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PID2019-105772GB-I00\/AEI\/10.13039\/501100011033"],"award-info":[{"award-number":["ref. PID2019-105772GB-I00\/AEI\/10.13039\/501100011033"]}]},{"name":"CNRS, IPAL"}],"content-domain":{"domain":["www.ploscompbiol.org"],"crossmark-restriction":false},"short-container-title":["PLoS Comput Biol"],"abstract":"<jats:p>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\u2019s 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.<\/jats:p>","DOI":"10.1371\/journal.pcbi.1012973","type":"journal-article","created":{"date-parts":[[2025,4,22]],"date-time":"2025-04-22T16:04:23Z","timestamp":1745337863000},"page":"e1012973","update-policy":"https:\/\/doi.org\/10.1371\/journal.pcbi.corrections_policy","source":"Crossref","is-referenced-by-count":5,"title":["Emergence and maintenance of modularity in neural networks with Hebbian and anti-Hebbian inhibitory 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Vogels","year":"2011","journal-title":"Science"},{"issue":"6300","key":"pcbi.1012973.ref041","doi-asserted-by":"crossref","first-page":"691","DOI":"10.1126\/science.aaf7560","article-title":"Imprinting and recalling cortical ensembles","volume":"353","author":"L Carrillo-Reid","year":"2016","journal-title":"Science"},{"key":"pcbi.1012973.ref042","first-page":"2021","article-title":"Assembly formation is stabilized by Parvalbumin neurons and accelerated by Somatostatin neurons","author":"F Lagzi","year":"2021","journal-title":"BioRxiv"},{"issue":"5293","key":"pcbi.1012973.ref043","doi-asserted-by":"crossref","first-page":"1724","DOI":"10.1126\/science.274.5293.1724","article-title":"Chaos in neuronal networks with balanced excitatory and inhibitory activity","volume":"274","author":"C Van Vreeswijk","year":"1996","journal-title":"Science"},{"key":"pcbi.1012973.ref044","doi-asserted-by":"crossref","first-page":"183","DOI":"10.1023\/A:1008925309027","article-title":"Dynamics of sparsely connected networks of excitatory and inhibitory spiking neurons","volume":"8","author":"N Brunel","year":"2000","journal-title":"J Comput Neurosci"},{"issue":"24","key":"pcbi.1012973.ref045","doi-asserted-by":"crossref","first-page":"10464","DOI":"10.1523\/JNEUROSCI.18-24-10464.1998","article-title":"Synaptic modifications in cultured hippocampal neurons: dependence on spike timing, synaptic strength, and postsynaptic cell type","volume":"18","author":"G Bi","year":"1998","journal-title":"J Neurosci"},{"issue":"1","key":"pcbi.1012973.ref046","doi-asserted-by":"crossref","first-page":"139","DOI":"10.1146\/annurev.neuro.24.1.139","article-title":"Synaptic modification by correlated activity: Hebb\u2019s postulate revisited","volume":"24","author":"Gq Bi","year":"2001","journal-title":"Annu Rev Neurosci"},{"issue":"2","key":"pcbi.1012973.ref047","doi-asserted-by":"crossref","first-page":"1362","DOI":"10.4249\/scholarpedia.1362","article-title":"Spike-timing dependent 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cortex","volume":"2","author":"EL Bienenstock","year":"1982","journal-title":"J Neurosci"},{"issue":"7","key":"pcbi.1012973.ref051","doi-asserted-by":"crossref","first-page":"916","DOI":"10.1038\/nn1486","article-title":"Hebbian LTP in feed-forward inhibitory interneurons and the temporal fidelity of input discrimination","volume":"8","author":"K Lamsa","year":"2005","journal-title":"Nat Neurosci"},{"issue":"5816","key":"pcbi.1012973.ref052","doi-asserted-by":"crossref","first-page":"1262","DOI":"10.1126\/science.1137450","article-title":"Anti-Hebbian long-term potentiation in the hippocampal feedback inhibitory circuit","volume":"315","author":"KP Lamsa","year":"2007","journal-title":"Science."},{"issue":"1","key":"pcbi.1012973.ref053","doi-asserted-by":"crossref","first-page":"334","DOI":"10.1523\/JNEUROSCI.13-01-00334.1993","article-title":"The highly irregular firing of cortical cells is inconsistent with temporal integration of random EPSPs","volume":"13","author":"WR Softky","year":"1993","journal-title":"J Neurosci"},{"issue":"2","key":"pcbi.1012973.ref054","doi-asserted-by":"crossref","first-page":"233","DOI":"10.1137\/0146017","article-title":"Parabolic bursting in an excitable system coupled with a slow oscillation","volume":"46","author":"GB Ermentrout","year":"1986","journal-title":"SIAM J Appl Math"},{"issue":"4","key":"pcbi.1012973.ref055","first-page":"419","article-title":"Neuronal spike trains and stochastic point processes: II","volume":"7","author":"DH Perkel","year":"1967","journal-title":"Simultaneous spike trains. Biophys J"},{"issue":"7","key":"pcbi.1012973.ref056","doi-asserted-by":"crossref","first-page":"619","DOI":"10.1093\/cercor\/7.7.619","article-title":"Inhibitory synaptogenesis in mouse somatosensory cortex","volume":"7","author":"J De Felipe","year":"1997","journal-title":"Cereb Cortex"},{"issue":"11","key":"pcbi.1012973.ref057","doi-asserted-by":"crossref","first-page":"e1004632","DOI":"10.1371\/journal.pcbi.1004632","article-title":"Remodeling and tenacity of inhibitory synapses: relationships with network activity and neighboring excitatory synapses","volume":"11","author":"A Rubinski","year":"2015","journal-title":"PLoS Comput Biol"},{"issue":"3","key":"pcbi.1012973.ref058","doi-asserted-by":"crossref","first-page":"454","DOI":"10.1038\/nn.4231","article-title":"PV plasticity sustained through D1\/5 dopamine signaling required for long-term memory consolidation","volume":"19","author":"S Karunakaran","year":"2016","journal-title":"Nat Neurosci"},{"issue":"26","key":"pcbi.1012973.ref059","doi-asserted-by":"crossref","first-page":"6666","DOI":"10.1073\/pnas.1701812114","article-title":"Inhibitory engrams in perception and memory","volume":"114","author":"HC Barron","year":"2017","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"10","key":"pcbi.1012973.ref060","doi-asserted-by":"crossref","first-page":"1463","DOI":"10.1038\/s41593-018-0226-x","article-title":"Inhibitory connectivity defines the realm of excitatory plasticity","volume":"21","author":"G Mongillo","year":"2018","journal-title":"Nat Neurosci"},{"key":"pcbi.1012973.ref061","doi-asserted-by":"crossref","first-page":"689952","DOI":"10.3389\/fnmol.2021.689952","article-title":"Roles and transcriptional responses of inhibitory neurons in learning and memory","volume":"14","author":"C Giorgi","year":"2021","journal-title":"Front Mol Neurosci"},{"key":"pcbi.1012973.ref062","doi-asserted-by":"crossref","unstructured":"Arcelli P, Frassoni C, Regondi M, De Biasi S, Spreafico R. GABAergic neurons in mammalian thalamus: a marker of thalamic complexity? 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Morphometrical-statistical structure analysis of human striatum, pallidum and subthalamic nucleus. 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A robust balancing mechanism for spiking neural networks. Chaos 2024;34(4):041102. doi: 10.1063\/5.0199298","DOI":"10.1063\/5.0199298"},{"issue":"2","key":"pcbi.1012973.ref089","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1007\/BF02331346","article-title":"Forming sparse representations by local anti-Hebbian learning","volume":"64","author":"P F\u00f6ldi\u00e1k","year":"1990","journal-title":"Biol Cybern"},{"issue":"1","key":"pcbi.1012973.ref090","doi-asserted-by":"crossref","first-page":"e1002334","DOI":"10.1371\/journal.pcbi.1002334","article-title":"Balancing feed-forward excitation and inhibition via Hebbian inhibitory synaptic plasticity","volume":"8","author":"Y Luz","year":"2012","journal-title":"PLoS Comput Biol"},{"key":"pcbi.1012973.ref091","doi-asserted-by":"crossref","first-page":"53","DOI":"10.3389\/fncom.2014.00053","article-title":"Excitatory and inhibitory STDP jointly tune feedforward neural circuits to selectively propagate correlated spiking activity","volume":"8","author":"FI Kleberg","year":"2014","journal-title":"Front Comput Neurosci"},{"issue":"6407","key":"pcbi.1012973.ref092","doi-asserted-by":"crossref","first-page":"31","DOI":"10.1038\/361031a0","article-title":"A synaptic model of memory: long-term potentiation in the hippocampus","volume":"361","author":"TV Bliss","year":"1993","journal-title":"Nature"},{"issue":"5451","key":"pcbi.1012973.ref093","doi-asserted-by":"crossref","first-page":"248","DOI":"10.1126\/science.287.5451.248","article-title":"Memory\u2013a century of consolidation","volume":"287","author":"JL McGaugh","year":"2000","journal-title":"Science"},{"issue":"1","key":"pcbi.1012973.ref094","doi-asserted-by":"crossref","first-page":"5","DOI":"10.1016\/j.neuron.2004.09.012","article-title":"LTP and LTD: an embarrassment of riches","volume":"44","author":"RC Malenka","year":"2004","journal-title":"Neuron"},{"key":"pcbi.1012973.ref095","doi-asserted-by":"crossref","first-page":"609645","DOI":"10.3389\/fnsys.2021.609645","article-title":"Up and down states during slow oscillations in slow-wave sleep and different levels of anesthesia","volume":"15","author":"M Torao-Angosto","year":"2021","journal-title":"Front Syst Neurosci"},{"issue":"6","key":"pcbi.1012973.ref096","doi-asserted-by":"crossref","first-page":"e13562","DOI":"10.1111\/jsr.13562","article-title":"No difference between slow oscillation up-and down-state cueing for memory consolidation during sleep","volume":"31","author":"JY Wang","year":"2022","journal-title":"J Sleep Res"},{"issue":"2","key":"pcbi.1012973.ref097","doi-asserted-by":"crossref","first-page":"169","DOI":"10.1016\/0959-4388(95)80023-9","article-title":"Retrograde amnesia and memory consolidation: a neurobiological perspective","volume":"5","author":"LR Squire","year":"1995","journal-title":"Curr Opin 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Buzsaki","year":"2004","journal-title":"Science"},{"issue":"10","key":"pcbi.1012973.ref105","doi-asserted-by":"crossref","first-page":"474","DOI":"10.1016\/j.tics.2005.08.011","article-title":"A mechanism for cognitive dynamics: neuronal communication through neuronal coherence","volume":"9","author":"P Fries","year":"2005 Oct","journal-title":"Trends Cogn Sci"},{"key":"pcbi.1012973.ref106","article-title":"The noisy brain: stochastic dynamics as a principle of brain function","author":"ET Rolls","year":"2010"},{"issue":"8","key":"pcbi.1012973.ref107","doi-asserted-by":"crossref","first-page":"2554","DOI":"10.1073\/pnas.79.8.2554","article-title":"Neural networks and physical systems with emergent collective computational abilities","volume":"79","author":"JJ Hopfield","year":"1982","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"14","key":"pcbi.1012973.ref108","doi-asserted-by":"crossref","first-page":"1530","DOI":"10.1103\/PhysRevLett.55.1530","article-title":"Storing infinite numbers of patterns in a spin-glass model of neural networks","volume":"55","author":"DJ Amit","year":"1985","journal-title":"Phys Rev Lett"},{"issue":"7045","key":"pcbi.1012973.ref109","doi-asserted-by":"crossref","first-page":"1102","DOI":"10.1038\/nature03687","article-title":"Invariant visual representation by single neurons in the human brain","volume":"435","author":"RQ Quiroga","year":"2005","journal-title":"Nature"},{"issue":"2","key":"pcbi.1012973.ref110","doi-asserted-by":"crossref","first-page":"e1007544","DOI":"10.1371\/journal.pcbi.1007544","article-title":"Nonlinear mixed selectivity supports reliable neural computation","volume":"16","author":"WJ Johnston","year":"2020","journal-title":"PLoS Comput Biol"},{"issue":"5958","key":"pcbi.1012973.ref111","doi-asserted-by":"crossref","first-page":"1419","DOI":"10.1126\/science.1175509","article-title":"GABAergic hub neurons orchestrate synchrony in developing hippocampal networks","volume":"326","author":"P Bonifazi","year":"2009","journal-title":"Science"},{"issue":"44","key":"pcbi.1012973.ref112","doi-asserted-by":"crossref","first-page":"15775","DOI":"10.1523\/JNEUROSCI.3539-11.2011","article-title":"Rich-club organization of the human connectome","volume":"31","author":"MP Van Den Heuvel","year":"2011","journal-title":"J Neurosci"},{"issue":"4","key":"pcbi.1012973.ref113","doi-asserted-by":"crossref","first-page":"408","DOI":"10.1152\/jn.1957.20.4.408","article-title":"Modality and topographic properties of single neurons of cat\u2019s somatic sensory cortex","volume":"20","author":"VB Mountcastle","year":"1957","journal-title":"J Neurophysiol"},{"issue":"2","key":"pcbi.1012973.ref114","doi-asserted-by":"crossref","first-page":"107","DOI":"10.1016\/S0361-9230(97)00094-4","article-title":"Topographic maps are fundamental to sensory processing","volume":"44","author":"JH Kaas","year":"1997","journal-title":"Brain Res Bull"},{"issue":"4","key":"pcbi.1012973.ref115","doi-asserted-by":"crossref","first-page":"498","DOI":"10.1016\/S0959-4388(00)00240-3","article-title":"The organization of sensory cortex","volume":"11","author":"JH Kaas","year":"2001","journal-title":"Curr Opin Neurobiol"},{"issue":"7233","key":"pcbi.1012973.ref116","doi-asserted-by":"crossref","first-page":"1142","DOI":"10.1038\/nature07709","article-title":"The subcellular organization of neocortical excitatory connections","volume":"457","author":"L Petreanu","year":"2009","journal-title":"Nature"},{"issue":"6197","key":"pcbi.1012973.ref117","doi-asserted-by":"crossref","first-page":"660","DOI":"10.1126\/science.1254126","article-title":"Long-range and local circuits for top-down modulation of visual cortex processing","volume":"345","author":"S Zhang","year":"2014","journal-title":"Science"},{"issue":"2","key":"pcbi.1012973.ref118","doi-asserted-by":"crossref","first-page":"179","DOI":"10.1016\/j.conb.2013.01.021","article-title":"The long and short of GABAergic neurons","volume":"23","author":"A Caputi","year":"2013","journal-title":"Curr Opin Neurobiol"},{"key":"pcbi.1012973.ref119","doi-asserted-by":"crossref","unstructured":"Gerstner W, Kistler WM, Naud R, Paninski L. Neuronal dynamics: from single neurons to networks and models of cognition. Cambridge University Press; 2014.","DOI":"10.1017\/CBO9781107447615"},{"issue":"11","key":"pcbi.1012973.ref120","doi-asserted-by":"crossref","first-page":"2519","DOI":"10.1162\/089976600300014827","article-title":"On the computational power of winner-take-all","volume":"12","author":"W Maass","year":"2000","journal-title":"Neural Comput"},{"key":"pcbi.1012973.ref121","doi-asserted-by":"crossref","DOI":"10.1017\/CBO9780511574566","article-title":"Corticonics: neural circuits of the cerebral cortex","author":"M Abeles","year":"1991"},{"key":"pcbi.1012973.ref122","doi-asserted-by":"crossref","DOI":"10.1002\/9783527683147","article-title":"Stochastic numerical methods: an introduction for students and scientists","author":"R Toral","year":"2014"},{"issue":"13","key":"pcbi.1012973.ref123","doi-asserted-by":"crossref","first-page":"4240","DOI":"10.1523\/JNEUROSCI.16-13-04240.1996","article-title":"Stimulus specificity of phase-locked and non-phase-locked 40 Hz visual responses in human","volume":"16","author":"C Tallon-Baudry","year":"1996","journal-title":"J Neurosci"},{"key":"pcbi.1012973.ref124","doi-asserted-by":"crossref","first-page":"346","DOI":"10.1007\/s002210100682","article-title":"Human EEG responses to 1\u2013100 Hz flicker: resonance phenomena in visual cortex and their potential correlation to cognitive phenomena","volume":"137","author":"CS Herrmann","year":"2001","journal-title":"Exp Brain Res"},{"key":"pcbi.1012973.ref125","first-page":"1","article-title":"Biologically plausible models of homeostasis and STDP: stability and learning in spiking neural networks. In: The 2013 International Joint Conference on Neural Networks (IJCNN). IEEE","author":"KD Carlson","year":"2013"},{"key":"pcbi.1012973.ref126","doi-asserted-by":"crossref","first-page":"235","DOI":"10.1146\/annurev.psych.55.090902.141555","article-title":"The psychology and neuroscience of forgetting","volume":"55","author":"JT Wixted","year":"2004","journal-title":"Annu Rev Psychol"},{"issue":"3","key":"pcbi.1012973.ref127","doi-asserted-by":"crossref","first-page":"111","DOI":"10.1016\/j.tics.2013.01.001","article-title":"Decay happens: the role of active forgetting in memory","volume":"17","author":"O Hardt","year":"2013","journal-title":"Trends Cogn Sci"},{"issue":"16","key":"pcbi.1012973.ref128","doi-asserted-by":"crossref","first-page":"9401","DOI":"10.1073\/pnas.161493498","article-title":"A hebbian form of long-term potentiation dependent on mGluR1a in hippocampal inhibitory interneurons","volume":"98","author":"Y Perez","year":"2001","journal-title":"Proc Natl Acad Sci U S A"},{"issue":"6","key":"pcbi.1012973.ref129","doi-asserted-by":"crossref","first-page":"823","DOI":"10.1016\/S0893-6080(05)80127-3","article-title":"Efficient information transfer and anti-Hebbian neural networks","volume":"6","author":"MD Plumbley","year":"1993","journal-title":"Neural Networks"},{"key":"pcbi.1012973.ref130","doi-asserted-by":"crossref","unstructured":"Jin Y, Li P. AP-STDP: A novel self-organizing mechanism for efficient reservoir computing. In: 2016 International Joint Conference on Neural Networks (IJCNN). IEEE; 2016. pp. 1158\u201365.","DOI":"10.1109\/IJCNN.2016.7727328"},{"issue":"12","key":"pcbi.1012973.ref131","doi-asserted-by":"crossref","first-page":"e1002836","DOI":"10.1371\/journal.pcbi.1002836","article-title":"Soft-bound synaptic plasticity increases storage capacity","volume":"8","author":"MC Van Rossum","year":"2012","journal-title":"PLoS Comput Biol"},{"issue":"10","key":"pcbi.1012973.ref132","doi-asserted-by":"crossref","first-page":"e25339","DOI":"10.1371\/journal.pone.0025339","article-title":"Stability versus neuronal specialization for STDP: long-tail weight distributions solve the dilemma","volume":"6","author":"M Gilson","year":"2011","journal-title":"PLoS One"},{"key":"pcbi.1012973.ref133","article-title":"Chemical oscillations, waves, and turbulence. 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