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Non-neurogenic SVZ-like niche in dolphins, mammals devoid of olfaction

Abstract

Adult neurogenesis has been implicated in brain plasticity and brain repair. In mammals, it is mostly restricted to specific brain regions and specific physiological functions. The function and evolutionary history of mammalian adult neurogenesis has been elusive so far. The largest neurogenic site in mammals (subventricular zone, SVZ) generates neurons destined to populate the olfactory bulb. The SVZ neurogenic activity appears to be related to the dependence of the species on olfaction since it occurs at high rates throughout life in animals strongly dependent on this function for their survival. Indeed, it dramatically decreases in humans, who do not depend so much on it. This study investigates whether the SVZ neurogenic site exists in mammals devoid of olfaction and olfactory brain structures, such as dolphins. Our results demonstate that a small SVZ-like region persists in these aquatic mammals. However, this region seems to have lost its neurogenic capabilities since neonatal stages. In addition, instead of the typical newly generated neuroblasts, some mature neurons were observed in the dolphin SVZ. Since cetaceans evolved from terrestrial ancestors, non-neurogenic SVZ may indicate extinction of adult neurogenesis in the absence of olfactory function, with the retention of an SVZ-like anatomical region either vestigial or of still unknown role.

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Acknowledgements

The authors thank Fondazione CRT for financial support (Bando Ricerca e Istruzione 2014), the University of Turin (PhD programme in Veterinary Sciences), and the MMMTB of the University of Padova for supplying tissue samples of the dolphin brain. Special thanks to Antonella Peruffo, Mattia Panin, Stefano Montelli, Maristella Giurisato for their help in gathering and handling the dolphin brain specimens, to Silvia Messina and Chiara La Rosa for technical help in the cryostat sectioning, and to Telmo Pievani for reading the manuscript.

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Correspondence to Luca Bonfanti.

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Parolisi, R., Cozzi, B. & Bonfanti, L. Non-neurogenic SVZ-like niche in dolphins, mammals devoid of olfaction. Brain Struct Funct 222, 2625–2639 (2017). https://doi.org/10.1007/s00429-016-1361-3

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Keywords

  • Adult neurogenesis
  • Olfactory bulb
  • Cetaceans
  • Subventricular zone
  • Brain plasticity
  • Evolution
  • Doublecortin