Adult Neurogenesis in Reptiles

  • Susana González-Granero
  • Melissa Lezameta
  • José Manuel García-VerdugoEmail author


Adult neurogenesis in reptiles is a well-documented phenomenon and exists in many telencephalic areas. The newly generated neurons originate along the walls of the lateral ventricles, mainly in the sulci. The putative neural progenitors are radial glial cells. These glial cells give rise to neuroblasts that migrate to their final destination. In general, the new neurons are born in the portion of the ventricular zone (VZ) adjacent to the telencephalic area where they will be recruited and migrate radially through the brain parenchyma along the processes of radial glial cells to their final destination, although migration to the olfactory bulbs (OB) is different. Specifically, it seems that new neurons of the OB are not produced in the ventricular walls of the OB ventricle, but instead in more caudal levels of the lateral ventricles. They then migrate tangentially over the soma of the VZ radial glia until they reach the OB. Adult neurogenesis creates microneurons and projection neurons, and occasionally there is gliogenesis as well.

One last striking feature of the reptilian brain is their ability to regenerate large neuronal populations that have died as a result of physical and chemical injuries.


Glial Fibrillary Acidic Protein Olfactory Bulb Granular Layer Adult Neurogenesis Plexiform Layer 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.





Tritiated thymidine


Anterior dorsal ventricular ridge


Accesory olfactory bulb


Anterior olfactory nucleus




Central nervous system


Collapsin response-mediated protein 4


Dorsal cortex


Dorsomedial cortex


Dorsal ventricular ridge


Glial fibrillary acidic protein


Lateral cortex


Medial cortex


Main olfactory bulb


Nucleus sphericus


Olfactory bulb


Polysialic neural cell adhesion molecule


Sulcus lateralis




Sulcus septomedialis


Sulcus terminalis




Sulcus ventralis


Subventricular zone


Ventricular zone



Special thanks to Enrique Font, from the Instituto Cavanilles de Biodiver­sidad y Biologia Evolutiva, and Nader Sanai, MD, at the University of California San Francisco, for their comments and suggestions on the manuscript. This review was supported by CIBERNED and TerCel.


  1. Ahboucha S, Laalaoui A, Didier-Bazes M, Montange M, Cooper HM, Gamrani H (2003) Differential patterns of glial fibrillary acidic protein-immunolabeling in the brain of adult lizards. J Comp Neurol 464:159–171.PubMedCrossRefGoogle Scholar
  2. Alibardi L (1994) H3-thymidine labeled cerebrospinal fluid contacting cells in the regenerating caudal spinal cord of the lizard Lampropholis. Ann Anat 176:347–356.PubMedCrossRefGoogle Scholar
  3. Alvarez-Buylla A (1990) Mechanism of neurogenesis in adult avian brain. Experientia 46:948–955.CrossRefGoogle Scholar
  4. Alvarez-Buylla A, Theelen M, Nottebohm F (1990) Proliferation “hot spots” in adult avian ventricular zone reveal radial cell division. Neuron 5:101–109.PubMedCrossRefGoogle Scholar
  5. Alvarez-Buylla A, Garcia-Verdugo JM, Mateo AS, Merchant-Larios H (1998) Primary neural precursors and intermitotic nuclear migration in the ventricular zone of adult canaries. J Neurosci 18:1020–1037.PubMedGoogle Scholar
  6. Austin CP, Cepko CL (1990) Cellular migration patterns in the developing mouse cerebral cortex. Development 110:713–732.Google Scholar
  7. Beazley LD, Sheard PW, Tennant M, Starac D, Dunlop SA (1997) Optic nerve regenerates but does not restore topographic projections in the lizard Ctenophorus ornatus. J Comp Neurol 377:105–120.PubMedCrossRefGoogle Scholar
  8. Bruce LL, Neary TJ (1995) The limbic system of tetrapods: a comparative analysis of cortical and amygdalar populations. Brain Behav Evol 46:224–234.PubMedCrossRefGoogle Scholar
  9. Butler AB, Hodos W (1996) Comparative vertebrate neuroanatomy: Evolution and adaptation. Wiley-Liss, New York.Google Scholar
  10. Chernoff EA (1996) Spinal cord regeneration: a phenomenon unique to urodeles? Int J Dev Biol 40:823–831.PubMedGoogle Scholar
  11. Davila JC, Guirado S, De la Calle A, Marin-Giron F (1985) Electron microscopy of the medial cortex in the lizard Psammodromus algirus. J Morphol 185:327–338.CrossRefGoogle Scholar
  12. Del Grande P, Franceschini V, Minelli G, Ciani F (1990) Mitotic activity of the telencephalic matrix areas following optic tectum or pallial cortex lesion in newt. Z Mikrosk Anat Forsch 104:617–624.PubMedGoogle Scholar
  13. Delgado-Gonzalez FJ, Alonso-Fuentes A, Delgado-Fumero A, Garcia-Verdugo JM, Gonzalez-Granero S, Trujillo-Trujillo CM, Damas-Hernandez MC (2008) Seasonal differences in ventricular proliferation of adult Gallotia galloti lizards. Brain Res 1191:39–46.PubMedCrossRefGoogle Scholar
  14. Desfilis E, Garcia-Verdugo JM, Font E (1993) Regeneration in the adult lizard brain: further evidence from 3TH autoradiography. Eur J Neurosci S6:290.Google Scholar
  15. Doetsch F, Garcia-Verdugo JM, Alvarez-Buylla A (1997) Cellular composition and three-dimensional organization of the subventricular germinal zone in the adult mammalian brain. J Neurosci 17:5046–5061.PubMedGoogle Scholar
  16. Doetsch F, Caille I, Lim DA, Garcia-Verdugo JM, Alvarez-Buylla A (1999) Subventricular zone astrocytes are neural stem cells in the adult mammalian brain. Cell 97:703–716.PubMedCrossRefGoogle Scholar
  17. Duffy MT, Simpson SB, Liebich DR, Davis BM (1990) Origin of spinal cord axons in the lizard regenerated tail: supernormal projections from local spinal neurons. J Comp Neurol 293:208–222.PubMedCrossRefGoogle Scholar
  18. Duffy MT, Liebich DR, Garner LK, Hawrych A, Simpson SB, Jr., Davis BM (1992) Axonal sprouting and frank regeneration in the lizard tail spinal cord: correlation between changes in synaptic circuitry and axonal growth. J Comp Neurol 316:363–374.PubMedCrossRefGoogle Scholar
  19. Font E, Garcia-Verdugo JM, Alcantara S, Lopez-Garcia C (1991) Neuron regeneration reverses 3-acetylpyridine-induced cell loss in the cerebral cortex of adult lizards. Brain Res 551:230–235.PubMedCrossRefGoogle Scholar
  20. Font C, Hoogland PV, Vermeulen van der Zee E, Perez-Clausell J, Martinez-Garcia F (1995a) The septal complex of the telencephalon of the lizard Podarcis hispanica. I. Chemoarchitectonical organization. J Comp Neurol 359:117–130.PubMedCrossRefGoogle Scholar
  21. Font E, Garcia-Verdugo JM, Desfilis E, Perez-Cañellas M (1995b) Neuron-glia interrelations during 3-acetylpyridine-induced degeneration and regeneration in the adult lizard brain. In: Vernadakis A, Roots B (eds) Neuron-glia interrelations during phylogeny: II. Plasticity and regeneration. Humana press Inc, Totowa.Google Scholar
  22. Font E, Desfilis E, Perez-Cañellas M, Alcantara S, Garcia-Verdugo JM (1997) 3-Acetylpyridine-induced degeneration and regeneration in the adult lizard brain: a qualitative and quantitative analysis. Brain Res 754:245–259.PubMedCrossRefGoogle Scholar
  23. Font E, Desfilis E, Perez-Cañellas MM, Garcia-Verdugo JM (2001) Neurogenesis and neuronal regeneration in the adult reptilian brain. Brain Behav Evol 58:276–295.PubMedCrossRefGoogle Scholar
  24. Garcia-Verdugo JM, Berbel PJ, Lopez-Garcia C (1981) [Golgi and electron microscopy study of cerebral ependymocytes of the lizard Lacerta galloti]. Trab Inst Cajal 72:269–278.PubMedGoogle Scholar
  25. Garcia-Verdugo JM, Berbel-Navarro P, Regidor-Garcia J, Lopez-Garcia C (1984) Ultrastructure of neuronal cell bodies in the medial cortex of Lacerta galloti. J Hirnforsch 25:187–196.PubMedGoogle Scholar
  26. Garcia-Verdugo JM, Fariñas I, Molowny A, Lopez-Garcia C (1986a) Ultrastructure of putative migrating cells in the cerebral cortex of Lacerta galloti. J Morphol 189:189–197.PubMedCrossRefGoogle Scholar
  27. Garcia-Verdugo JM, Llahi S, Fariñas I, Martin V (1986b) Laminar organization of the main olfactory bulb of Podarcis hispanica: an electron microscopic and Golgi study. J Hirnforsch 27:87–100.PubMedGoogle Scholar
  28. Garcia-Verdugo JM, Llahi S, Ferrer I, Lopez-Garcia C (1989) Postnatal neurogenesis in the olfactory bulbs of a lizard. A tritiated thymidine autoradiographic study. Neurosci Lett 98:247–252.PubMedCrossRefGoogle Scholar
  29. Garcia-Verdugo JM, Ferron S, Flames N, Collado L, Desfilis E, Font E (2002) The proliferative ventricular zone in adult vertebrates: a comparative study using reptiles, birds, and mammals. Brain Res Bull 57:765–775.PubMedCrossRefGoogle Scholar
  30. Goffinet AM, Daumerie C, Langerwerf B, Pieau C (1986) Neurogenesis in reptilian cortical structures: 3H-thymidine autoradiographic analysis. J Comp Neurol 243:106–116.PubMedCrossRefGoogle Scholar
  31. Gould E, Tanapat P (1997) Lesion-induced proliferation of neuronal progenitors in the dentate gyrus of the adult rat. Neuroscience 80:427–436.PubMedCrossRefGoogle Scholar
  32. Gould E, Tanapat P (1999) Stress and hippocampal neurogenesis. Biol Psychiatry 46:1472–1479.PubMedCrossRefGoogle Scholar
  33. Holtzman DA (1993) The ontogeny of nasal chemical senses in garter snakes. Brain Behav Evol 41:163–170.PubMedCrossRefGoogle Scholar
  34. Holtzman DA, Halpern M (1991) Incorporation of 3H-thymidine in telencephalic structures of the vomeronasal and olfactory systems of embryonic garter snakes. J Comp Neurol 304:450–466.PubMedCrossRefGoogle Scholar
  35. Hoogland PV, Vermeulen-Vanderzee E (1995) Efferent connections of the lateral cortex of the lizard Gekko gecko: evidence for separate origins of medial and lateral pathways from the lateral cortex to the hypothalamus. J Comp Neurol 352:469–480.PubMedCrossRefGoogle Scholar
  36. Hulsebosch CE, Bittner GD (1980) Evolution of abilities to regenerate neurons in central nervous system. Am Nat 115:276–284.CrossRefGoogle Scholar
  37. Johnston JB (1916) Evidence of a motor pallium in the forebrain of reptiles. J Comp Neurol 26:469–480.Google Scholar
  38. Kempermann G (2006) Adult neurogenesis: stem cells and neuronal development in the adult brain. Oxford, New York.Google Scholar
  39. Kirsche W (1983) The significance of matrix zones for brain regeneration and brain transplantation with special consideration of lower vertebrates. In: Wallace RB, Das GD (eds) Neural tissue transplantation research. Springer, Berlin.Google Scholar
  40. Lang DM, Monzon-Mayor M, Bandtlow CE, Stuermer CA (1998) Retinal axon regeneration in the lizard Gallotia galloti in the presence of CNS myelin and oligodendrocytes. Glia 23:61–74.PubMedCrossRefGoogle Scholar
  41. Lang DM, Romero-Aleman MM, Arbelo-Galvan JF, Stuermer CA, Monzon-Mayor M (2002) Regeneration of retinal axons in the lizard Gallotia galloti is not linked to generation of new retinal ganglion cells. J Neurobiol 52:322–335.PubMedCrossRefGoogle Scholar
  42. Lois C, Alvarez-Buylla A (1994) Long-distance neuronal migration in the adult mammalian brain. Science 264:1145–1148.PubMedCrossRefGoogle Scholar
  43. Lopez-Garcia C (1993) Postnatal neurogenesis and regeneration in the lizard cerebral cortex. In: Cuello AC (ed) Restorative neurology. Elsevier, Amsterdam.Google Scholar
  44. Lopez-Garcia C, Martinez-Guijarro FJ (1988) Neurons in the medial cortex give rise to Timm-positive boutons in the cerebral cortex of lizards. Brain Res 463:205–217.PubMedCrossRefGoogle Scholar
  45. Lopez-Garcia C, Tineo PL, Del Corral J (1984) Increase of the neuron number in some cerebral cortical areas of a lizard, Podarcis hispanica, (Steind., 1870), during postnatal periods of life. J Hirnforsch 25:255–259.Google Scholar
  46. Lopez-Garcia C, Molowny A, Garcia-Verdugo JM, Ferrer I (1988a) Delayed postnatal neurogenesis in the cerebral cortex of lizards. Brain Res 471:167–174.PubMedGoogle Scholar
  47. Lopez-Garcia C, Molowny A, Rodriguez-Serna R, Garcia Verdugo JM, Martinez-Guijarro FJ (1988b) Postnatal development of neurons in the telencephalic cortex of lizards. In: Schwerdtfeger WK, Smeets WJAJ (eds) The forebrain of reptiles: Current concepts of structure and function. Karger, Basel.Google Scholar
  48. Lopez-Garcia C, Molowny A, Garcia-Verdugo JM, Martinez-Guijarro FJ, Bernabeu A (1990a) Late generated neurons in the medial cortex of adult lizards send axons that reach the Timm-reactive zones. Brain Res Dev Brain Res 57:249–254.PubMedCrossRefGoogle Scholar
  49. Lopez-Garcia C, Molowny A, Garcia-Verdugo JM, Perez-Sanchez F, Martinez-Guijarro FJ (1990b) Postnatal neurogenesis in the brain of the lizard Podarcis hispanica. In: Schwerdtfeger WK, Germroth P (eds) The forebrain in nonmammals: New aspects of structure and development. Springer, Berlin.Google Scholar
  50. Lopez-Garcia C, Molowny A, Martinez-Guijarro FJ, Blasco-Ibanez JM, Luis de la Iglesia JA, Bernabeu A, Garcia-Verdugo JM (1992) Lesion and regeneration in the medial cerebral cortex of lizards. Histol Histopathol 7:725–746.PubMedGoogle Scholar
  51. Lopez-Garcia C, Nacher J, Castellano B, Luis de la Iglesia JA, Molowny A (1994) Transitory disappearance of microglia during the regeneration of the lizard medial cortex. Glia 12:52–61.PubMedCrossRefGoogle Scholar
  52. Luis de la Iglesia JA, Lopez-Garcia C (1997a) A Golgi study of the short-axon interneurons of the cell layer and inner plexiform layer of the medial cortex of the lizard Podarcis hispanica. J Comp Neurol 385:565–598.PubMedCrossRefGoogle Scholar
  53. Luis de la Iglesia JA, Lopez-Garcia C (1997b) A Golgi study of the principal projection neurons of the medial cortex of the lizard Podarcis hispanica. J Comp Neurol 385:528–564.PubMedCrossRefGoogle Scholar
  54. Marchioro M, Nunes JM, Ramalho AM, Molowny A, Perez-Martinez E, Ponsoda X, Lopez-Garcia C (2005) Postnatal neurogenesis in the medial cortex of the tropical lizard Tropidurus hispidus. Neuroscience 134:407–413.PubMedCrossRefGoogle Scholar
  55. Margotta V, Morelli A (1996) Encephalic matrix areas and post-natal neurogenesis under natural and experimental conditions. Anim Biol 5:117–131.Google Scholar
  56. Martinez-Garcia F, Amiguet M, Olucha F, Lopez-Garcia C (1986) Connections of the lateral cortex in the lizard Podarcis hispanica. Neurosci Lett 63:39–44.PubMedCrossRefGoogle Scholar
  57. Martinez-Garcia F, Amiguet M, Schwerdfeger WK (1990) Interhemispheric connections through the pallial commissures in the brain of Podarcis hispanica and Gallotia-Stehlinii (Reptilia, Lacertidae). J Morphol 205:17–31.Google Scholar
  58. Martinez-Garcia F, Martinez-Marcos A, Lanuza E (2002) The pallial amygdala of amniote vertebrates: evolution of the concept, evolution of the structure. Brain Res Bull 57:463–469.PubMedCrossRefGoogle Scholar
  59. Martinez-Guijarro FJ, Soriano E, Del Rio JA, Lopez-Garcia C (1991) Zinc-positive boutons in the cerebral cortex of lizards show glutamate immunoreactivity. J Neurocytol 20:834–843.PubMedCrossRefGoogle Scholar
  60. Minelli G, del Grande P, Mambelli MC (1977) Preliminary study of the regenerative processes of the dorsal cortex of the telencephalon of Lacerta viridis. Z Mikrosk Anat Forsch 91:241–256.PubMedGoogle Scholar
  61. Minelli G, Franceschini V, Del Grande P, Ciani F (1987) Newly-formed neurons in the regenerating optic tectum of Triturus cristatus carnifex. Basic Appl Histochem 31:43–52.PubMedGoogle Scholar
  62. Molowny A, Nacher J, Lopez-Garcia C (1995) Reactive neurogenesis during regeneration of the lesioned medial cerebral cortex of lizards. Neuroscience 68:823–836.PubMedCrossRefGoogle Scholar
  63. Monzon-Mayor M, Yanes C, Tholey G, De Barry J, Gombos G (1990) Immunohistochemical localization of glutamine synthetase in mesencephalon and telencephalon of the lizard Gallotia galloti during ontogeny. Glia 3:81–97.PubMedCrossRefGoogle Scholar
  64. Nacher J, Ramirez C, Palop JJ, Molowny A, Luis de la Iglesia JA, Lopez-Garcia C (1999a) Radial glia and cell debris removal during lesion-regeneration of the lizard medial cortex. Histol Histopathol 14:89–101.PubMedGoogle Scholar
  65. Nacher J, Ramirez C, Palop JJ, Artal P, Molowny A, Lopez-Garcia C (1999b) Microglial cells during the lesion-regeneration of the lizard medial cortex. Histol Histopathol 14:103–117.PubMedGoogle Scholar
  66. Nacher J, Soriano S, Varea E, Molowny A, Ponsoda X, Lopez-Garcia C (2002) CRMP-4 expression in the adult cerebral cortex and other telencephalic areas of the lizard Podarcis hispanica. Brain Res Dev Brain Res 139:285–294.PubMedCrossRefGoogle Scholar
  67. O’Rourke NA, Sullivan DP, Kaznowski CE, Jacobs AA, McConnell SK (1995) Tangential migration of neurons in the developing cerebral cortex. Development 121:2165–2176.Google Scholar
  68. Peñafiel A, Gutierrez A, Martin R, Perez-Cañellas MM, de la Calle A (1996) A tangential neuronal migration in the olfactory bulbs of adult lizards. Neuroreport 7:1257–1260.PubMedCrossRefGoogle Scholar
  69. Perez-Cañellas MM, Garcia-Verdugo JM (1996) Adult neurogenesis in the telencephalon of a lizard: a [3H]thymidine autoradiographic and bromodeoxyuridine immunocytochemical study. Brain Res Dev Brain Res 93:49–61.PubMedCrossRefGoogle Scholar
  70. Perez-Cañellas MM, Font E, Garcia-Verdugo JM (1997) Postnatal neurogenesis in the telencephalon of turtles: evidence for nonradial migration of new neurons from distant proliferative ventricular zones to the olfactory bulbs. Brain Res Dev Brain Res 101:125–137.PubMedCrossRefGoogle Scholar
  71. Perez-Sanchez F, Molowny A, Garcia-Verdugo JM, Lopez-Garcia C (1989) Postnatal neurogenesis in the nucleus sphericus of the lizard, Podarcis hispanica. Neurosci Lett 106:71–75.PubMedCrossRefGoogle Scholar
  72. Rakic P (1971) Guidance of neurons migrating to the fetal monkey neocortex. Brain Res 33:471–476.PubMedCrossRefGoogle Scholar
  73. Ramirez C, Nacher J, Molowny A, Sanchez-Sanchez F, Irurzun A, Lopez-Garcia C (1997) Photoperiod-temperature and neuroblast proliferation-migration in the adult lizard cortex. Neuroreport 8:2337–2342.PubMedCrossRefGoogle Scholar
  74. Ramirez-Castillejo C, Nacher J, Molowny A, Ponsoda X, Lopez-Garcia C (2002) PSA-NCAM immunocytochemistry in the cerebral cortex and other telencephalic areas of the lizard Podarcis hispanica: differential expression during medial cortex neuronal regeneration. J Comp Neurol 453:145–156.PubMedCrossRefGoogle Scholar
  75. Romero-Aleman MM, Monzon-Mayor M, Yanes C, Lang D (2004) Radial glial cells, proliferating periventricular cells, and microglia might contribute to successful structural repair in the cerebral cortex of the lizard Gallotia galloti. Exp Neurol 188:74–85.PubMedCrossRefGoogle Scholar
  76. Scharff C, Kirn JR, Grossman M, Macklis JD, Nottebohm F (2000) Targeted neuronal death affects neuronal replacement and vocal behavior in adult songbirds. Neuron 25:481–492.PubMedCrossRefGoogle Scholar
  77. Seri B, Garcia-Verdugo JM, McEwen BS, Alvarez-Buylla A (2001) Astrocytes give rise to new neurons in the adult mammalian hippocampus. J Neurosci 21:7153–7160.PubMedGoogle Scholar
  78. Simpson SB, Jr., Duffy MT (1994) The lizard spinal cord: a model system for the study of spinal cord injury and repair. Prog Brain Res 103:229–241.PubMedCrossRefGoogle Scholar
  79. Stensaas LJ, Stensaas SS (1968) Light microscopy of glial cells in turtles and birds. Z Zellforsch Mikrosk Anat 91:315–340.PubMedCrossRefGoogle Scholar
  80. Striedter GF (1997) The telencephalon of tetrapods in evolution. Brain Behav Evol 49:179–213.PubMedCrossRefGoogle Scholar
  81. Tineo PL, Planelles MD, Del-Corral J (1987) Modifications in cortical ependyma of the lizard, Podarcis hispanica, during postnatal development. J Hirnforsch 28:485–489.PubMedGoogle Scholar
  82. Ulinski PS (1990) The cerebral cortex of reptiles. In: Jones EG, Peters A (eds) Cerebral cortex. Plenum, New York.Google Scholar
  83. Ulinski PS, Kanarek DA (1973) Cytoarchitecture of nucleus sphericus in the common boa, Constrictor constrictor. J Comp Neurol 151:159–174.PubMedCrossRefGoogle Scholar
  84. Yanes-Mendez C, Martin-Trujillo JM, Perez-Batista MA, Mozon-Mayor M, Marrero A (1988) Ependymogenesis of the lizard basal areas. I. Ependymal zones. Z Mikrosk Anat Forsch 102:555–572.Google Scholar
  85. Zupanc GK, Ott R (1999) Cell proliferation after lesions in the cerebellum of adult teleost fish: time course, origin, and type of new cells produced. Exp Neurol 160:78–87.PubMedCrossRefGoogle Scholar

Copyright information

© Springer 2011

Authors and Affiliations

  • Susana González-Granero
    • 1
  • Melissa Lezameta
    • 1
  • José Manuel García-Verdugo
    • 1
    • 2
    • 3
    Email author
  1. 1.Unidad de Neurobiología Comparada, Instituto Cavanilles de Biodiversidad y Biología EvolutivaUniversidad de ValenciaPaternaSpain
  2. 2.Laboratorio de Morfología CelularCentro de Investigación Príncipe FelipeValenciaSpain
  3. 3.CIBERNEDMadridSpain

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