Brain Structure and Function

, Volume 222, Issue 6, pp 2625–2639 | Cite as

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

Original Article

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.

Keywords

Adult neurogenesis Olfactory bulb Cetaceans Subventricular zone Brain plasticity Evolution Doublecortin 

References

  1. Aimone JB, Li Y, Lee SW, Clemenson GD, Deng W, Gage FH (2014) Regulation and function of adult neurogenesis: from genes to cognition. Physiol Rev 94:1991–1026CrossRefGoogle Scholar
  2. Amrein I (2015) Adult hippocampal neurogenesis in natural populations of mammals. Cold Spring Harb Perspect Biol 7(5):a021295CrossRefPubMedPubMedCentralGoogle Scholar
  3. Armentano M, Canalia N, Crociara P, Bonfanti L (2011) Culturing conditions affect viability and organization of mouse subventricular zone in ex vivo cultured forebrain slices. J Neurosci Meth 197:65–81CrossRefGoogle Scholar
  4. Barker JM, Boonstra R, Wojtowicz JM (2011) From pattern to purpose: how comparative studies contribute to understanding the function of adult neurogenesis. Eur J Neurosci 34:963–977CrossRefPubMedGoogle Scholar
  5. Bonfanti L (2011) From hydra regeneration to human brain structural plasticity: a long trip through narrowing roads. Sci World J 11:1270–1299CrossRefGoogle Scholar
  6. Bonfanti L, Nacher J (2012) New scenarios for neuronal structural plasticity in non-neurogenic brain parenchyma: the case of cortical layer II immature neurons. Prog Neurobiol 98:1–15CrossRefPubMedGoogle Scholar
  7. Bonfanti L, Peretto P (2011) Adult neurogenesis in mammals—a theme with many variations. Eur J Neurosci 34:930–950CrossRefPubMedGoogle Scholar
  8. Bonfanti L, Ponti G (2008) Adult mammalian neurogenesis and the New Zealand white rabbit. Vet J 175:310–331CrossRefPubMedGoogle Scholar
  9. Bordiuk OL, Smith K, Morin PJ, Semenov MV (2014) Cell proliferation and neurogenesis in adult mouse brain. PLoS One 9(11):e111453CrossRefPubMedPubMedCentralGoogle Scholar
  10. Breathnach AS (1953) The olfactory tubercle, prepyriform cortex and precommisural region of the porpoise (Phocaenaphocaena). J Anat 87:96–113PubMedPubMedCentralGoogle Scholar
  11. Breathnach A, Goldby F (1954) The amygdaloid nuclei, hippocampus and other parts of the rhinencephalon in the porpoise (Phocoenaphocoena). J Anat 88:267–291PubMedPubMedCentralGoogle Scholar
  12. Brown JP, Couillard-Despres S, Cooper-Kuhn CM, Winkler J, Aigner L, Kuhn HG (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1–10CrossRefPubMedGoogle Scholar
  13. Buhl EH, Oelschläger HA (1986) Ontogenetic development of the nervus terminalis in toothed whales. Evidence for its non-olfactory nature. Anat Embryol 173:285–294CrossRefPubMedGoogle Scholar
  14. Buhl EH, Oelschläger HA (1988) Morphogenesis of the brain in the harbour porpoise. J Comp Neurol 277:109–125CrossRefPubMedGoogle Scholar
  15. Cozzi B, Huggenberger S, Oelschläger HHA (2017) The anatomy of dolphins. Insights into body structure and function. Chapter 6: Brain, Spinal Cord, and Cranial Nerves. Academic Press, London, pp 191–285Google Scholar
  16. Dawson MRL, Polito A, Levine JM, Reynolds R (2003) NG2-expressing glial progenitor cells: an abundant and widespread population of cycling cells in the adult rat CNS. Mol Cell Neurosci 24:476–488CrossRefPubMedGoogle Scholar
  17. Del Bigio MR (2011) Cell proliferation in human ganglionic eminence and suppression after prematurity-associated haemorrhage. Brain 134:1344–1361CrossRefPubMedGoogle Scholar
  18. Eriksson PS, Perfilieva E, Biork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317CrossRefPubMedGoogle Scholar
  19. Feliciano DM, Bordey A, Bonfanti L (2015) Noncanonical sites of adult neurogenesis in the mammalian brain. Cold Spring Harb Perspect Biol 7(10):a018846CrossRefPubMedGoogle Scholar
  20. Fung SJ, Joshi D, Allen KM, Sivagnanasundaram S, Rothmond DA, Saunders R, Noble PL, Webster MJ, Weickert CS (2011) Developmental patterns of doublecortin expression and white matter density in the postnatal primate prefrontal cortex and schizophrenia. PLoS One 6(9):e25194CrossRefPubMedPubMedCentralGoogle Scholar
  21. Gingerich PD, Wells NA, Russell DE, Shah SM (1983) Origin of whales in epicontinental remnant seas: new evidence from the early eocene of pakistan. Science 220:403–406CrossRefPubMedGoogle Scholar
  22. Gomez-Climent MA, Castillo-Gomez E, Varea E, Guirado R, Blasco-Ibanez JM, Crespo C, Martinez-Guijarro FJ, Nacher J (2008) A population of prenatallygenerated cells in the rat paleocortex maintains an immature neuronal phenotypeinto adulthood. Cereb Cortex 18:2229–2240CrossRefPubMedGoogle Scholar
  23. Grandel H, Brand M (2013) Comparative aspects of adult neural stem cell activity in vertebrates. Dev Genes Evol 223:131–147CrossRefPubMedGoogle Scholar
  24. Herzog W, Weber K (1978) Fractionation of brain microtubule-associated proteins. Isolation of two different proteins which stimulate tubulin polymerization in vitro. Eur J Biochem 92:1–8CrossRefPubMedGoogle Scholar
  25. Kee N, Sivalingam S, Boonstra R, Wojtowicz JM (2002) The utility of Ki-67 and BrdU as proliferative markers of adult neurogenesis. J Neurosci Meth 115:97–105CrossRefGoogle Scholar
  26. Kempermann G (2012) New neurons for “survival of the fittest”. Nat Rev Neurosci 13:727–736PubMedGoogle Scholar
  27. Kempermann G (2016) Adult neurogenesis: an evolutionary perspective. Cold Spring Harb Perspect Biol 8:a018986CrossRefGoogle Scholar
  28. Kishida T, Thewissen JGM, Hayakawa T, Imai H, Agata K (2015) Aquatic adaptation and the evolution of smell and taste in whales. Zool Lett 1:9CrossRefGoogle Scholar
  29. Kriegstein A, Alvarez-Buylla A (2009) The glial nature of embryonic and adult neural stem cells. Annu Rev Neurosci 32:149–184CrossRefPubMedPubMedCentralGoogle Scholar
  30. Lepousez G, Valley MT, Lledo PM (2013) The impact of adult neurogenesis on olfactory bulb circuits and computations. Annu Rev Physiol 75:339–363CrossRefPubMedGoogle Scholar
  31. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145–1148CrossRefPubMedGoogle Scholar
  32. Lois C, Garcia-Verdugo JM, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978–981CrossRefPubMedGoogle Scholar
  33. Luzzati F, Peretto P, Aimar P, Ponti G, Fasolo A, Bonfanti L (2003) Glia-independent chains of neuroblasts through the subcortical parenchyma of the adult rabbit brain. Proc Natl Acad Sci USA 100:13036–13041CrossRefPubMedPubMedCentralGoogle Scholar
  34. Luzzati F, Bonfanti L, Fasolo A, Peretto P (2009) DCX and PSA-NCAM expression identifies a population of neurons preferentially distributed in associative areas of different pallial derivatives and vertebrate species. Cereb Cortex 19:1028–1041CrossRefPubMedGoogle Scholar
  35. Marino L, Rilling JK, Lin SK, Ridgway SH (2000) Relative volume of the cerebellum in dolphins and comparison with anthropoid primates. Brain Behav Evol 56:204–211CrossRefPubMedGoogle Scholar
  36. Marriott S, Cowan E, Cohen J, Hallock RM (2013) Somatosensation, echolocation, and underwater sniffing: adaptations allow mammals without traditional olfactory capabilities to forage for food underwater. Zool Sci 30:69–75CrossRefPubMedGoogle Scholar
  37. Morgane PJ, Jacobs MS, McFarland WL (1980) The anatomy of the brain of the bottlenose dolphin (Tursiops truncatus). Surface configurations of the telencephalon of the bottlenose dolphin with comparative anatomical observations in four other cetaceans species. Brain Res Bull 5:1–107CrossRefGoogle Scholar
  38. Nacher J, Crespo C, McEwen BS (2001) Doublecortin expression in the adult rat telencephalon. Eur J Neurosci 14:629–644CrossRefPubMedGoogle Scholar
  39. Obernier K, Tong CK, Alvarez-Buylla A (2014) Restricted nature of adult neural stem cells: re-evaluation of their potential for brain repair. Front Neurosci 8:162CrossRefPubMedPubMedCentralGoogle Scholar
  40. Oelschläger HHA (2008) The dolphin brain—a challenge for synthetic neurobiology. Brain Res Bull 75:450–459CrossRefPubMedGoogle Scholar
  41. Oelschläger HHA, Oelschläger JS (2009) “Brain”. In: Perrin WF, Würsin B, Thewissen JGM (eds) Encyclopedia of marine mammals, II edn. Academic Press, San Diego, pp 134–149CrossRefGoogle Scholar
  42. Parolisi R, Peruffo A, Messina S, Panin M, Montelli S, Giurisato M, Cozzi B, Bonfanti L (2015) Forebrain neuroanatomy of the neonatal and juvenile dolphin (T. truncatus and S. coeruloalba). Front Neuroanat 9:140CrossRefPubMedPubMedCentralGoogle Scholar
  43. Patzke N, Spocter MA, Karlsson KÆ, Bertelsen MF, Haagensen M, Chawana R, Streicher S, Kaswera C, Gilissen E, Alagaili AN, Mohammed OB, Reep RL, Bennett NC, Siegel JM, Ihunwo AO, Manger PR (2015) In contrast to many other mammals, cetaceans have relatively small hippocampi that appear to lack adult neurogenesis. Brain Struct Funct 220: 361–383CrossRefPubMedGoogle Scholar
  44. Peretto P, Bonfanti L (2014) Major unsolved points in adult neurogenesis: doors open on a translational future? Front Neurosci 8:154CrossRefPubMedPubMedCentralGoogle Scholar
  45. Peretto P, Merighi A, Fasolo A, Bonfanti L (1997) Glial tubes in the rostral migratory stream of the adult rat. Brain Res Bull 42:9–21CrossRefPubMedGoogle Scholar
  46. Peretto P, Giachino C, Aimar P, Fasolo A, Bonfanti L (2005) Chain formation and glial tube assembly in the shift from neonatal to adult subventricular zone of the rodent forebrain. J Comp Neurol 487:407–427CrossRefPubMedGoogle Scholar
  47. Ponti G, Aimar P, Bonfanti L (2006a) Cellular composition and cytoarchitecture of the rabbit subventricular zone (SVZ) and its extensions in the forebrain. J Comp Neurol 498:491–507Google Scholar
  48. Ponti G, Peretto P, Bonfanti L (2006b) A subpial, transitory germinal zone forms chains of neuronal precursors in the rabbit cerebellum. Dev Biol 294:168–180Google Scholar
  49. Ponti G, Obernier K, Guinto C, Jose L, Bonfanti L, Alvarez-Buylla A (2013) Cell cycle and lineage progression of neural progenitors in the ventricular-subventricular zones of adult mice. Proc Nat Acad Sci USA 110:E1045–E1054CrossRefPubMedPubMedCentralGoogle Scholar
  50. Ridgway SH (1990). The central nervous system of the bottlenose dolphin. In: Leatherwood S, Reeves RR (eds) The Bottlenose Dolphin. Academic Press, USA, pp 69–97Google Scholar
  51. Ridgway SH, Demski LS, Bullock TH, Schwanzel-Fukuda M (1987) The terminal nerve in odontocete cetaceans. Ann NY Acad Sci 519:201–212CrossRefPubMedGoogle Scholar
  52. Rolando C, Parolisi R, Boda E, Schwab ME, Rossi F, Buffo A (2012) Distinct roles of Nogo-a and Npogo receptor 1 in the homeostatic regulation of adult neural stem cell function and neuroblast migration. J Neurosci 32:17788–17799CrossRefPubMedGoogle Scholar
  53. Rose KD (2006) The beginning of the age of mammals. JHU PressGoogle Scholar
  54. Sahay A, Wilson DA, Hen R (2011) Pattern separation: a common function for new neurons in hippocampus and olfactory bulb. Neuron 70:582–588CrossRefPubMedPubMedCentralGoogle Scholar
  55. Sakamoto M, Kageyama R, Imayoshi I (2014) The functional significance of newly born neurons integrated into olfactory bulb circuits. Front Neurosci 8:121PubMedPubMedCentralGoogle Scholar
  56. Sanai N et al (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427:740–744CrossRefPubMedGoogle Scholar
  57. Sanai N, Nguyen T, Ihrie RA, Mirzadeh Z, Tsai H-H, Wong M, Gupta N, Berger MS, Huang E, Garcia-Verdugo JM, Rowitch DH, Alvarez-Buylla A (2011) Corridors of migrating neurons in the human brain and their decline during infancy. Nature 478:382–386CrossRefPubMedPubMedCentralGoogle Scholar
  58. Thewissen JG, Williams EM, Roe LJ, Hussain ST (2001) Skeletons of terrestrial cetaceans and the relationship of whales to artiodactyls. Nature 413:277–281CrossRefPubMedGoogle Scholar
  59. Tong CK, Alvarez-Buylla A (2014) Snapshot: adult neurogenesis in the V-SVZ. Neuron 81:220–220CrossRefPubMedPubMedCentralGoogle Scholar
  60. Tramontin AD, Garcìa-Verdugo JM, Lim DA, Alvarez-Buylla A (2003) Postnatal development of radial glia and the ventricular zone (VZ): a continuum of the neural stem cell compartment. Cereb Cortex 13:580–587CrossRefPubMedGoogle Scholar
  61. Vadoaria KC, Gage FH (2014) Snapshot: adult hippocampal neurogenesis. Cell 156:1114CrossRefGoogle Scholar
  62. von Bohlen O, Halbach O (2011) Immunohistological markers for proliferative events, gliogenesis, and neurogenesis within the adult hippocampus. Cell Tissue Res 345:1–19CrossRefGoogle Scholar
  63. Wang C, Liu F, Liu YY, Zhao CH, You Y, Wang L, Zhang J, Wei B, Ma T, Zhang Q, Zhang Y, Chen R, Song H, Yang Z (2011) Identification and characterization of neuroblasts in the subventricular zone and rostral migratory stream of the adult human brain. Cell Res 21:1534–1550CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2017

Authors and Affiliations

  1. 1.Neuroscience Institute Cavalieri Ottolenghi (NICO)OrbassanoItaly
  2. 2.Department of Veterinary SciencesUniversity of TurinGrugliascoItaly
  3. 3.Department of Comparative Biomedicine and Food ScienceUniversity of PaduaLegnaroItaly

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