Abstract
The cytoskeletal protein doublecortin (DCX) is a marker for neuronal cells retaining high potential for structural plasticity, originating from both embryonic and adult neurogenic processes. Some of these cells have been described in the subcortical white matter of neonatal and postnatal mammals. In mice and humans it has been shown they are young neurons migrating through the white matter after birth, reaching the cortex in a sort of protracted neurogenesis. Here we show that DCX+ cells in the white matter of neonatal and young Cetartiodactyla (dolphin and sheep) form large clusters which are not newly generated (in sheep, and likely neither in dolphins) and do not reach the cortical layers, rather appearing “trapped” in the white matter tissue. No direct contact or continuity can be observed between the subventricular zone region and the DCX+ clusters, thus indicating their independence from any neurogenic source (in dolphins further confirmed by the recent demonstration that periventricular neurogenesis is inactive since birth). Cetartiodactyla include two orders of large-brained, relatively long-living mammals (cetaceans and artiodactyls) which were recognized as two separate monophyletic clades until recently, yet, despite the evident morphological distinctions, they are monophyletic in origin. The brain of Cetartiodactyla is characterized by an advanced stage of development at birth, a feature that might explain the occurrence of “static” cell clusters confined within their white matter. These results further confirm the existence of high heterogeneity in the occurrence, distribution and types of structural plasticity among mammals, supporting the emerging view that multiple populations of DCX+, non-newly generated cells can be abundant in large-brained, long-living species.
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Acknowledgements
The authors thank Bruno Cozzi (expertise in dolphin and sheep brain neuroanatomy) and Barbara Finlay and Christine Charvet (expertise in neurodevelopmental “translating time” modeling) for helpful discussion; Alessandra Pecora for technical help and Enrica Boda for kindly providing cryostat mouse sections.
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The present work has been supported by MIUR-PRIN2015 (Grant 2015Y5W9YP).
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All experiments have been carried out on fixed tissue material obtained from institutions which hold the appropriate authorizations. Dolphin tissues were stored in the Mediterranean Marine Mammal Tissue Bank (MMMTB) of the University of Padova, Italy, a CITES-recognized (IT020) research center and tissue bank, sponsored by the Italian Ministry of the Environment and the University of Padova, with the aim of harvesting tissues from wild and captive cetaceans and distributing them to qualified research centers worldwide. Sheep tissues came from the INRA research center (Nouzilly; Indre et Loire, France—ethical permissions reported in Brus et al. 2013b).
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La Rosa, C., Parolisi, R., Palazzo, O. et al. Clusters of DCX+ cells “trapped” in the subcortical white matter of early postnatal Cetartiodactyla (Tursiops truncatus, Stenella coeruloalba and Ovis aries). Brain Struct Funct 223, 3613–3632 (2018). https://doi.org/10.1007/s00429-018-1708-z
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DOI: https://doi.org/10.1007/s00429-018-1708-z