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The information theory of developmental pruning: Optimizing global network architectures using local synaptic rules

During development, biological neural networks produce more synapses and neurons than needed. Many of these synapses and neurons are later removed in a process known as neural pruning. Why networks should initially be over-populated, and the processes that determine which synapses and neurons are ul...

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Autores principales: Scholl, Carolin, Rule, Michael E., Hennig, Matthias H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Public Library of Science 2021
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8584672/
https://www.ncbi.nlm.nih.gov/pubmed/34634045
http://dx.doi.org/10.1371/journal.pcbi.1009458
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author Scholl, Carolin
Rule, Michael E.
Hennig, Matthias H.
author_facet Scholl, Carolin
Rule, Michael E.
Hennig, Matthias H.
author_sort Scholl, Carolin
collection PubMed
description During development, biological neural networks produce more synapses and neurons than needed. Many of these synapses and neurons are later removed in a process known as neural pruning. Why networks should initially be over-populated, and the processes that determine which synapses and neurons are ultimately pruned, remains unclear. We study the mechanisms and significance of neural pruning in model neural networks. In a deep Boltzmann machine model of sensory encoding, we find that (1) synaptic pruning is necessary to learn efficient network architectures that retain computationally-relevant connections, (2) pruning by synaptic weight alone does not optimize network size and (3) pruning based on a locally-available measure of importance based on Fisher information allows the network to identify structurally important vs. unimportant connections and neurons. This locally-available measure of importance has a biological interpretation in terms of the correlations between presynaptic and postsynaptic neurons, and implies an efficient activity-driven pruning rule. Overall, we show how local activity-dependent synaptic pruning can solve the global problem of optimizing a network architecture. We relate these findings to biology as follows: (I) Synaptic over-production is necessary for activity-dependent connectivity optimization. (II) In networks that have more neurons than needed, cells compete for activity, and only the most important and selective neurons are retained. (III) Cells may also be pruned due to a loss of synapses on their axons. This occurs when the information they convey is not relevant to the target population.
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spelling pubmed-85846722021-11-12 The information theory of developmental pruning: Optimizing global network architectures using local synaptic rules Scholl, Carolin Rule, Michael E. Hennig, Matthias H. PLoS Comput Biol Research Article During development, biological neural networks produce more synapses and neurons than needed. Many of these synapses and neurons are later removed in a process known as neural pruning. Why networks should initially be over-populated, and the processes that determine which synapses and neurons are ultimately pruned, remains unclear. We study the mechanisms and significance of neural pruning in model neural networks. In a deep Boltzmann machine model of sensory encoding, we find that (1) synaptic pruning is necessary to learn efficient network architectures that retain computationally-relevant connections, (2) pruning by synaptic weight alone does not optimize network size and (3) pruning based on a locally-available measure of importance based on Fisher information allows the network to identify structurally important vs. unimportant connections and neurons. This locally-available measure of importance has a biological interpretation in terms of the correlations between presynaptic and postsynaptic neurons, and implies an efficient activity-driven pruning rule. Overall, we show how local activity-dependent synaptic pruning can solve the global problem of optimizing a network architecture. We relate these findings to biology as follows: (I) Synaptic over-production is necessary for activity-dependent connectivity optimization. (II) In networks that have more neurons than needed, cells compete for activity, and only the most important and selective neurons are retained. (III) Cells may also be pruned due to a loss of synapses on their axons. This occurs when the information they convey is not relevant to the target population. Public Library of Science 2021-10-11 /pmc/articles/PMC8584672/ /pubmed/34634045 http://dx.doi.org/10.1371/journal.pcbi.1009458 Text en © 2021 Scholl et al https://creativecommons.org/licenses/by/4.0/This is an open access article distributed under the terms of the Creative Commons Attribution License (https://creativecommons.org/licenses/by/4.0/) , which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
spellingShingle Research Article
Scholl, Carolin
Rule, Michael E.
Hennig, Matthias H.
The information theory of developmental pruning: Optimizing global network architectures using local synaptic rules
title The information theory of developmental pruning: Optimizing global network architectures using local synaptic rules
title_full The information theory of developmental pruning: Optimizing global network architectures using local synaptic rules
title_fullStr The information theory of developmental pruning: Optimizing global network architectures using local synaptic rules
title_full_unstemmed The information theory of developmental pruning: Optimizing global network architectures using local synaptic rules
title_short The information theory of developmental pruning: Optimizing global network architectures using local synaptic rules
title_sort information theory of developmental pruning: optimizing global network architectures using local synaptic rules
topic Research Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC8584672/
https://www.ncbi.nlm.nih.gov/pubmed/34634045
http://dx.doi.org/10.1371/journal.pcbi.1009458
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