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Specific paucity of unmyelinated C-fibers in cutaneous peripheral nerves of the African naked-mole rat: Comparative analysis using six species of bathyergidae

Authors

  • Ewan S Smith,

    1. Department of Neuroscience, Max-Delbrück Center for Molecular Medicine, D 13125 Berlin, Germany
    Current affiliation:
    1. Skirball Institute of Biomolecular Medicine, New York University Langone Medical Center, New York, NY 10016
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  • Bettina Purfürst,

    1. Electron Microscopy Core Facility, Max-Delbrück Center for Molecular Medicine, D 13125 Berlin, Germany
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  • Tamara Grigoryan,

    1. Department of Cancer Research, Max-Delbrück Center for Molecular Medicine, D 13125 Berlin, Germany
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  • Thomas J. Park,

    1. Laboratory of Integrative Neuroscience, Department of Biological Sciences, University of Illinois at Chicago, Chicago, Illinois 60612
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  • Nigel C. Bennett,

    1. Department of Zoology and Entomology, Mammal Research Institute, University of Pretoria, 5100 Pretoria, South Africa
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  • Gary R. Lewin

    Corresponding author
    1. Department of Neuroscience, Max-Delbrück Center for Molecular Medicine, D 13125 Berlin, Germany
    • Department of Neuroscience, Max-Delbrück Center for Molecular Medicine, Robert-Rössle Str. 10, D 13125 Berlin, Germany
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Abstract

In mammalian peripheral nerves, unmyelinated C-fibers usually outnumber myelinated A-fibers. By using transmission electron microscopy, we recently showed that the saphenous nerve of the naked mole-rat (Heterocephalus glaber) has a C-fiber deficit manifested as a substantially lower C:A-fiber ratio compared with other mammals. Here we determined the uniqueness of this C-fiber deficit by performing a quantitative anatomical analysis of several peripheral nerves in five further members of the Bathyergidae mole-rat family: silvery (Heliophobius argenteocinereus), giant (Fukomys mechowii), Damaraland (Fukomys damarensis), Mashona (Fukomys darlingi), and Natal (Cryptomys hottentotus natalensis) mole-rats. In the largely cutaneous saphenous and sural nerves, the naked mole-rat had the lowest C:A-fiber ratio (∼1.5:1 compared with ∼3:1), whereas, in nerves innervating both skin and muscle (common peroneal and tibial) or just muscle (lateral/medial gastrocnemius), this pattern was mostly absent. We asked whether lack of hair follicles alone accounts for the C-fiber paucity by using as a model a mouse that loses virtually all its hair as a consequence of conditional deletion of the β-catenin gene in the skin. These β-catenin loss-of function mice (β-cat LOF mice) displayed only a mild decrease in C:A-fiber ratio compared with wild-type mice (4.42 compared with 3.81). We suggest that the selective cutaneous C-fiber deficit in the cutaneous nerves of naked mole-rats is unlikely to be due primarily to lack of skin hair follicles. Possible mechanisms contributing to this unique peripheral nerve anatomy are discussed. J. Comp. Neurol. 520:2785–2803, 2012. © 2012 Wiley Periodicals, Inc.

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