Dynamics of positional information in the vertebrate neural tube

In developing embryos, cells acquire distinct identities depending on their position in a tissue. Secreted signalling molecules, known as morphogens, act as long-range cues to provide the spatial information that controls these cell fate decisions. In several tissues, both the level and the duration of morphogen signalling appear to be important for determining cell fates. This is the case in the forming vertebrate nervous system where antiparallel morphogen gradients pattern the dorsal-ventral axis by partitioning the tissue into sharply delineated domains of molecularly distinct neural progenitors. How information in the gradients is decoded to generate precisely positioned boundaries of gene expression remains an open question. Here, we adopt tools from information theory to quantify the positional information in the neural tube and investigate how temporal changes in signalling could influence positional precision. The results reveal that the use of signalling dynamics, as well as the signalling level, substantially increases the precision possible for the estimation of position from morphogen gradients. This analysis links the dynamics of opposing morphogen gradients with precise pattern formation and provides an explanation for why time is used to impart positional information.

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Publication Details

Journal
Journal of The Royal Society Interface
Published
2024-12-01
DOI
https://doi.org/10.1098/rsif.2024.0414
Citations
5
Primary Topic
Memory and Neural Mechanisms
Type
article
Field-Weighted Citation Impact
1.71

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article

Dynamics of positional information in the vertebrate neural tube

Karen M. Page, James Briscoe, Anđela Marković
5 citations
Journal of The Royal Society Interface
Memory and Neural Mechanisms
1.71
article

Dynamics of positional information in the vertebrate neural tube

Karen M. Page, James Briscoe, Anđela Marković
article en
5 citations

Abstract

In developing embryos, cells acquire distinct identities depending on their position in a tissue. Secreted signalling molecules, known as morphogens, act as long-range cues to provide the spatial information that controls these cell fate decisions. In several tissues, both the level and the duration of morphogen signalling appear to be important for determining cell fates. This is the case in the forming vertebrate nervous system where antiparallel morphogen gradients pattern the dorsal-ventral axis by partitioning the tissue into sharply delineated domains of molecularly distinct neural progenitors. How information in the gradients is decoded to generate precisely positioned boundaries of gene expression remains an open question. Here, we adopt tools from information theory to quantify the positional information in the neural tube and investigate how temporal changes in signalling could influence positional precision. The results reveal that the use of signalling dynamics, as well as the signalling level, substantially increases the precision possible for the estimation of position from morphogen gradients. This analysis links the dynamics of opposing morphogen gradients with precise pattern formation and provides an explanation for why time is used to impart positional information.

Journal of The Royal Society InterfaceVol. 21(221)
The Francis Crick Institute (GB), Living Systems (United States) (US), University College London (GB)
Wellcome Trust, Cancer Research UK, Medical Research Council, Department of Mathematics, University College London
Openalex Percentile: Top 15%
Memory and Neural Mechanisms
1.71
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