Bayesian computation emerges in generic cortical microcircuits through spike-timing-dependent plasticity
The principles by which networks of neurons compute, and how spike-timing dependent plasticity (STDP) of synaptic weights generates and maintains their computational function, are unknown. Preceding work has shown that soft winner-take-all (WTA) circuits, where pyramidal neurons inhibit each other v...
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description | The principles by which networks of neurons compute, and how spike-timing dependent plasticity (STDP) of synaptic weights generates and maintains their computational function, are unknown. Preceding work has shown that soft winner-take-all (WTA) circuits, where pyramidal neurons inhibit each other via interneurons, are a common motif of cortical microcircuits. We show through theoretical analysis and computer simulations that Bayesian computation is induced in these network motifs through STDP in combination with activity-dependent changes in the excitability of neurons. The fundamental components of this emergent Bayesian computation are priors that result from adaptation of neuronal excitability and implicit generative models for hidden causes that are created in the synaptic weights through STDP. In fact, a surprising result is that STDP is able to approximate a powerful principle for fitting such implicit generative models to high-dimensional spike inputs: Expectation Maximization. Our results suggest that the experimentally observed spontaneous activity and trial-to-trial variability of cortical neurons are essential features of their information processing capability, since their functional role is to represent probability distributions rather than static neural codes. Furthermore it suggests networks of Bayesian computation modules as a new model for distributed information processing in the cortex. |
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Preceding work has shown that soft winner-take-all (WTA) circuits, where pyramidal neurons inhibit each other via interneurons, are a common motif of cortical microcircuits. We show through theoretical analysis and computer simulations that Bayesian computation is induced in these network motifs through STDP in combination with activity-dependent changes in the excitability of neurons. The fundamental components of this emergent Bayesian computation are priors that result from adaptation of neuronal excitability and implicit generative models for hidden causes that are created in the synaptic weights through STDP. In fact, a surprising result is that STDP is able to approximate a powerful principle for fitting such implicit generative models to high-dimensional spike inputs: Expectation Maximization. Our results suggest that the experimentally observed spontaneous activity and trial-to-trial variability of cortical neurons are essential features of their information processing capability, since their functional role is to represent probability distributions rather than static neural codes. Furthermore it suggests networks of Bayesian computation modules as a new model for distributed information processing in the cortex.</description><identifier>ISSN: 1553-7358</identifier><identifier>ISSN: 1553-734X</identifier><identifier>EISSN: 1553-7358</identifier><identifier>DOI: 10.1371/journal.pcbi.1003037</identifier><identifier>PMID: 23633941</identifier><language>eng</language><publisher>United States: Public Library of Science</publisher><subject>Action Potentials - physiology ; Animals ; Bayes Theorem ; Bayesian statistical decision theory ; Biology ; Brain - physiology ; Computational biology ; Computational Biology - methods ; Computer Simulation ; Experiments ; Humans ; Models, Neurological ; Nerve Net - physiology ; Neural circuitry ; Neural networks ; Neuronal Plasticity - physiology ; Neurons ; Neurons - physiology ; Neuroplasticity ; Physiological aspects ; Probability ; Studies ; Synapses - physiology ; Synaptic Transmission - physiology</subject><ispartof>PLoS computational biology, 2013-04, Vol.9 (4), p.e1003037-e1003037</ispartof><rights>COPYRIGHT 2013 Public Library of Science</rights><rights>2013 Nessler et al 2013 Nessler et al</rights><rights>2013 Nessler et al. This is an open-access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited: Nessler B, Pfeiffer M, Buesing L, Maass W (2013) Bayesian Computation Emerges in Generic Cortical Microcircuits through Spike-Timing-Dependent Plasticity. 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Preceding work has shown that soft winner-take-all (WTA) circuits, where pyramidal neurons inhibit each other via interneurons, are a common motif of cortical microcircuits. We show through theoretical analysis and computer simulations that Bayesian computation is induced in these network motifs through STDP in combination with activity-dependent changes in the excitability of neurons. The fundamental components of this emergent Bayesian computation are priors that result from adaptation of neuronal excitability and implicit generative models for hidden causes that are created in the synaptic weights through STDP. In fact, a surprising result is that STDP is able to approximate a powerful principle for fitting such implicit generative models to high-dimensional spike inputs: Expectation Maximization. Our results suggest that the experimentally observed spontaneous activity and trial-to-trial variability of cortical neurons are essential features of their information processing capability, since their functional role is to represent probability distributions rather than static neural codes. Furthermore it suggests networks of Bayesian computation modules as a new model for distributed information processing in the cortex.</description><subject>Action Potentials - physiology</subject><subject>Animals</subject><subject>Bayes Theorem</subject><subject>Bayesian statistical decision theory</subject><subject>Biology</subject><subject>Brain - physiology</subject><subject>Computational biology</subject><subject>Computational Biology - methods</subject><subject>Computer Simulation</subject><subject>Experiments</subject><subject>Humans</subject><subject>Models, Neurological</subject><subject>Nerve Net - physiology</subject><subject>Neural circuitry</subject><subject>Neural networks</subject><subject>Neuronal Plasticity - physiology</subject><subject>Neurons</subject><subject>Neurons - physiology</subject><subject>Neuroplasticity</subject><subject>Physiological aspects</subject><subject>Probability</subject><subject>Studies</subject><subject>Synapses - physiology</subject><subject>Synaptic Transmission - physiology</subject><issn>1553-7358</issn><issn>1553-734X</issn><issn>1553-7358</issn><fulltext>true</fulltext><rsrctype>article</rsrctype><creationdate>2013</creationdate><recordtype>article</recordtype><sourceid>EIF</sourceid><sourceid>DOA</sourceid><recordid>eNqVkk1v1DAQhiMEoqXwDxDkCIcscezE9gWpVAVWqkDi42w5ziTrJbGD7aDuv2eW3VbdI_LB1viZ1zPjN8teknJFKCfvtn4JTo-r2bR2RcqSlpQ_ys5JXdOC01o8fnA-y57FuEWmFrJ5mp1VtKFUMnKebT7oHUSrXW78NC9JJ-tdDhOEAWJuXT6Ag2ANXodkjR7zyZrgjQ1msSnmaRP8MmzyONtfUCQ7WTcUHczgOnApn0cdMc2m3fPsSa_HCC-O-0X28-P1j6vPxc3XT-ury5vCNJykQrbQNyB7DQ3taFuVjaaEdj3TNWMla3mlBTHMQGc63lQNYRUxFPup6poJ09GL7PVBdx59VMchRUVoTQTnFSNIrA9E5_VWzcFOOuyU11b9C_gwKL3vdQTFJaMEDG8ZFawVXSs4JTVnksle1Fyi1vvja0s7YU3Yc9DjiejpjbMbNfg_Cj-gKSuBAm-OAsH_XiAmNdloYBy1A7_s62acCylJg-jqgA4aS7Ou96hocHWAf-Id9BbjlxSngXXLvfbbkwRkEtymQS8xqvX3b__Bfjll2YFFI8QYoL_vl5Rq7827sau9N9XRm5j26uGs7pPuzEj_AhuR4pw</recordid><startdate>20130401</startdate><enddate>20130401</enddate><creator>Nessler, Bernhard</creator><creator>Pfeiffer, Michael</creator><creator>Buesing, Lars</creator><creator>Maass, Wolfgang</creator><general>Public Library of Science</general><general>Public Library of Science (PLoS)</general><scope>CGR</scope><scope>CUY</scope><scope>CVF</scope><scope>ECM</scope><scope>EIF</scope><scope>NPM</scope><scope>AAYXX</scope><scope>CITATION</scope><scope>ISN</scope><scope>ISR</scope><scope>7X8</scope><scope>5PM</scope><scope>DOA</scope></search><sort><creationdate>20130401</creationdate><title>Bayesian computation emerges in generic cortical microcircuits through spike-timing-dependent plasticity</title><author>Nessler, Bernhard ; Pfeiffer, Michael ; Buesing, Lars ; Maass, Wolfgang</author></sort><facets><frbrtype>5</frbrtype><frbrgroupid>cdi_FETCH-LOGICAL-c671t-9bef6e9fae63d3b206a313df4a54404b72a81c4cedcd76261421c323625548cd3</frbrgroupid><rsrctype>articles</rsrctype><prefilter>articles</prefilter><language>eng</language><creationdate>2013</creationdate><topic>Action Potentials - physiology</topic><topic>Animals</topic><topic>Bayes Theorem</topic><topic>Bayesian statistical decision theory</topic><topic>Biology</topic><topic>Brain - physiology</topic><topic>Computational biology</topic><topic>Computational Biology - methods</topic><topic>Computer Simulation</topic><topic>Experiments</topic><topic>Humans</topic><topic>Models, Neurological</topic><topic>Nerve Net - physiology</topic><topic>Neural circuitry</topic><topic>Neural networks</topic><topic>Neuronal Plasticity - physiology</topic><topic>Neurons</topic><topic>Neurons - physiology</topic><topic>Neuroplasticity</topic><topic>Physiological aspects</topic><topic>Probability</topic><topic>Studies</topic><topic>Synapses - physiology</topic><topic>Synaptic Transmission - physiology</topic><toplevel>peer_reviewed</toplevel><toplevel>online_resources</toplevel><creatorcontrib>Nessler, Bernhard</creatorcontrib><creatorcontrib>Pfeiffer, Michael</creatorcontrib><creatorcontrib>Buesing, Lars</creatorcontrib><creatorcontrib>Maass, Wolfgang</creatorcontrib><collection>Medline</collection><collection>MEDLINE</collection><collection>MEDLINE (Ovid)</collection><collection>MEDLINE</collection><collection>MEDLINE</collection><collection>PubMed</collection><collection>CrossRef</collection><collection>Gale In Context: Canada</collection><collection>Gale In Context: Science</collection><collection>MEDLINE - Academic</collection><collection>PubMed Central (Full Participant titles)</collection><collection>DOAJ Directory of Open Access Journals</collection><jtitle>PLoS computational biology</jtitle></facets><delivery><delcategory>Remote Search Resource</delcategory><fulltext>fulltext</fulltext></delivery><addata><au>Nessler, Bernhard</au><au>Pfeiffer, Michael</au><au>Buesing, Lars</au><au>Maass, Wolfgang</au><au>Sporns, Olaf</au><format>journal</format><genre>article</genre><ristype>JOUR</ristype><atitle>Bayesian computation emerges in generic cortical microcircuits through spike-timing-dependent plasticity</atitle><jtitle>PLoS computational biology</jtitle><addtitle>PLoS Comput Biol</addtitle><date>2013-04-01</date><risdate>2013</risdate><volume>9</volume><issue>4</issue><spage>e1003037</spage><epage>e1003037</epage><pages>e1003037-e1003037</pages><issn>1553-7358</issn><issn>1553-734X</issn><eissn>1553-7358</eissn><abstract>The principles by which networks of neurons compute, and how spike-timing dependent plasticity (STDP) of synaptic weights generates and maintains their computational function, are unknown. Preceding work has shown that soft winner-take-all (WTA) circuits, where pyramidal neurons inhibit each other via interneurons, are a common motif of cortical microcircuits. We show through theoretical analysis and computer simulations that Bayesian computation is induced in these network motifs through STDP in combination with activity-dependent changes in the excitability of neurons. The fundamental components of this emergent Bayesian computation are priors that result from adaptation of neuronal excitability and implicit generative models for hidden causes that are created in the synaptic weights through STDP. In fact, a surprising result is that STDP is able to approximate a powerful principle for fitting such implicit generative models to high-dimensional spike inputs: Expectation Maximization. Our results suggest that the experimentally observed spontaneous activity and trial-to-trial variability of cortical neurons are essential features of their information processing capability, since their functional role is to represent probability distributions rather than static neural codes. Furthermore it suggests networks of Bayesian computation modules as a new model for distributed information processing in the cortex.</abstract><cop>United States</cop><pub>Public Library of Science</pub><pmid>23633941</pmid><doi>10.1371/journal.pcbi.1003037</doi><oa>free_for_read</oa></addata></record> |
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subjects | Action Potentials - physiology Animals Bayes Theorem Bayesian statistical decision theory Biology Brain - physiology Computational biology Computational Biology - methods Computer Simulation Experiments Humans Models, Neurological Nerve Net - physiology Neural circuitry Neural networks Neuronal Plasticity - physiology Neurons Neurons - physiology Neuroplasticity Physiological aspects Probability Studies Synapses - physiology Synaptic Transmission - physiology |
title | Bayesian computation emerges in generic cortical microcircuits through spike-timing-dependent plasticity |
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