Flexible neural connectivity under constraints on total connection strength.

Neural computation is determined by neurons' dynamics and circuit connectivity. Uncertain and dynamic environments may require neural hardware to adapt to different computational tasks, each requiring different connectivity configurations. At the same time, connectivity is subject to a variety...

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Main Authors: Gabriel Koch Ocker, Michael A Buice
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2020-08-01
Series:PLoS Computational Biology
Online Access:https://doi.org/10.1371/journal.pcbi.1008080
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author Gabriel Koch Ocker
Michael A Buice
author_facet Gabriel Koch Ocker
Michael A Buice
author_sort Gabriel Koch Ocker
collection DOAJ
description Neural computation is determined by neurons' dynamics and circuit connectivity. Uncertain and dynamic environments may require neural hardware to adapt to different computational tasks, each requiring different connectivity configurations. At the same time, connectivity is subject to a variety of constraints, placing limits on the possible computations a given neural circuit can perform. Here we examine the hypothesis that the organization of neural circuitry favors computational flexibility: that it makes many computational solutions available, given physiological constraints. From this hypothesis, we develop models of connectivity degree distributions based on constraints on a neuron's total synaptic weight. To test these models, we examine reconstructions of the mushroom bodies from the first instar larva and adult Drosophila melanogaster. We perform a Bayesian model comparison for two constraint models and a random wiring null model. Overall, we find that flexibility under a homeostatically fixed total synaptic weight describes Kenyon cell connectivity better than other models, suggesting a principle shaping the apparently random structure of Kenyon cell wiring. Furthermore, we find evidence that larval Kenyon cells are more flexible earlier in development, suggesting a mechanism whereby neural circuits begin as flexible systems that develop into specialized computational circuits.
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spelling doaj.art-a7951897f1244e279b535dede5683ddf2022-12-21T19:16:23ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582020-08-01168e100808010.1371/journal.pcbi.1008080Flexible neural connectivity under constraints on total connection strength.Gabriel Koch OckerMichael A BuiceNeural computation is determined by neurons' dynamics and circuit connectivity. Uncertain and dynamic environments may require neural hardware to adapt to different computational tasks, each requiring different connectivity configurations. At the same time, connectivity is subject to a variety of constraints, placing limits on the possible computations a given neural circuit can perform. Here we examine the hypothesis that the organization of neural circuitry favors computational flexibility: that it makes many computational solutions available, given physiological constraints. From this hypothesis, we develop models of connectivity degree distributions based on constraints on a neuron's total synaptic weight. To test these models, we examine reconstructions of the mushroom bodies from the first instar larva and adult Drosophila melanogaster. We perform a Bayesian model comparison for two constraint models and a random wiring null model. Overall, we find that flexibility under a homeostatically fixed total synaptic weight describes Kenyon cell connectivity better than other models, suggesting a principle shaping the apparently random structure of Kenyon cell wiring. Furthermore, we find evidence that larval Kenyon cells are more flexible earlier in development, suggesting a mechanism whereby neural circuits begin as flexible systems that develop into specialized computational circuits.https://doi.org/10.1371/journal.pcbi.1008080
spellingShingle Gabriel Koch Ocker
Michael A Buice
Flexible neural connectivity under constraints on total connection strength.
PLoS Computational Biology
title Flexible neural connectivity under constraints on total connection strength.
title_full Flexible neural connectivity under constraints on total connection strength.
title_fullStr Flexible neural connectivity under constraints on total connection strength.
title_full_unstemmed Flexible neural connectivity under constraints on total connection strength.
title_short Flexible neural connectivity under constraints on total connection strength.
title_sort flexible neural connectivity under constraints on total connection strength
url https://doi.org/10.1371/journal.pcbi.1008080
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