Abstract
Adult neurogenesis is a feature that is phylogenetically highly conserved, yet most of the current knowledge in this field is based on laboratory rodents. In addition to the differences among vertebrates, remarkable peculiarities are also emerging in the location and structural and functional features of neurogenic systems in mammals. Although the orders Lagomorpha and Rodentia are quite similar, unexpected features of structural plasticity and neurogenesis have been found to occur in the rabbit central nervous system. The structural and temporal characteristics of protracted and persistent neurogenesis in rabbits are herewith addressed. Attention is focused on the subventricular zone cytoarchitecture and extensions, as well as on processes of persistent neurogenesis that have been recently demonstrated to occur in the striatum and in the cerebellum. The existence of neural cell progenitors persisting within the rabbit brain parenchyma (so-called nonneurogenic in rodents) are discussed.
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References
Altman J, Bayer SA (1997) Development of the cerebellar system. CRC Press, Boca Raton, USA
Alvarez-Buylla A, Garcìa-Verdugo JM (2002) Neurogenesis in adult subventricular zone. J Neurosci 22:629–634
Anthony TE, Klein C, Fishell G, Heintz N (2004) Radial glia serve as neuronal progenitors in all regions of the central nervous system. Neuron 41:881–890
Arvidsson A, Collin T, Kirik D et al (2002) Neuronal replacement from endogenous precursors in the adult brain after stroke. Nat Med 8:963–970
Bédard A, Cossette M, Lévesque M, Parent A (2002) Proliferating cells can differentiate into neurons in the striatum of normal adult monkey. Neurosci Lett 328:213–216
Berardi N, Pizzorusso T, Maffei L (2000) Critical periods during sensory development. Curr Opin Neurobiol 10:138–145
Bonfanti L (2006) PSA-NCAM in mammalian structural plasticity and neurogenesis. Prog Neurobiol 80:129–164
Bonfanti L, Ponti G (2008) Adult neurogenesis and the New Zealand white rabbit. Vet J 175:310–331
Bonfanti L, Olive S, Poulain DA, Theodosis, DT (1992) Mapping of the distribution of polysialylated neural cell adhesion molecule throughout the central nervous system of the adult rat: an immunohistochemical study. Neuroscience 49:419–436
Brown JP, Couillard-Després S, Cooper-Kuhn CM et al (2003) Transient expression of doublecortin during adult neurogenesis. J Comp Neurol 467:1–10
Butt AM, Hamilton N, Hubbard P, Pugh M, Ibrahim M (2005) Synantocytes: the fifth element. J Anat 207:695–706
Chenn A, Walsh CA (2002) Regulation of cerebral cortical size by control of cell cycle exit in neural precursors. Science 297:365–369
Curtis MA, Kam M, Nannmark U et al (2007) Human neuroblasts migrate to the olfactory bulb via a lateral ventricular extension. Science 315:1243–1249
Dayer AG, Cleaver KM, Abouantoun T, Cameron HA (2005) New GABAergic interneurons in the adult neocortex and striatum are generated from different precursors. J Cell Biol 168, 415–427
Doetsch F, Garcìa-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17:5046–5041
Douzery EJ, Huchon D (2004) Rabbits, if anything, are likely Glires. Mol Phylogenet Evol 33:922–935
Engelkamp D, Rashbass P, Seawright A, van Heyningen V (1999) Role of Pax6 in development of the cerebellar system. Development 126:3585–3596
Fallon J, Reid S, Kinyamu R et al (2000) In vivo induction of massive proliferation, directed migration, and differentiation of neural cells in the adult mammalian brain. Proc Natl Acad Sci USA 97:14686–14691
Gage FH (2000) Mammalian neural stem cells. Science 287:1433–1438
Garcia-Verdugo JM, Ferron S et al (2002) The proliferative ventricular zone in adult vertebrates: a comparative study using reptiles, birds, and mammals. Brain Res Bull 57:765–775
Gould E (2007) How widespread is adult neurogenesis in mammals? Nat Rev Neurosci 8:481–488
Gould E, Reeves AJ, Graziano MS, Gross CG (1999) Neurogenesis in the neocortex of adult primates. Science 286:548–552
Gould E, Vail N, Wagers M, Gross CG (2001) Adult-generated hippocampal and neocortical neurons in macaques have a transient existence. Proc Natl Acad Sci USA 98:10910–10917
Ito M (2006) Cerebellar circuitry as a neuronal machine. Prog Neurobiol 78:272–303
Komuro H, Yacubova E, Yacubova E, Rakic P (2001) Mode and tempo of tangential cell migration in the cerebellar external granule layer. J Neurosci 21:527–540
Kondo T, Raff M (2000) Oligodendrocyte precursor cells reprogrammed to become multipotential CNS stem cells. Science 289:1754–1757
Kornack DR, Rakic P (2001) The generation, migration, and differentiation of olfactory neurons in the adult primate brain. Proc Natl Acad Sci USA 98:4752–4757
Kriegstein A, Noctor S, Martinez-Cerdeno V (2006) Patterns of neural stem and progenitor cell division may underlie evolutionary cortical expansion. Nat Rev Neurosci 7:883–890
Leonhardt H (1972) Topographic distribution of subependymal basement labyrinths of the ventricular system of brain in rabbit. Z Zellforsch Mikrosk Anat 127:392–406
Leto K, Bartolini A, Rossi F (2008) Neurogenesis in the cerebellum of rodents. In: Bonfanti L, ed. Postnatal and Adult Neurogenesis. Research Signpost, Trivandrum, India pp. 63–81
Lindsey BW, Tropepe V (2006) A comparative framework for understanding the biological principles of adult neurogenesis. Prog Neurobiol 80:281–307
Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145–1148
Lois C, Garcìa-Verdugo J, Alvarez-Buylla A (1996) Chain migration of neuronal precursors. Science 271:978–981
Luzzati F, Peretto P, Aimar P et al (2003) Glia-independent chains of neuroblasts through the subcortical parenchyma of the adult rabbit brain. Proc Natl Acad Sci USA 100:13036–13041
Luzzati F, De Marchis S, Fasolo A, Peretto P (2006) Neurogenesis in the caudate nucleus of the adult rabbit. J Neurosci 26:609–621
Luzzati F, De Marchis S, Fasolo A, Peretto P (2007) Adult neurogenesis and local neuronal progenitors in the striatum. Neurodegen Dis 4:322–327
Maricich SM, Herrup K (1999) Pax-2 expression defines a subset of GABAergic interneurons and their precursors in the developing murine cerebellum. J Neurobiol 41:281–294
McFarland WL, Morgane PJ, Jacobs MS (1969) Ventricular system of the brain of the dolphin, Tursiops truncatus, with comparative anatomical observations and relations to brain specializations. J Comp Neurol 135:275–368
Nishiyama A (2007) Polydendrocytes: NG2 cells with many roles in development and repair of the CNS. Neuroscientist 13:62–76
Nothias F, Fischer I, Murray M et al (1996) Expression of a phosphorylated isoform of MAP1B is maintained in adult central nervous system areas that retain capacity for structural plasticity. J Comp Neurol 368:317–334
Palmer TD, Markakis EA, Willhoite AR, Safar F, Gage, FH (1999) Fibroblast growth factor-2 activates a latent neurogenic program in neural stem cells from diverse regions of the adult CNS. J Neurosci 19:8487–8497
Peretto P, Merighi A, Fasolo A, Bonfanti L (1997) Glial tubes in the rostral migratory stream of the adult rat. Brain Res Bull 42:9–21
Peretto P, Giachino C, Aimar P et al (2005) Chain formation and glial tube assembly in the shift from neonatal to adult subventricular zone of the rodent forebrain. J Comp Neurol 487:407–427
Ponti G, Peretto P, Bonfanti L (2006a) A subpial, transitory germinal zone forms chains of neuronal precursors in the rabbit cerebellum. Dev Biol 294:168–180
Ponti G, Aimar P, Bonfanti L (2006b) Cellular composition and cytoarchitecture of the rabbit subventricular zone (SVZ) and its extensions in the forebrain. J Comp Neurol 498:491–507
Ponti G, Peretto P, Bonfanti L (2008) Genesis of neuronal and glial progenitors in the cerebellar cortex of peripuberal and adult rabbits. PLoS ONE 3:e2366
Quinones-Hinojosa A, Sanai N, Soriano-Navarro M et al (2006) Cellular composition and cytoarchitecture of the adult human subventricular zone: a niche of neural stem cells. J Comp Neurol 494:415–434
Rodriguez-Perez LM, Perez-Martin M, Jimenez, AJ et al (2003) Immunocytochemical characterization of the wall of the bovine ventricle. Cell Tissue Res 314:325–335
Sanai N, Tramontin AD, Quinones-Hinojosa A et al (2004) Unique astrocyte ribbon in adult human brain contains neural stem cells but lacks chain migration. Nature 427:740–744
Sanchez-Villagra MR, Sultan F (2001) The cerebellum at birth in therian mammals, with special reference to rodents. Brain Behav Evol 59:101–113
Seri B, Garcìa-Verdugo JM, Collaudo-Morente L et al (2004) Cell types, lineage, and architecture of the germinal zone in the adult dentate gyrus. J Comp Neurol 478:359–378
Takebayashi H, Nabeshima Y, Yoshida, S et al (2002) The basic helix-loop-helix factor olig2 is essential for the development of motoneuron and oligodendrocyte lineages. Curr Biol 12:1157–1163
Temple S (2001) The development of neural stem cells. Nature 414:112–117
Viereck C, Tucker RP, Matus A (1989) The adult rat olfactory system expresses microtubule-associated proteins found in the developing brain. J Neurosci 9:3547–3557
Weisheit G, Gliem M, Endl E et al (2006) Postnatal development of the murine cerebellar cortex: formation and early dispersal of basket, stellate and Golgi neurons. Eur J Neurosci 24:466–478
Wexler E, Palmer T (2002) Where, oh where, have my stem cells gone? Trends Neurosci 25:225–227
Weyer A, Schilling K (2003) Developmental and cell type-specific expression of the neuronal marker NeuN in the murine cerebellum. J Neurosci Res 73:400–409
Wu HY, Dawson MR, Reynolds R, Hardy RJ (2001) Expression of QKI proteins and MAP1B identifies actively myelinating oligodendrocytes in adult rat brain. Mol Cell Neurosci 17:292–302
Yamasaki T, Kawaji K, Ono K et al (2001) Pax6 regulates granule cell polarization during parallel fiber formation in the developing cerebellum. Development 128:3133–3144
Zhou Q, Anderson DJ (2002) The bHLH transcription factors OLIG2 and OLIG1 couple neuronal and glial subtype specification. Cell 109:61–73
Zupanc GK (2006) Neurogenesis and neuronal regeneration in the adult fish brain. J Comp Physiol A 192:649–670
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This work was supported by Compagnia di San Paolo (Progetto NEUROTRANSPLANT-2004.2019).
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Ponti, G., Luzzati, F., Peretto, P., Bonfanti, L. (2011). Neurogenesis in the Adult Rabbit: From Olfactory System to Cerebellum. In: Seki, T., Sawamoto, K., Parent, J.M., Alvarez-Buylla, A. (eds) Neurogenesis in the Adult Brain I. Springer, Tokyo. https://doi.org/10.1007/978-4-431-53933-9_13
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DOI: https://doi.org/10.1007/978-4-431-53933-9_13
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