memories in the absence of any control mechanism. We develop a model of spiking neurons, trained by stimuli targeting different sub-populations. The model satisfies some biologically plausible features: (i) it contains excitatory and inhibitory neurons with Hebbian and anti-Hebbian STDP; (ii) neither the neuronal activity nor the synaptic weights are frozen after the learning phase. Instead, the neurons are allowed to fire spontaneously while synaptic plasticity remains active. We find that only the combination of two inhibitory STDP sub-populations allows for the formation of stable modules in the network, with each sub-population playing a distinctive role. The Hebbian sub-population controls for the firing activity, while the anti-Hebbian neurons promote pattern selectivity. After the learning phase, the network settles into an asynchronous irregular resting-state. This post-learning activity is associated with spontaneous memory recalls which turn out to be fundamental for the long-term consolidation of the learned memories. Due to its simplicity, the introduced model can represent a test-bed for further investigations on the role played by STDP on memory storing and maintenance.
Campo DC Valore Lingua
dc.authority.ancejournal PLOS COMPUTATIONAL BIOLOGY en
dc.authority.orgunit Istituto dei Sistemi Complessi - ISC en
dc.authority.people Bergoin, Raphaël en
dc.authority.people Torcini, Alessandro en
dc.authority.people Deco, Gustavo en
dc.authority.people Quoy, Mathias en
dc.authority.people Zamora-López, Gorka en
dc.collection.id.s b3f88f24-048a-4e43-8ab1-6697b90e068e *
dc.collection.name 01.01 Articolo in rivista *
dc.contributor.appartenenza Istituto dei Sistemi Complessi - ISC - Sede Secondaria Sesto Fiorentino *
dc.contributor.appartenenza.mi 1037 *
dc.contributor.area Non assegn *
dc.date.accessioned 2025/05/29 07:36:38 -
dc.date.available 2025/05/29 07:36:38 -
dc.date.firstsubmission 2025/05/29 07:35:43 *
dc.date.issued 2025 -
dc.date.submission 2025/05/29 07:35:43 *
dc.description.abstracteng The modular and hierarchical organization of the brain is believed to support the coexistence of segregated (specialization) and integrated (binding) information processes. A relevant question is yet to understand how such architecture naturally emerges and is sustained over time, given the plastic nature of the brain’s wiring. Following evidences that the sensory cortices organize into assemblies under selective stimuli, it has been shown that stable neuronal assemblies can emerge due to targeted stimulation, embedding various forms of synaptic plasticity in presence of homeostatic and/or control mechanisms. Here, we show that simple spike-timing-dependent plasticity (STDP) rules, based only on pre- and post-synaptic spike times, can also lead to the stable encoding of memories in the absence of any control mechanism. We develop a model of spiking neurons, trained by stimuli targeting different sub-populations. The model satisfies some biologically plausible features: (i) it contains excitatory and inhibitory neurons with Hebbian and anti-Hebbian STDP; (ii) neither the neuronal activity nor the synaptic weights are frozen after the learning phase. Instead, the neurons are allowed to fire spontaneously while synaptic plasticity remains active. We find that only the combination of two inhibitory STDP sub-populations allows for the formation of stable modules in the network, with each sub-population playing a distinctive role. The Hebbian sub-population controls for the firing activity, while the anti-Hebbian neurons promote pattern selectivity. After the learning phase, the network settles into an asynchronous irregular resting-state. This post-learning activity is associated with spontaneous memory recalls which turn out to be fundamental for the long-term consolidation of the learned memories. Due to its simplicity, the introduced model can represent a test-bed for further investigations on the role played by STDP on memory storing and maintenance. -
dc.description.allpeople Bergoin, Raphaël; Torcini, Alessandro; Deco, Gustavo; Quoy, Mathias; Zamora-López, Gorka -
dc.description.allpeopleoriginal Bergoin, Raphaël; Torcini, Alessandro; Deco, Gustavo; Quoy, Mathias; Zamora-López, Gorka en
dc.description.fulltext open en
dc.description.numberofauthors 5 -
dc.identifier.doi 10.1371/journal.pcbi.1012973 en
dc.identifier.isi WOS:001473015000002 -
dc.identifier.scopus 2-s2.0-105003821787 en
dc.identifier.source crossref *
dc.identifier.uri https://hdl.handle.net/20.500.14243/545441 -
dc.identifier.url https://journals.plos.org/ploscompbiol/article?id=10.1371/journal.pcbi.1012973 en
dc.language.iso eng en
dc.relation.issue 4 en
dc.relation.numberofpages 35 en
dc.relation.volume 21 en
dc.subject.keywords -- -
dc.subject.singlekeyword -- *
dc.title Emergence and maintenance of modularity in neural networks with Hebbian and anti-Hebbian inhibitory STDP en
dc.type.driver info:eu-repo/semantics/article -
dc.type.full 01 Contributo su Rivista::01.01 Articolo in rivista it
dc.type.miur 262 -
iris.isi.extIssued 2025 -
iris.isi.extTitle Emergence and maintenance of modularity in neural networks with Hebbian and anti-Hebbian inhibitory STDP -
iris.mediafilter.data 2025/05/30 02:47:19 *
iris.orcid.lastModifiedDate 2025/05/31 01:09:14 *
iris.orcid.lastModifiedMillisecond 1748646554823 *
iris.scopus.extIssued 2025 -
iris.scopus.extTitle Emergence and maintenance of modularity in neural networks with Hebbian and anti-Hebbian inhibitory STDP -
iris.sitodocente.maxattempts 1 -
iris.unpaywall.bestoahost publisher *
iris.unpaywall.bestoaversion publishedVersion *
iris.unpaywall.doi 10.1371/journal.pcbi.1012973 *
iris.unpaywall.hosttype publisher *
iris.unpaywall.isoa true *
iris.unpaywall.journalisindoaj true *
iris.unpaywall.landingpage https://doi.org/10.1371/journal.pcbi.1012973 *
iris.unpaywall.license cc-by *
iris.unpaywall.metadataCallLastModified 31/05/2025 04:58:32 -
iris.unpaywall.metadataCallLastModifiedMillisecond 1748660312237 -
iris.unpaywall.oastatus gold *
isi.authority.ancejournal PLOS COMPUTATIONAL BIOLOGY###1553-734X *
isi.category MC *
isi.category CO *
isi.contributor.affiliation Centre National de la Recherche Scientifique (CNRS) -
isi.contributor.affiliation Centre National de la Recherche Scientifique (CNRS) -
isi.contributor.affiliation University of Barcelona -
isi.contributor.affiliation Centre National de la Recherche Scientifique (CNRS) -
isi.contributor.affiliation University of Barcelona -
isi.contributor.country France -
isi.contributor.country France -
isi.contributor.country Spain -
isi.contributor.country France -
isi.contributor.country Spain -
isi.contributor.name Raphael -
isi.contributor.name Alessandro -
isi.contributor.name Gustavo -
isi.contributor.name Mathias -
isi.contributor.name Gorka -
isi.contributor.researcherId IUH-5781-2023 -
isi.contributor.researcherId AAI-7275-2020 -
isi.contributor.researcherId MDJ-7554-2025 -
isi.contributor.researcherId DYA-3437-2022 -
isi.contributor.researcherId LXI-5279-2024 -
isi.contributor.subaffiliation ENSEA -
isi.contributor.subaffiliation CNRS -
isi.contributor.subaffiliation Ctr Brain & Cognit -
isi.contributor.subaffiliation ENSEA -
isi.contributor.subaffiliation Ctr Brain & Cognit -
isi.contributor.surname Bergoin -
isi.contributor.surname Torcini -
isi.contributor.surname Deco -
isi.contributor.surname Quoy -
isi.contributor.surname Zamora-Lopez -
isi.date.issued 2025 *
isi.description.abstracteng The modular and hierarchical organization of the brain is believed to support the coexistence of segregated (specialization) and integrated (binding) information processes. A relevant question is yet to understand how such architecture naturally emerges and is sustained over time, given the plastic nature of the brain's wiring. Following evidences that the sensory cortices organize into assemblies under selective stimuli, it has been shown that stable neuronal assemblies can emerge due to targeted stimulation, embedding various forms of synaptic plasticity in presence of homeostatic and/or control mechanisms. Here, we show that simple spike-timing-dependent plasticity (STDP) rules, based only on pre- and post-synaptic spike times, can also lead to the stable encoding of memories in the absence of any control mechanism. We develop a model of spiking neurons, trained by stimuli targeting different sub-populations. The model satisfies some biologically plausible features: (i) it contains excitatory and inhibitory neurons with Hebbian and anti-Hebbian STDP; (ii) neither the neuronal activity nor the synaptic weights are frozen after the learning phase. Instead, the neurons are allowed to fire spontaneously while synaptic plasticity remains active. We find that only the combination of two inhibitory STDP sub-populations allows for the formation of stable modules in the network, with each sub-population playing a distinctive role. The Hebbian sub-population controls for the firing activity, while the anti-Hebbian neurons promote pattern selectivity. After the learning phase, the network settles into an asynchronous irregular resting-state. This post-learning activity is associated with spontaneous memory recalls which turn out to be fundamental for the long-term consolidation of the learned memories. Due to its simplicity, the introduced model can represent a test-bed for further investigations on the role played by STDP on memory storing and maintenance. *
isi.description.allpeopleoriginal Bergoin, R; Torcini, A; Deco, G; Quoy, M; Zamora-López, G; *
isi.document.sourcetype WOS.SCI *
isi.document.type Article *
isi.document.types Article *
isi.identifier.doi 10.1371/journal.pcbi.1012973 *
isi.identifier.eissn 1553-7358 *
isi.identifier.isi WOS:001473015000002 *
isi.journal.journaltitle PLOS COMPUTATIONAL BIOLOGY *
isi.journal.journaltitleabbrev PLOS COMPUT BIOL *
isi.language.original English *
isi.publisher.place 1160 BATTERY STREET, STE 100, SAN FRANCISCO, CA 94111 USA *
isi.relation.issue 4 *
isi.relation.volume 21 *
isi.title Emergence and maintenance of modularity in neural networks with Hebbian and anti-Hebbian inhibitory STDP *
scopus.authority.ancejournal PLOS COMPUTATIONAL BIOLOGY###1553-734X *
scopus.category 1105 *
scopus.category 2611 *
scopus.category 2303 *
scopus.category 1312 *
scopus.category 1311 *
scopus.category 2804 *
scopus.category 1703 *
scopus.contributor.affiliation University Medical Center Hamburg-Eppendorf (UKE) -
scopus.contributor.affiliation CNRS -
scopus.contributor.affiliation Instituciò Catalana de Recerca i Estudis Avançats (ICREA) -
scopus.contributor.affiliation CNRS -
scopus.contributor.affiliation Pompeu Fabra University -
scopus.contributor.afid 60005036 -
scopus.contributor.afid 60134716 -
scopus.contributor.afid 60032907 -
scopus.contributor.afid 60157987 -
scopus.contributor.afid 60032942 -
scopus.contributor.auid 58222813200 -
scopus.contributor.auid 56028770100 -
scopus.contributor.auid 7006674531 -
scopus.contributor.auid 57203005814 -
scopus.contributor.auid 22942674100 -
scopus.contributor.country Germany -
scopus.contributor.country France -
scopus.contributor.country Spain -
scopus.contributor.country Singapore -
scopus.contributor.country Spain -
scopus.contributor.dptid 126776847 -
scopus.contributor.dptid -
scopus.contributor.dptid -
scopus.contributor.dptid -
scopus.contributor.dptid -
scopus.contributor.name Raphaël -
scopus.contributor.name Alessandro -
scopus.contributor.name Gustavo -
scopus.contributor.name Mathias -
scopus.contributor.name Gorka -
scopus.contributor.subaffiliation Institute of Neural Information Processing;Center for Molecular Neurobiology (ZMNH); -
scopus.contributor.subaffiliation Laboratoire de Physique Théorique et Modélisation;UMR 8089;CY Cergy Paris Université; -
scopus.contributor.subaffiliation -
scopus.contributor.subaffiliation IPAL; -
scopus.contributor.subaffiliation Department of Information and Communication Technologies; -
scopus.contributor.surname Bergoin -
scopus.contributor.surname Torcini -
scopus.contributor.surname Deco -
scopus.contributor.surname Quoy -
scopus.contributor.surname Zamora-López -
scopus.date.issued 2025 *
scopus.description.abstracteng The modular and hierarchical organization of the brain is believed to support the coexistence of segregated (specialization) and integrated (binding) information processes. A relevant question is yet to understand how such architecture naturally emerges and is sustained over time, given the plastic nature of the brain’s wiring. Following evidences that the sensory cortices organize into assemblies under selective stimuli, it has been shown that stable neuronal assemblies can emerge due to targeted stimulation, embedding various forms of synaptic plasticity in presence of homeostatic and/or control mechanisms. Here, we show that simple spike-timing-dependent plasticity (STDP) rules, based only on pre- and post-synaptic spike times, can also lead to the stable encoding of memories in the absence of any control mechanism. We develop a model of spiking neurons, trained by stimuli targeting different sub-populations. The model satisfies some biologically plausible features: (i) it contains excitatory and inhibitory neurons with Hebbian and anti-Hebbian STDP; (ii) neither the neuronal activity nor the synaptic weights are frozen after the learning phase. Instead, the neurons are allowed to fire spontaneously while synaptic plasticity remains active. We find that only the combination of two inhibitory STDP sub-populations allows for the formation of stable modules in the network, with each sub-population playing a distinctive role. The Hebbian sub-population controls for the firing activity, while the anti-Hebbian neurons promote pattern selectivity. After the learning phase, the network settles into an asynchronous irregular resting-state. This post-learning activity is associated with spontaneous memory recalls which turn out to be fundamental for the long-term consolidation of the learned memories. Due to its simplicity, the introduced model can represent a test-bed for further investigations on the role played by STDP on memory storing and maintenance. *
scopus.description.allpeopleoriginal Bergoin R.; Torcini A.; Deco G.; Quoy M.; Zamora-Lopez G. *
scopus.differences scopus.description.allpeopleoriginal *
scopus.document.type ar *
scopus.document.types ar *
scopus.funding.funders 501100007175 - Conseil National de la Recherche Scientifique; 501100008530 - European Regional Development Fund; 100010661 - Horizon 2020 Framework Programme; 501100004100 - Labex; 501100001665 - Agence Nationale de la Recherche; *
scopus.funding.ids 945539; ANR-11-LBX-0023-01; ANR-18-CE37-0014; *
scopus.identifier.doi 10.1371/journal.pcbi.1012973 *
scopus.identifier.eissn 1553-7358 *
scopus.identifier.pmid 40262082 *
scopus.identifier.pui 2038431928 *
scopus.identifier.scopus 2-s2.0-105003821787 *
scopus.journal.sourceid 4000151810 *
scopus.language.iso eng *
scopus.publisher.name Public Library of Science *
scopus.relation.article e1012973 *
scopus.relation.issue 4 *
scopus.relation.volume 21 *
scopus.title Emergence and maintenance of modularity in neural networks with Hebbian and anti-Hebbian inhibitory STDP *
scopus.titleeng Emergence and maintenance of modularity in neural networks with Hebbian and anti-Hebbian inhibitory STDP *
Appare nelle tipologie: 01.01 Articolo in rivista
File in questo prodotto:
File Dimensione Formato  
journal.pcbi.1012973 (1).pdf

accesso aperto

Descrizione: Emergence and maintenance of modularity in neural networks with Hebbian and anti-Hebbian inhibitory STDP
Tipologia: Versione Editoriale (PDF)
Licenza: Creative commons
Dimensione 1.9 MB
Formato Adobe PDF
1.9 MB Adobe PDF Visualizza/Apri

I documenti in IRIS sono protetti da copyright e tutti i diritti sono riservati, salvo diversa indicazione.

Utilizza questo identificativo per citare o creare un link a questo documento: https://hdl.handle.net/20.500.14243/545441
Citazioni
  • ???jsp.display-item.citation.pmc??? ND
  • Scopus 2
  • ???jsp.display-item.citation.isi??? 1
social impact