The complex simplicity of the brittle star nervous system View Full Text


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Article Info

DATE

2018-12

AUTHORS

Olga Zueva, Maleana Khoury, Thomas Heinzeller, Daria Mashanova, Vladimir Mashanov

ABSTRACT

Background: Brittle stars (Ophiuroidea, Echinodermata) have been increasingly used in studies of animal behavior, locomotion, regeneration, physiology, and bioluminescence. The success of these studies directly depends on good working knowledge of the ophiuroid nervous system. Results: Here, we describe the arm nervous system at different levels of organization, including the microanatomy of the radial nerve cord and peripheral nerves, ultrastructure of the neural tissue, and localization of different cell types using specific antibody markers. We standardize the nomenclature of nerves and ganglia, and provide an anatomically accurate digital 3D model of the arm nervous system as a reference for future studies. Our results helped identify several general features characteristic to the adult echinoderm nervous system, including the extensive anatomical interconnections between the ectoneural and hyponeural components, neuroepithelial organization of the central nervous system, and the supporting scaffold of the neuroepithelium formed by radial glial cells. In addition, we provide further support to the notion that the echinoderm radial glia is a complex and diverse cell population. We also tested the suitability of a range of specific cell-type markers for studies of the brittle star nervous system and established that the radial glial cells are reliably labeled with the ERG1 antibodies, whereas the best neuronal markers are acetylated tubulin, ELAV, and synaptotagmin B. The transcription factor Brn1/2/4 - a marker of neuronal progenitors - is expressed not only in neurons, but also in a subpopulation of radial glia. For the first time, we describe putative ophiuroid proprioceptors associated with the hyponeural part of the central nervous system. Conclusions: Together, our data help establish both the general principles of neural architecture common to the phylum Echinodermata and the specific ophiuroid features. More... »

PAGES

1

References to SciGraph publications

  • 1989. Enigmas of Echinoderm Nervous Systems in EVOLUTION OF THE FIRST NERVOUS SYSTEMS
  • 2005. Mutable Collagenous Tissue: Overview and Biotechnological Perspective in ECHINODERMATA
  • 2006-03. Ultrastructure of the circumoral nerve ring and the radial nerve cords in holothurians (Echinodermata) in ZOOMORPHOLOGY
  • 2016-12. Skeletal regeneration in the brittle star Amphiura filiformis in FRONTIERS IN ZOOLOGY
  • 1995. The nervous systems of Echinodermata: Recent results and new approaches in THE NERVOUS SYSTEMS OF INVERTEBRATES: AN EVOLUTIONARY AND COMPARATIVE APPROACH
  • 2013-12. Radial glial cells play a key role in echinoderm neural regeneration in BMC BIOLOGY
  • 2015-12. Myc regulates programmed cell death and radial glia dedifferentiation after neural injury in an echinoderm in BMC DEVELOPMENTAL BIOLOGY
  • 1979-04. The juxtaligamental cells of Ophiocomina nigra (Abildgaard) (Echinodermata: Ophiuroidea) and their possible role in mechano-effector function of collagenous tissue in CELL AND TISSUE RESEARCH
  • 2010-02. Direct conversion of fibroblasts to functional neurons by defined factors in NATURE
  • 2012-07. Fiji: an open-source platform for biological-image analysis in NATURE METHODS
  • 1981-08. The giant neurone system in ophiuroids in CELL AND TISSUE RESEARCH
  • 2009-12. The central nervous system of sea cucumbers (Echinodermata: Holothuroidea) shows positive immunostaining for a chordate glial secretion in FRONTIERS IN ZOOLOGY
  • 1987. Neurobiology of the Echinodermata in NERVOUS SYSTEMS IN INVERTEBRATES
  • 2016-12. Low coverage sequencing of three echinoderm genomes: the brittle star Ophionereis fasciata, the sea star Patiriella regularis, and the sea cucumber Australostichopus mollis in GIGASCIENCE
  • 2008-01. Coelomic expression of a novel bone morphogenetic protein in regenerating arms of the brittle star Amphiura filiformis in DEVELOPMENT GENES AND EVOLUTION
  • Identifiers

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    http://scigraph.springernature.com/pub.10.1186/s12983-017-0247-4

    DOI

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    DIMENSIONS

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    PUBMED

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    39 schema:description Background: Brittle stars (Ophiuroidea, Echinodermata) have been increasingly used in studies of animal behavior, locomotion, regeneration, physiology, and bioluminescence. The success of these studies directly depends on good working knowledge of the ophiuroid nervous system. Results: Here, we describe the arm nervous system at different levels of organization, including the microanatomy of the radial nerve cord and peripheral nerves, ultrastructure of the neural tissue, and localization of different cell types using specific antibody markers. We standardize the nomenclature of nerves and ganglia, and provide an anatomically accurate digital 3D model of the arm nervous system as a reference for future studies. Our results helped identify several general features characteristic to the adult echinoderm nervous system, including the extensive anatomical interconnections between the ectoneural and hyponeural components, neuroepithelial organization of the central nervous system, and the supporting scaffold of the neuroepithelium formed by radial glial cells. In addition, we provide further support to the notion that the echinoderm radial glia is a complex and diverse cell population. We also tested the suitability of a range of specific cell-type markers for studies of the brittle star nervous system and established that the radial glial cells are reliably labeled with the ERG1 antibodies, whereas the best neuronal markers are acetylated tubulin, ELAV, and synaptotagmin B. The transcription factor Brn1/2/4 - a marker of neuronal progenitors - is expressed not only in neurons, but also in a subpopulation of radial glia. For the first time, we describe putative ophiuroid proprioceptors associated with the hyponeural part of the central nervous system. Conclusions: Together, our data help establish both the general principles of neural architecture common to the phylum Echinodermata and the specific ophiuroid features.
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