Discovering sparse control strategies in neural activity.

Biological circuits such as neural or gene regulation networks use internal states to map sensory input to an adaptive repertoire of behavior. Characterizing this mapping is a major challenge for systems biology. Though experiments that probe internal states are developing rapidly, organismal comple...

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Main Authors: Edward D Lee, Xiaowen Chen, Bryan C Daniels
Format: Article
Language:English
Published: Public Library of Science (PLoS) 2022-05-01
Series:PLoS Computational Biology
Online Access:https://doi.org/10.1371/journal.pcbi.1010072
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author Edward D Lee
Xiaowen Chen
Bryan C Daniels
author_facet Edward D Lee
Xiaowen Chen
Bryan C Daniels
author_sort Edward D Lee
collection DOAJ
description Biological circuits such as neural or gene regulation networks use internal states to map sensory input to an adaptive repertoire of behavior. Characterizing this mapping is a major challenge for systems biology. Though experiments that probe internal states are developing rapidly, organismal complexity presents a fundamental obstacle given the many possible ways internal states could map to behavior. Using C. elegans as an example, we propose a protocol for systematic perturbation of neural states that limits experimental complexity and could eventually help characterize collective aspects of the neural-behavioral map. We consider experimentally motivated small perturbations-ones that are most likely to preserve natural dynamics and are closer to internal control mechanisms-to neural states and their impact on collective neural activity. Then, we connect such perturbations to the local information geometry of collective statistics, which can be fully characterized using pairwise perturbations. Applying the protocol to a minimal model of C. elegans neural activity, we find that collective neural statistics are most sensitive to a few principal perturbative modes. Dominant eigenvalues decay initially as a power law, unveiling a hierarchy that arises from variation in individual neural activity and pairwise interactions. Highest-ranking modes tend to be dominated by a few, "pivotal" neurons that account for most of the system's sensitivity, suggesting a sparse mechanism of collective control.
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spelling doaj.art-aa77872b716b4ecfa69278e898f1e0832022-12-22T03:00:34ZengPublic Library of Science (PLoS)PLoS Computational Biology1553-734X1553-73582022-05-01185e101007210.1371/journal.pcbi.1010072Discovering sparse control strategies in neural activity.Edward D LeeXiaowen ChenBryan C DanielsBiological circuits such as neural or gene regulation networks use internal states to map sensory input to an adaptive repertoire of behavior. Characterizing this mapping is a major challenge for systems biology. Though experiments that probe internal states are developing rapidly, organismal complexity presents a fundamental obstacle given the many possible ways internal states could map to behavior. Using C. elegans as an example, we propose a protocol for systematic perturbation of neural states that limits experimental complexity and could eventually help characterize collective aspects of the neural-behavioral map. We consider experimentally motivated small perturbations-ones that are most likely to preserve natural dynamics and are closer to internal control mechanisms-to neural states and their impact on collective neural activity. Then, we connect such perturbations to the local information geometry of collective statistics, which can be fully characterized using pairwise perturbations. Applying the protocol to a minimal model of C. elegans neural activity, we find that collective neural statistics are most sensitive to a few principal perturbative modes. Dominant eigenvalues decay initially as a power law, unveiling a hierarchy that arises from variation in individual neural activity and pairwise interactions. Highest-ranking modes tend to be dominated by a few, "pivotal" neurons that account for most of the system's sensitivity, suggesting a sparse mechanism of collective control.https://doi.org/10.1371/journal.pcbi.1010072
spellingShingle Edward D Lee
Xiaowen Chen
Bryan C Daniels
Discovering sparse control strategies in neural activity.
PLoS Computational Biology
title Discovering sparse control strategies in neural activity.
title_full Discovering sparse control strategies in neural activity.
title_fullStr Discovering sparse control strategies in neural activity.
title_full_unstemmed Discovering sparse control strategies in neural activity.
title_short Discovering sparse control strategies in neural activity.
title_sort discovering sparse control strategies in neural activity
url https://doi.org/10.1371/journal.pcbi.1010072
work_keys_str_mv AT edwarddlee discoveringsparsecontrolstrategiesinneuralactivity
AT xiaowenchen discoveringsparsecontrolstrategiesinneuralactivity
AT bryancdaniels discoveringsparsecontrolstrategiesinneuralactivity